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Okumura T, Saito K, Harada R, Ohki T, Hanihara H, Kida I. Latent preference representation in the human brain for scented products: Effects of novelty and familiarity. Neuroimage 2025; 310:121131. [PMID: 40058534 DOI: 10.1016/j.neuroimage.2025.121131] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/30/2024] [Revised: 03/03/2025] [Accepted: 03/06/2025] [Indexed: 03/20/2025] Open
Abstract
Decoding latent preferences for novel products is crucial for understanding decision-making processes, especially when subjective evaluations are unclear. Brain activity in regions like the medial orbitofrontal cortex and nucleus accumbens (NAcc) correlates with subjective preferences. However, whether these regions represent preferences toward novel products and whether coding persists after familiarity remain unclear. We examined the brain coding of latent preferences for novel scented products and how they evolve with familiarity. We measured functional magnetic resonance imaging (fMRI) signals evoked by three fabric softener odors, both when novel and when familiar, in 25 previously unexposed females. To obtain reliable preferences, participants chose one softener after using all three twice at home after the first fMRI measurement (Day 1) and continued using it at home for four months until the second day of the fMRI measurement (Day 2). Subjective ratings were also obtained after each fMRI run. On Day 1, no significant differences in subjective ratings between selected and non-selected odors were found. However, the decoding analysis revealed that future odor preferences for novel products were coded in several regions, including the left superior frontal lobe (SF), right NAcc, and left piriform cortex. On Day 2, the left SF continued to encode preferences after familiarity. These results suggest that odor preferences for novel products are coded in the brain even without conscious awareness, and that the coding in the SF is robust against familiarity. These findings provide insights into a more comprehensive understanding of the brain coding of latent preferences.
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Affiliation(s)
- Toshiki Okumura
- Center for Information and Neural Networks (CiNet), National Institute of Information and Communications Technology (NICT), Osaka, Japan, 1-4 Yamadaoka, Suita-shi, Osaka, 565-0871, Japan
| | - Kai Saito
- Research and Development Headquarters, LION Corporation, Tokyo, Japan, 1-3-28 Kuramae, Taitou-ku, Tokyo, 111-8644, Japan
| | - Risako Harada
- Research and Development Headquarters, LION Corporation, Tokyo, Japan, 1-3-28 Kuramae, Taitou-ku, Tokyo, 111-8644, Japan
| | - Tohru Ohki
- Research and Development Headquarters, LION Corporation, Tokyo, Japan, 1-3-28 Kuramae, Taitou-ku, Tokyo, 111-8644, Japan
| | - Hiroyuki Hanihara
- Research and Development Headquarters, LION Corporation, Tokyo, Japan, 1-3-28 Kuramae, Taitou-ku, Tokyo, 111-8644, Japan
| | - Ikuhiro Kida
- Center for Information and Neural Networks (CiNet), National Institute of Information and Communications Technology (NICT), Osaka, Japan, 1-4 Yamadaoka, Suita-shi, Osaka, 565-0871, Japan.
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2
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Jang G, Kragel PA. Understanding human amygdala function with artificial neural networks. J Neurosci 2025; 45:e1436242025. [PMID: 40086868 PMCID: PMC12044042 DOI: 10.1523/jneurosci.1436-24.2025] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/29/2024] [Revised: 01/07/2025] [Accepted: 01/16/2025] [Indexed: 03/16/2025] Open
Abstract
The amygdala is a cluster of subcortical nuclei that receives diverse sensory inputs and projects to the cortex, midbrain, and other subcortical structures. Numerous accounts of amygdalar contributions to social and emotional behavior have been offered, yet an overarching description of amygdala function remains elusive. Here we adopt a computationally explicit framework that aims to develop a model of amygdala function based on the types of sensory inputs it receives, rather than individual constructs such as threat, arousal, or valence. Characterizing human fMRI signal acquired as male and female participants viewed a full-length film, we developed encoding models that predict both patterns of amygdala activity and self-reported valence evoked by naturalistic images. We use deep image synthesis to generate artificial stimuli that distinctly engage encoding models of amygdala subregions that systematically differ from one another in terms of their low-level visual properties. These findings characterize how the amygdala compresses high-dimensional sensory inputs into low-dimensional representations relevant for behavior.Significance Statement The amygdala is a cluster of subcortical nuclei critical for motivation, emotion, and social behavior. Characterizing the contribution of the amygdala to behavior has been challenging due to its structural complexity, broad connectivity, and functional heterogeneity. Here we use a combination of human neuroimaging and computational modeling to investigate how visual inputs relate to low-dimensional representations encoded in the amygdala. We find that the amygdala encodes an array of visual features, which systematically vary across specific nuclei and relate to the affective properties of the sensory environment.
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3
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Pirc M, Krale C, Smeets P, Boesveldt S. Perceptual differences in olfactory fat discrimination are not detected in neural activation. Chem Senses 2025; 50:bjaf007. [PMID: 39964953 PMCID: PMC11931621 DOI: 10.1093/chemse/bjaf007] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 04/19/2024] [Indexed: 02/20/2025] Open
Abstract
Olfaction is involved in detecting, identifying, and discriminating dietary fat within foods, yet the underlying neural mechanisms remain uncharted. Our functional magnetic resonance imaging (fMRI) study investigated the neural correlates of olfactory fat perception and their association with discrimination ability in a complex food matrix. We measured brain activation resulting from orthonasal exposure to an ecologically relevant fat-related odor source-dairy milk, manipulated to contain 0%, 3.5%, or 14% fat. Twenty-six healthy, normosmic adults underwent olfactory fat content discrimination testing, followed by an fMRI task during which the 3 odor stimuli were delivered via an olfactometer (25 times/fat level) and rated on perceived intensity and liking. Participants discriminated between all fat levels, with fat level influencing perceived odor intensity and liking. These perceptual differences, however, were not reflected in differential brain activation. Brain activation differences were observed only when comparing odor exposure with no exposure. Specifically, in response to any odor, activation occurred in the anterior part of the supplementary motor area (SMA) while deactivating parts of the hippocampus, putamen, superior temporal gyrus, anterior cingulate cortex, insula, and posterior part of the SMA. Exposure to the 0% fat odor also activated the thalamus. No associations were found between perceived intensity and liking and neural responses. Results reaffirm the human ability to distinguish food fat content using solely olfactory cues and reveal a divergence between sensory perception and neural processing. Subsequent research should replicate and extend these findings onto retronasal fat perception while also examining potential effects of hunger, genetics, and dietary habits.
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Affiliation(s)
- Matjaž Pirc
- Division of Human Nutrition and Health, Wageningen University, Wageningen, The Netherlands
| | - Catoo Krale
- Division of Human Nutrition and Health, Wageningen University, Wageningen, The Netherlands
| | - Paul Smeets
- Division of Human Nutrition and Health, Wageningen University, Wageningen, The Netherlands
| | - Sanne Boesveldt
- Division of Human Nutrition and Health, Wageningen University, Wageningen, The Netherlands
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Dumitru ML, Johnsen E, Kroken RA, Løberg EM, Lilleskare L, Ersland L, Hugdahl K. Widespread asymmetries of amygdala nuclei predict auditory verbal hallucinations in schizophrenia. BMC Psychiatry 2024; 24:826. [PMID: 39563258 DOI: 10.1186/s12888-024-06301-1] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 04/17/2024] [Accepted: 11/14/2024] [Indexed: 11/21/2024] Open
Abstract
BACKGROUND Auditory verbal hallucinations, which frequently involve negative emotions, are reliable symptoms of schizophrenia. Brain asymmetries have also been linked to the condition, but the relevance of asymmetries within the amygdala, which coordinates all emotional signals, to the content of and response to auditory verbal hallucinations has not been explored. METHODS We evaluated the performance of two asymmetry biomarkers that were recently introduced in literature: the distance index, which captures global asymmetries, and a revised version of the laterality index, which captures left-right local asymmetries. We deployed random forest regression models over values computed with the distance index and with the laterality index over amygdala nuclei volumes (lateral, basal, accessory-basal, anterior amygdaloid area, central, medial, cortical, cortico-amygdaloid area, and paralaminar) for 71 patients and 71 age-matched controls. RESULTS Both biomarkers made successful predictions for the 35 items of the revised version of the Belief About Voices Questionnaire, such that hallucination severity increased with increasing local asymmetries and with decreasing global asymmetries of the amygdala. CONCLUSIONS Our findings highlight a global reorganization of the amygdala, where left and right nuclei volumes differ pairwise but become proportionally more similar as hallucinations increase in severity. Identifying asymmetries in particular brain structures relevant to specific symptoms could help monitor the evolution and outcome of psychopathological conditions.
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Affiliation(s)
- Magda L Dumitru
- Department of Biological Sciences, University of Bergen, Thormøhlens Gate 53 A/B, Postboks 5006, Bergen, Norway.
- Department of Biological and Medical Psychology, University of Bergen, Bergen, Norway.
| | - Erik Johnsen
- Division of Psychiatry, Haukeland University Hospital, Bergen, Norway
- NORMENT Centre of Excellence, Haukeland University Hospital, Bergen, Norway
- Institute of Clinical Psychology, University of Bergen, Bergen, Norway
| | - Rune A Kroken
- Division of Psychiatry, Haukeland University Hospital, Bergen, Norway
- NORMENT Centre of Excellence, Haukeland University Hospital, Bergen, Norway
- Institute of Clinical Psychology, University of Bergen, Bergen, Norway
| | - Else-Marie Løberg
- Division of Psychiatry, Haukeland University Hospital, Bergen, Norway
- Institute of Clinical Psychology, University of Bergen, Bergen, Norway
| | - Lin Lilleskare
- Institute of Clinical Psychology, University of Bergen, Bergen, Norway
| | - Lars Ersland
- Department of Biological and Medical Psychology, University of Bergen, Bergen, Norway
- NORMENT Centre of Excellence, Haukeland University Hospital, Bergen, Norway
- Department of Clinical Engineering, Haukeland University Hospital, Bergen, Norway
| | - Kenneth Hugdahl
- Department of Biological and Medical Psychology, University of Bergen, Bergen, Norway
- Division of Psychiatry, Haukeland University Hospital, Bergen, Norway
- Department of Radiology, Haukeland University Hospital, Bergen, Norway
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Mou YK, Song XY, Wang HR, Wang Y, Liu WC, Yang T, Zhang MJ, Hu Y, Ren C, Song XC. Understanding the nose-brain axis and its role in related diseases: A conceptual review. Neurobiol Dis 2024; 202:106690. [PMID: 39389156 DOI: 10.1016/j.nbd.2024.106690] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/14/2024] [Revised: 09/30/2024] [Accepted: 09/30/2024] [Indexed: 10/12/2024] Open
Abstract
The nose-brain axis (NBA), a critical component of the body-brain axis, not only serves as a drug transport route for the treatment of brain diseases but also mediates changes such as neuroimmune disorders, which may be an important mechanism in the occurrence and development of some nasal or brain diseases. Despite its importance, there are substantial gaps that remain in our understanding of the characteristics of NBA-mediated diseases and of the cellular and molecular mechanisms underlying the bidirectional NBA crosstalk. These gaps have limited the translational application of NBA-related research findings to some extent. Therefore, this review aims to address the conceptual framework of NBA and highlight its values in representative diseases by combining existing literature with new research results from our group. We hope that this paper will provide a basis for further in-depth research in this field, and facilitate the clinical translation of NBA.
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Affiliation(s)
- Ya-Kui Mou
- Department of Otorhinolaryngology, Head and Neck Surgery, Yantai Yuhuangding Hospital, Qingdao University, Yantai, China; Shandong Provincial Key Laboratory of Neuroimmune Interaction and Regulation, Yantai Yuhuangding Hospital, Yantai, China; Shandong Provincial Clinical Research Center for Otorhinolaryngologic Diseases, Yantai Yuhuangding Hospital, Yantai, China; Yantai Key Laboratory of Otorhinolaryngologic Diseases, Yantai Yuhuangding Hospital, Yantai, China
| | - Xiao-Yu Song
- Department of Otorhinolaryngology, Head and Neck Surgery, Yantai Yuhuangding Hospital, Qingdao University, Yantai, China; Shandong Provincial Key Laboratory of Neuroimmune Interaction and Regulation, Yantai Yuhuangding Hospital, Yantai, China; Shandong Provincial Clinical Research Center for Otorhinolaryngologic Diseases, Yantai Yuhuangding Hospital, Yantai, China; Yantai Key Laboratory of Otorhinolaryngologic Diseases, Yantai Yuhuangding Hospital, Yantai, China
| | - Han-Rui Wang
- Department of Otorhinolaryngology, Head and Neck Surgery, Yantai Yuhuangding Hospital, Qingdao University, Yantai, China; Shandong Provincial Key Laboratory of Neuroimmune Interaction and Regulation, Yantai Yuhuangding Hospital, Yantai, China; Shandong Provincial Clinical Research Center for Otorhinolaryngologic Diseases, Yantai Yuhuangding Hospital, Yantai, China; Yantai Key Laboratory of Otorhinolaryngologic Diseases, Yantai Yuhuangding Hospital, Yantai, China
| | - Yao Wang
- Department of Otorhinolaryngology, Head and Neck Surgery, Yantai Yuhuangding Hospital, Qingdao University, Yantai, China; Shandong Provincial Key Laboratory of Neuroimmune Interaction and Regulation, Yantai Yuhuangding Hospital, Yantai, China; Shandong Provincial Clinical Research Center for Otorhinolaryngologic Diseases, Yantai Yuhuangding Hospital, Yantai, China; Yantai Key Laboratory of Otorhinolaryngologic Diseases, Yantai Yuhuangding Hospital, Yantai, China
| | - Wan-Chen Liu
- Department of Otorhinolaryngology, Head and Neck Surgery, Yantai Yuhuangding Hospital, Qingdao University, Yantai, China; Shandong Provincial Key Laboratory of Neuroimmune Interaction and Regulation, Yantai Yuhuangding Hospital, Yantai, China; Shandong Provincial Clinical Research Center for Otorhinolaryngologic Diseases, Yantai Yuhuangding Hospital, Yantai, China; Yantai Key Laboratory of Otorhinolaryngologic Diseases, Yantai Yuhuangding Hospital, Yantai, China
| | - Ting Yang
- Department of Otorhinolaryngology, Head and Neck Surgery, Yantai Yuhuangding Hospital, Qingdao University, Yantai, China; Shandong Provincial Key Laboratory of Neuroimmune Interaction and Regulation, Yantai Yuhuangding Hospital, Yantai, China; Shandong Provincial Clinical Research Center for Otorhinolaryngologic Diseases, Yantai Yuhuangding Hospital, Yantai, China; Yantai Key Laboratory of Otorhinolaryngologic Diseases, Yantai Yuhuangding Hospital, Yantai, China
| | - Ming-Jun Zhang
- Department of Otorhinolaryngology, Head and Neck Surgery, Yantai Yuhuangding Hospital, Qingdao University, Yantai, China; Shandong Provincial Key Laboratory of Neuroimmune Interaction and Regulation, Yantai Yuhuangding Hospital, Yantai, China; Shandong Provincial Clinical Research Center for Otorhinolaryngologic Diseases, Yantai Yuhuangding Hospital, Yantai, China; Yantai Key Laboratory of Otorhinolaryngologic Diseases, Yantai Yuhuangding Hospital, Yantai, China
| | - Yue Hu
- Department of Otorhinolaryngology, Head and Neck Surgery, Yantai Yuhuangding Hospital, Qingdao University, Yantai, China; Shandong Provincial Key Laboratory of Neuroimmune Interaction and Regulation, Yantai Yuhuangding Hospital, Yantai, China; Shandong Provincial Clinical Research Center for Otorhinolaryngologic Diseases, Yantai Yuhuangding Hospital, Yantai, China; Yantai Key Laboratory of Otorhinolaryngologic Diseases, Yantai Yuhuangding Hospital, Yantai, China
| | - Chao Ren
- Department of Otorhinolaryngology, Head and Neck Surgery, Yantai Yuhuangding Hospital, Qingdao University, Yantai, China; Shandong Provincial Key Laboratory of Neuroimmune Interaction and Regulation, Yantai Yuhuangding Hospital, Yantai, China; Shandong Provincial Clinical Research Center for Otorhinolaryngologic Diseases, Yantai Yuhuangding Hospital, Yantai, China; Yantai Key Laboratory of Otorhinolaryngologic Diseases, Yantai Yuhuangding Hospital, Yantai, China; Department of Neurology, Yantai Yuhuangding Hospital, Qingdao University, Yantai, China.
| | - Xi-Cheng Song
- Department of Otorhinolaryngology, Head and Neck Surgery, Yantai Yuhuangding Hospital, Qingdao University, Yantai, China; Shandong Provincial Key Laboratory of Neuroimmune Interaction and Regulation, Yantai Yuhuangding Hospital, Yantai, China; Shandong Provincial Clinical Research Center for Otorhinolaryngologic Diseases, Yantai Yuhuangding Hospital, Yantai, China; Yantai Key Laboratory of Otorhinolaryngologic Diseases, Yantai Yuhuangding Hospital, Yantai, China.
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6
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Kehl MS, Mackay S, Ohla K, Schneider M, Borger V, Surges R, Spehr M, Mormann F. Single-neuron representations of odours in the human brain. Nature 2024; 634:626-634. [PMID: 39385026 PMCID: PMC11485236 DOI: 10.1038/s41586-024-08016-5] [Citation(s) in RCA: 1] [Impact Index Per Article: 1.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 11/27/2023] [Accepted: 09/04/2024] [Indexed: 10/11/2024]
Abstract
Olfaction is a fundamental sensory modality that guides animal and human behaviour1,2. However, the underlying neural processes of human olfaction are still poorly understood at the fundamental-that is, the single-neuron-level. Here we report recordings of single-neuron activity in the piriform cortex and medial temporal lobe in awake humans performing an odour rating and identification task. We identified odour-modulated neurons within the piriform cortex, amygdala, entorhinal cortex and hippocampus. In each of these regions, neuronal firing accurately encodes odour identity. Notably, repeated odour presentations reduce response firing rates, demonstrating central repetition suppression and habituation. Different medial temporal lobe regions have distinct roles in odour processing, with amygdala neurons encoding subjective odour valence, and hippocampal neurons predicting behavioural odour identification performance. Whereas piriform neurons preferably encode chemical odour identity, hippocampal activity reflects subjective odour perception. Critically, we identify that piriform cortex neurons reliably encode odour-related images, supporting a multimodal role of the human piriform cortex. We also observe marked cross-modal coding of both odours and images, especially in the amygdala and piriform cortex. Moreover, we identify neurons that respond to semantically coherent odour and image information, demonstrating conceptual coding schemes in olfaction. Our results bridge the long-standing gap between animal models and non-invasive human studies and advance our understanding of odour processing in the human brain by identifying neuronal odour-coding principles, regional functional differences and cross-modal integration.
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Affiliation(s)
- Marcel S Kehl
- Department of Epileptology, University Hospital Bonn, Bonn, Germany
- Department of Experimental Psychology, University of Oxford, Oxford, UK
| | - Sina Mackay
- Department of Epileptology, University Hospital Bonn, Bonn, Germany
| | - Kathrin Ohla
- Science & Research, dsm-firmenich, Satigny, Switzerland
| | | | - Valeri Borger
- Department of Neurosurgery, University Hospital Bonn, Bonn, Germany
| | - Rainer Surges
- Department of Epileptology, University Hospital Bonn, Bonn, Germany
| | - Marc Spehr
- Department of Chemosensation, Institute for Biology II, RWTH Aachen University, Aachen, Germany.
| | - Florian Mormann
- Department of Epileptology, University Hospital Bonn, Bonn, Germany.
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Yao F, Chang X, Zhou B, Zhou W. Olfaction modulates cortical arousal independent of perceived odor intensity and pleasantness. Neuroimage 2024; 299:120843. [PMID: 39251115 DOI: 10.1016/j.neuroimage.2024.120843] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/02/2024] [Revised: 08/22/2024] [Accepted: 09/06/2024] [Indexed: 09/11/2024] Open
Abstract
Throughout history, various odors have been harnessed to invigorate or relax the mind. The mechanisms underlying odors' diverse arousal effects remain poorly understood. We conducted five experiments (184 participants) to investigate this issue, using pupillometry, electroencephalography, and the attentional blink paradigm, which exemplifies the limit in attentional capacity. Results demonstrated that exposure to citral, compared to vanillin, enlarged pupil size, reduced resting-state alpha oscillations and alpha network efficiency, augmented beta-gamma oscillations, and enhanced the coordination between parietal alpha and frontal beta-gamma activities. In parallel, it attenuated the attentional blink effect. These effects were observed despite citral and vanillin being comparable in perceived odor intensity, pleasantness, and nasal pungency, and were unlikely driven by semantic biases. Our findings reveal that odors differentially alter the small-worldness of brain network architecture, and thereby brain state and arousal. Furthermore, they establish arousal as a unique dimension in olfactory space, distinct from intensity and pleasantness.
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Affiliation(s)
- Fangshu Yao
- State Key Laboratory of Brain and Cognitive Science, Institute of Psychology, Chinese Academy of Sciences, Beijing 100101, China; Department of Psychology, University of Chinese Academy of Sciences, Beijing 100049, China; School of Psychology, Shanghai University of Sport, Shanghai 200438, China
| | - Xiaoyue Chang
- State Key Laboratory of Brain and Cognitive Science, Institute of Psychology, Chinese Academy of Sciences, Beijing 100101, China; Department of Psychology, University of Chinese Academy of Sciences, Beijing 100049, China
| | - Bin Zhou
- State Key Laboratory of Brain and Cognitive Science, Institute of Psychology, Chinese Academy of Sciences, Beijing 100101, China; Department of Psychology, University of Chinese Academy of Sciences, Beijing 100049, China.
| | - Wen Zhou
- State Key Laboratory of Brain and Cognitive Science, Institute of Psychology, Chinese Academy of Sciences, Beijing 100101, China; Department of Psychology, University of Chinese Academy of Sciences, Beijing 100049, China; Chinese Institute for Brain Research, Beijing 102206, China.
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8
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Jang G, Kragel PA. Understanding human amygdala function with artificial neural networks. BIORXIV : THE PREPRINT SERVER FOR BIOLOGY 2024:2024.07.29.605621. [PMID: 39131372 PMCID: PMC11312467 DOI: 10.1101/2024.07.29.605621] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Grants] [Track Full Text] [Download PDF] [Subscribe] [Scholar Register] [Indexed: 08/13/2024]
Abstract
The amygdala is a cluster of subcortical nuclei that receives diverse sensory inputs and projects to the cortex, midbrain and other subcortical structures. Numerous accounts of amygdalar contributions to social and emotional behavior have been offered, yet an overarching description of amygdala function remains elusive. Here we adopt a computationally explicit framework that aims to develop a model of amygdala function based on the types of sensory inputs it receives, rather than individual constructs such as threat, arousal, or valence. Characterizing human fMRI signal acquired as participants viewed a full-length film, we developed encoding models that predict both patterns of amygdala activity and self-reported valence evoked by naturalistic images. We use deep image synthesis to generate artificial stimuli that distinctly engage encoding models of amygdala subregions that systematically differ from one another in terms of their low-level visual properties. These findings characterize how the amygdala compresses high-dimensional sensory inputs into low-dimensional representations relevant for behavior.
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9
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Zou L, Qi Y, Shen L, Huang Y, Huang J, Xia Z, Fan M, Fan W, Chai GB, Shi QZ, Zhang Q, Yan C. The neural representations of valence transformation in indole processing. Cereb Cortex 2024; 34:bhae167. [PMID: 38652554 DOI: 10.1093/cercor/bhae167] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/16/2024] [Revised: 03/18/2024] [Accepted: 03/20/2024] [Indexed: 04/25/2024] Open
Abstract
Indole is often associated with a sweet and floral odor typical of jasmine flowers at low concentrations and an unpleasant, animal-like odor at high concentrations. However, the mechanism whereby the brain processes this opposite valence of indole is not fully understood yet. In this study, we aimed to investigate the neural mechanisms underlying indole valence encoding in conversion and nonconversion groups using the smelling task to arouse pleasantness. For this purpose, 12 conversion individuals and 15 nonconversion individuals participated in an event-related functional magnetic resonance imaging paradigm with low (low-indole) and high (high-indole) indole concentrations in which valence was manipulated independent of intensity. The results of this experiment showed that neural activity in the right amygdala, orbitofrontal cortex and insula was associated with valence independent of intensity. Furthermore, activation in the right orbitofrontal cortex in response to low-indole was positively associated with subjective pleasantness ratings. Conversely, activation in the right insula and amygdala in response to low-indole was positively correlated with anticipatory hedonic traits. Interestingly, while amygdala activation in response to high-indole also showed a positive correlation with these hedonic traits, such correlation was observed solely with right insula activation in response to high-indole. Additionally, activation in the right amygdala in response to low-indole was positively correlated with consummatory pleasure and hedonic traits. Regarding olfactory function, only activation in the right orbitofrontal cortex in response to high-indole was positively correlated with olfactory identification, whereas activation in the insula in response to low-indole was negatively correlated with the level of self-reported olfactory dysfunction. Based on these findings, valence transformation of indole processing in the right orbitofrontal cortex, insula, and amygdala may be associated with individual hedonic traits and perceptual differences.
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Affiliation(s)
- Laiquan Zou
- Chemical Senses and Mental Health Lab, Department of Psychology, School of Public Health, Southern Medical University, South Shatai Road 1023, Guangzhou 510515, China
| | - Yue Qi
- Chemical Senses and Mental Health Lab, Department of Psychology, School of Public Health, Southern Medical University, South Shatai Road 1023, Guangzhou 510515, China
| | - Lei Shen
- Key Laboratory of Brain Functional Genomics (MOE & STCSM), Shanghai Changning-ECNU Mental Health Center, School of Psychology and Cognitive Science, East China Normal University, North Zhongshan Road 3663, Shanghai 200062, China
- Shanghai Key Laboratory of Magnetic Resonance, East China Normal University, North Zhongshan Road 3663, Shanghai 20062, China
| | - Yanyang Huang
- Chemical Senses and Mental Health Lab, Department of Psychology, School of Public Health, Southern Medical University, South Shatai Road 1023, Guangzhou 510515, China
| | - Jiayu Huang
- Chemical Senses and Mental Health Lab, Department of Psychology, School of Public Health, Southern Medical University, South Shatai Road 1023, Guangzhou 510515, China
| | - Zheng Xia
- Key Laboratory of Brain Functional Genomics (MOE & STCSM), Shanghai Changning-ECNU Mental Health Center, School of Psychology and Cognitive Science, East China Normal University, North Zhongshan Road 3663, Shanghai 200062, China
- Shanghai Key Laboratory of Magnetic Resonance, East China Normal University, North Zhongshan Road 3663, Shanghai 20062, China
| | - Mingxia Fan
- Key Laboratory of Brain Functional Genomics (MOE & STCSM), Shanghai Changning-ECNU Mental Health Center, School of Psychology and Cognitive Science, East China Normal University, North Zhongshan Road 3663, Shanghai 200062, China
| | - Wu Fan
- Zhengzhou Tobacco Research Institute of CNTC, Fengyang Road 2, Zhengzhou 450001, China
| | - Guo-Bi Chai
- Zhengzhou Tobacco Research Institute of CNTC, Fengyang Road 2, Zhengzhou 450001, China
| | - Qing-Zhao Shi
- Zhengzhou Tobacco Research Institute of CNTC, Fengyang Road 2, Zhengzhou 450001, China
| | - Qidong Zhang
- Zhengzhou Tobacco Research Institute of CNTC, Fengyang Road 2, Zhengzhou 450001, China
| | - Chao Yan
- Key Laboratory of Brain Functional Genomics (MOE & STCSM), Shanghai Changning-ECNU Mental Health Center, School of Psychology and Cognitive Science, East China Normal University, North Zhongshan Road 3663, Shanghai 200062, China
- Shanghai Key Laboratory of Magnetic Resonance, East China Normal University, North Zhongshan Road 3663, Shanghai 20062, China
- Key Laboratory of Philosophy and Social Science of Anhui Province on Adolescent Mental Health and Crisis Intelligence Intervention, South Jiuhua Road 189, Hefei 241002, China
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Liu D, Lu J, Wei L, Yao M, Yang H, Lv P, Wang H, Zhu Y, Zhu Z, Zhang X, Chen J, Yang QX, Zhang B. Olfactory deficit: a potential functional marker across the Alzheimer's disease continuum. Front Neurosci 2024; 18:1309482. [PMID: 38435057 PMCID: PMC10907997 DOI: 10.3389/fnins.2024.1309482] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/08/2023] [Accepted: 02/02/2024] [Indexed: 03/05/2024] Open
Abstract
Alzheimer's disease (AD) is a prevalent form of dementia that affects an estimated 32 million individuals globally. Identifying early indicators is vital for screening at-risk populations and implementing timely interventions. At present, there is an urgent need for early and sensitive biomarkers to screen individuals at risk of AD. Among all sensory biomarkers, olfaction is currently one of the most promising indicators for AD. Olfactory dysfunction signifies a decline in the ability to detect, identify, or remember odors. Within the spectrum of AD, impairment in olfactory identification precedes detectable cognitive impairments, including mild cognitive impairment (MCI) and even the stage of subjective cognitive decline (SCD), by several years. Olfactory impairment is closely linked to the clinical symptoms and neuropathological biomarkers of AD, accompanied by significant structural and functional abnormalities in the brain. Olfactory behavior examination can subjectively evaluate the abilities of olfactory identification, threshold, and discrimination. Olfactory functional magnetic resonance imaging (fMRI) can provide a relatively objective assessment of olfactory capabilities, with the potential to become a promising tool for exploring the neural mechanisms of olfactory damage in AD. Here, we provide a timely review of recent literature on the characteristics, neuropathology, and examination of olfactory dysfunction in the AD continuum. We focus on the early changes in olfactory indicators detected by behavioral and fMRI assessments and discuss the potential of these techniques in MCI and preclinical AD. Despite the challenges and limitations of existing research, olfactory dysfunction has demonstrated its value in assessing neurodegenerative diseases and may serve as an early indicator of AD in the future.
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Affiliation(s)
- Dongming Liu
- Department of Radiology, Nanjing Drum Tower Hospital, Affiliated Hospital of Medical School, Nanjing University, Nanjing, China
- Institute of Medical Imaging and Artificial Intelligence, Nanjing University, Nanjing, China
- Medical Imaging Center, The Affiliated Drum Tower Hospital, Medical School of Nanjing University, Nanjing, China
| | - Jiaming Lu
- Department of Radiology, Nanjing Drum Tower Hospital, Affiliated Hospital of Medical School, Nanjing University, Nanjing, China
- Institute of Medical Imaging and Artificial Intelligence, Nanjing University, Nanjing, China
- Medical Imaging Center, The Affiliated Drum Tower Hospital, Medical School of Nanjing University, Nanjing, China
| | - Liangpeng Wei
- Department of Radiology, Nanjing Drum Tower Hospital, Affiliated Hospital of Medical School, Nanjing University, Nanjing, China
- Institute of Medical Imaging and Artificial Intelligence, Nanjing University, Nanjing, China
- Medical Imaging Center, The Affiliated Drum Tower Hospital, Medical School of Nanjing University, Nanjing, China
| | - Mei Yao
- Department of Radiology, Nanjing Drum Tower Hospital, Affiliated Hospital of Medical School, Nanjing University, Nanjing, China
- Institute of Medical Imaging and Artificial Intelligence, Nanjing University, Nanjing, China
- Medical Imaging Center, The Affiliated Drum Tower Hospital, Medical School of Nanjing University, Nanjing, China
| | - Huiquan Yang
- Department of Radiology, Nanjing Drum Tower Hospital, Affiliated Hospital of Medical School, Nanjing University, Nanjing, China
- Institute of Medical Imaging and Artificial Intelligence, Nanjing University, Nanjing, China
- Medical Imaging Center, The Affiliated Drum Tower Hospital, Medical School of Nanjing University, Nanjing, China
| | - Pin Lv
- Department of Radiology, Nanjing Drum Tower Hospital, Affiliated Hospital of Medical School, Nanjing University, Nanjing, China
- Institute of Medical Imaging and Artificial Intelligence, Nanjing University, Nanjing, China
- Medical Imaging Center, The Affiliated Drum Tower Hospital, Medical School of Nanjing University, Nanjing, China
| | - Haoyao Wang
- Department of Radiology, Nanjing Drum Tower Hospital, Affiliated Hospital of Medical School, Nanjing University, Nanjing, China
- Institute of Medical Imaging and Artificial Intelligence, Nanjing University, Nanjing, China
- Medical Imaging Center, The Affiliated Drum Tower Hospital, Medical School of Nanjing University, Nanjing, China
| | - Yajing Zhu
- Department of Radiology, Nanjing Drum Tower Hospital, Affiliated Hospital of Medical School, Nanjing University, Nanjing, China
| | - Zhengyang Zhu
- Department of Radiology, Nanjing Drum Tower Hospital, Affiliated Hospital of Medical School, Nanjing University, Nanjing, China
| | - Xin Zhang
- Department of Radiology, Nanjing Drum Tower Hospital, Affiliated Hospital of Medical School, Nanjing University, Nanjing, China
- Institute of Medical Imaging and Artificial Intelligence, Nanjing University, Nanjing, China
- Medical Imaging Center, The Affiliated Drum Tower Hospital, Medical School of Nanjing University, Nanjing, China
| | - Jiu Chen
- Department of Radiology, Nanjing Drum Tower Hospital, Affiliated Hospital of Medical School, Nanjing University, Nanjing, China
- Institute of Medical Imaging and Artificial Intelligence, Nanjing University, Nanjing, China
- Medical Imaging Center, The Affiliated Drum Tower Hospital, Medical School of Nanjing University, Nanjing, China
| | - Qing X. Yang
- Department of Radiology, Center for NMR Research, Penn State University College of Medicine, Hershey, PA, United States
| | - Bing Zhang
- Department of Radiology, Nanjing Drum Tower Hospital, Affiliated Hospital of Medical School, Nanjing University, Nanjing, China
- Institute of Medical Imaging and Artificial Intelligence, Nanjing University, Nanjing, China
- Medical Imaging Center, The Affiliated Drum Tower Hospital, Medical School of Nanjing University, Nanjing, China
- State Key Laboratory of Pharmaceutical Biotechnology, Nanjing University, Nanjing, China
- Jiangsu Key Laboratory of Molecular Medicine, Nanjing, China
- Institute of Brain Science, Nanjing University, Nanjing, China
- Jiangsu Provincial Medical Key Discipline (Laboratory), Nanjing, China
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11
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Ai Y, Hummel T, Nie H, Yang J, Han P. Reduced neural responses to pleasant odor stimuli after acute psychological stress is associated with cortisol reactivity. Neuroimage 2023; 284:120474. [PMID: 38008298 DOI: 10.1016/j.neuroimage.2023.120474] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/21/2023] [Revised: 11/07/2023] [Accepted: 11/23/2023] [Indexed: 11/28/2023] Open
Abstract
Acute stress alters olfactory perception. However, little is known about the neural processing of olfactory stimuli after acute stress exposure and the role of cortisol in such an effect. Here, we used an event-related olfactory fMRI paradigm to investigate brain responses to odors of different valence (unpleasant, pleasant, or neutral) in healthy young adults following an acute stress (Trier Social Stress Test, TSST) induction (N = 22) or a non-stressful resting condition (N = 22). We obtained the odor pleasantness, intensity, and familiarity ratings after the acute stress induction or resting condition. We also measured the participants' perceived stress and salivary cortisol at four time points during the procedure. We found a stress-related decrease in brain activation in response to the pleasant, but not to the neutral or unpleasant odor stimuli in the right piriform cortex extending to the right amygdala, the right orbitofrontal cortex, and the right insula. In addition, activation of clusters within the regions of interest were negatively associated with individual baseline-to-peak increase in salivary cortisol levels after stress. We also found increased functional connectivity between the right piriform cortex and the right insula after stress when the pleasant odor was presented. The strength of the connectivity was positively correlated with increased perceived stress levels immediately after stress exposure. These results provide novel evidence for the effects of acute stress in attenuating the neural processing of a pleasant olfactory stimulus. Together with previous findings, the effect of acute stress on human olfactory perception appears to depend on both the valence and the concentration (e.g., peri-threshold or suprathreshold levels) of odor stimuli.
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Affiliation(s)
- Yun Ai
- Faculty of Psychology, Southwest University, Chongqing, China; MOE Key Laboratory of Cognition and Personality, Southwest University, Chongqing, China
| | - Thomas Hummel
- Interdisciplinary Centre Smell and Taste, Department of Otorhinolaryngology, TU Dresden, Dresden, Germany
| | - Haoyu Nie
- Faculty of Psychology, Southwest University, Chongqing, China
| | - Juan Yang
- Faculty of Psychology, Southwest University, Chongqing, China; MOE Key Laboratory of Cognition and Personality, Southwest University, Chongqing, China
| | - Pengfei Han
- Faculty of Psychology, Southwest University, Chongqing, China; MOE Key Laboratory of Cognition and Personality, Southwest University, Chongqing, China.
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12
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Sagar V, Shanahan LK, Zelano CM, Gottfried JA, Kahnt T. High-precision mapping reveals the structure of odor coding in the human brain. Nat Neurosci 2023; 26:1595-1602. [PMID: 37620443 PMCID: PMC10726579 DOI: 10.1038/s41593-023-01414-4] [Citation(s) in RCA: 11] [Impact Index Per Article: 5.5] [Reference Citation Analysis] [Abstract] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 02/26/2022] [Accepted: 07/18/2023] [Indexed: 08/26/2023]
Abstract
Odor perception is inherently subjective. Previous work has shown that odorous molecules evoke distributed activity patterns in olfactory cortices, but how these patterns map on to subjective odor percepts remains unclear. In the present study, we collected neuroimaging responses to 160 odors from 3 individual subjects (18 h per subject) to probe the neural coding scheme underlying idiosyncratic odor perception. We found that activity in the orbitofrontal cortex (OFC) represents the fine-grained perceptual identity of odors over and above coarsely defined percepts, whereas this difference is less pronounced in the piriform cortex (PirC) and amygdala. Furthermore, the implementation of perceptual encoding models enabled us to predict olfactory functional magnetic resonance imaging responses to new odors, revealing that the dimensionality of the encoded perceptual spaces increases from the PirC to the OFC. Whereas encoding of lower-order dimensions generalizes across subjects, encoding of higher-order dimensions is idiosyncratic. These results provide new insights into cortical mechanisms of odor coding and suggest that subjective olfactory percepts reside in the OFC.
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Affiliation(s)
- Vivek Sagar
- Department of Neurology, Feinberg School of Medicine, Northwestern University, Chicago, IL, USA
| | | | - Christina M Zelano
- Department of Neurology, Feinberg School of Medicine, Northwestern University, Chicago, IL, USA
| | - Jay A Gottfried
- Department of Neurology, University of Pennsylvania, Philadelphia, PA, USA
- Department of Psychology, University of Pennsylvania, Philadelphia, PA, USA
| | - Thorsten Kahnt
- National Institute on Drug Abuse Intramural Research Program, Baltimore, MD, USA.
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13
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Wang L, Li J, Pan Y, Huang P, Li D, Voon V. Subacute alpha frequency (10Hz) subthalamic stimulation for emotional processing in Parkinson's disease. Brain Stimul 2023; 16:1223-1231. [PMID: 37567462 DOI: 10.1016/j.brs.2023.08.005] [Citation(s) in RCA: 5] [Impact Index Per Article: 2.5] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/18/2023] [Revised: 05/21/2023] [Accepted: 08/07/2023] [Indexed: 08/13/2023] Open
Abstract
BACKGROUND Psychiatric comorbidities are common in Parkinson's disease (PD) and may change with high-frequency stimulation targeting the subthalamic nucleus. Numerous accounts indicate subthalamic alpha-frequency oscillation is implicated in emotional processing. While intermittent alpha-frequency (10Hz) stimulation induces positive emotional effects, with more ventromedial contacts inducing larger effects, little is known about the subacute effect of ventral 10Hz subthalamic stimulation on emotional processing. OBJECTIVE/HYPOTHESIS To evaluate the subacute effect of 10Hz stimulation at bilateral ventral subthalamic nucleus on emotional processing in PD patients using an affective task, compared to that of clinical-frequency stimulation and off-stimulation. METHODS Twenty PD patients with bilateral subthalamic deep brain stimulation for more than six months were tested with the affective task under three stimulation conditions (10Hz, 130Hz, and off-stimulation) in a double-blinded randomized design. RESULTS While 130Hz stimulation reduced arousal ratings in all patients, 10Hz stimulation increased arousal selectively in patients with higher depression scores. Furthermore, 10Hz stimulation induced a positive shift in valence rating to negative emotional stimuli in patients with lower apathy scores, and 130Hz stimulation led to more positive valence to emotional stimuli in the patients with higher apathy scores. Notably, we found correlational relationships between stimulation site and affective rating: arousal ratings increase with stimulation from anterior to posterior site, and positive valence ratings increase with stimulation from dorsal to ventral site of the ventral subthalamic nucleus. CONCLUSIONS Our findings highlight the distinctive role of 10Hz stimulation on subjective emotional experience and unveil the spatial organization of the stimulation effect.
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Affiliation(s)
- Linbin Wang
- Institute of Science and Technology for Brain-Inspired Intelligence (ISTBI), Fudan University, Shanghai, China; Department of Neurosurgery, Center for Functional Neurosurgery, Ruijin Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, China
| | - Jun Li
- School of Information Science and Technology, ShanghaiTech University, Shanghai, China
| | - Yixin Pan
- Department of Neurosurgery, Center for Functional Neurosurgery, Ruijin Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, China
| | - Peng Huang
- Department of Neurosurgery, Center for Functional Neurosurgery, Ruijin Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, China
| | - Dianyou Li
- Department of Neurosurgery, Center for Functional Neurosurgery, Ruijin Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, China.
| | - Valerie Voon
- Institute of Science and Technology for Brain-Inspired Intelligence (ISTBI), Fudan University, Shanghai, China; Department of Psychiatry, University of Cambridge, Cambridge, United Kingdom.
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14
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Chen W. Neural circuits provide insights into reward and aversion. Front Neural Circuits 2022; 16:1002485. [PMID: 36389177 PMCID: PMC9650032 DOI: 10.3389/fncir.2022.1002485] [Citation(s) in RCA: 3] [Impact Index Per Article: 1.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/28/2022] [Accepted: 10/12/2022] [Indexed: 01/07/2023] Open
Abstract
Maladaptive changes in the neural circuits associated with reward and aversion result in some common symptoms, such as drug addiction, anxiety, and depression. Historically, the study of these circuits has been hampered by technical limitations. In recent years, however, much progress has been made in understanding the neural mechanisms of reward and aversion owing to the development of technologies such as cell type-specific electrophysiology, neuronal tracing, and behavioral manipulation based on optogenetics. The aim of this paper is to summarize the latest findings on the mechanisms of the neural circuits associated with reward and aversion in a review of previous studies with a focus on the ventral tegmental area (VTA), nucleus accumbens (NAc), and basal forebrain (BF). These findings may inform efforts to prevent and treat mental illnesses associated with dysfunctions of the brain's reward and aversion system.
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15
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Van Regemorter V, Rombaux P, Dricot L, Kupers R, Grégoire A, Hox V, Huart C. Functional Imaging in Olfactory Disorders. CURRENT OTORHINOLARYNGOLOGY REPORTS 2022; 10:421-426. [PMID: 36276577 PMCID: PMC9579609 DOI: 10.1007/s40136-022-00433-2] [Citation(s) in RCA: 4] [Impact Index Per Article: 1.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Accepted: 09/30/2022] [Indexed: 11/06/2022]
Abstract
Purpose of Review The aim was to synthesize key findings regarding the use of functional MRI (fMRI) to assess olfactory dysfunction (OD), and thus, to evaluate whether fMRI could be a reliable clinical diagnostic tool. Recent Findings In response to olfactory stimulation, patients with quantitative OD display reduced activation in olfactory-related brain regions but also stronger activation in non-olfactory brain areas. Parosmic patients also seem to show both weaker and higher brain signals. As to trigeminal chemosensory system, fMRI suggests that central processing may be declined in patients with OD. Functional connectivity studies report a possible correlation between altered neuronal connections within brain networks and olfactory performances. Summary fMRI emerges as a valuable and promising objective method in OD evaluation. Yet, its high inter-individual variability still precludes its routine clinical use for diagnostic purpose. Future research should focus on optimizing stimulation paradigms and analysis methods.
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Affiliation(s)
- V. Van Regemorter
- Institute of Neuroscience, Université catholique de Louvain, Brussels, Belgium
- Department of Anesthesiology, Cliniques universitaires Saint-Luc, Brussels, Belgium
| | - Ph. Rombaux
- Institute of Neuroscience, Université catholique de Louvain, Brussels, Belgium
- Department of Otorhinolaryngology, Cliniques universitaires Saint-Luc, Brussels, Belgium
| | - L. Dricot
- Institute of Neuroscience, Université catholique de Louvain, Brussels, Belgium
| | - R. Kupers
- Institute of Neuroscience, Université catholique de Louvain, Brussels, Belgium
- School of Optometry, University of Montreal, Montreal, QC Canada
- BRAINlab, University of Copenhagen, Copenhagen, Denmark
| | - A. Grégoire
- Institute of Neuroscience, Université catholique de Louvain, Brussels, Belgium
- Department of Otorhinolaryngology, Cliniques universitaires Saint-Luc, Brussels, Belgium
| | - V. Hox
- Department of Otorhinolaryngology, Cliniques universitaires Saint-Luc, Brussels, Belgium
| | - C. Huart
- Institute of Neuroscience, Université catholique de Louvain, Brussels, Belgium
- Department of Otorhinolaryngology, Cliniques universitaires Saint-Luc, Brussels, Belgium
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16
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Iwaoki H, Nakamura K. Neuronal Encoding of Emotional Valence and Intensity in the Monkey Amygdala. J Neurosci 2022; 42:7615-7623. [PMID: 36658460 PMCID: PMC9546443 DOI: 10.1523/jneurosci.0021-22.2022] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/04/2022] [Revised: 07/22/2022] [Accepted: 08/19/2022] [Indexed: 02/02/2023] Open
Abstract
Neuropsychological and neuroimaging studies have suggested that the primate amygdala plays an essential role in processing the emotional valence and intensity of visual stimuli, which is necessary for determining whether to approach or avoid a stimulus. However, the neuronal mechanisms underlying the evaluation of emotional value remain unknown. In the present study, we trained male macaque monkeys to perform an operant conditioning task in which fractal visual patterns were associated with three different amounts of air puff delivered to the cheek (negative) or liquid reward (positive). After confirming that the monkeys successfully differentiated the emotional valence and intensity of the visual stimuli, we analyzed neuronal responses to the stimuli in the amygdala. Most amygdala neurons conveyed information concerning the emotional valence and/or intensity of the visual stimuli, and the majority of those conveying information about emotional valence responded optimally to negative stimuli. Further, some amygdala neurons conveyed information related to both emotional valence and intensity, whereas a small portion conveyed information related to emotional intensity alone. These results indicate that the primate amygdala encodes both emotional valence and intensity, highlighting its important role in the avoidance of dangerous stimuli and animal survival.SIGNIFICANCE STATEMENT Evaluating the emotional value of visual stimuli is essential for animal survival, especially in primates. Emotional value is estimated from the emotional valence and intensity of stimuli, and evidence indicates that the amygdala is likely to play a major role in processing these types of information. To our knowledge, the current study is the first to examine the responses of neurons in the monkey amygdala to visual stimuli that differ in emotional valence and intensity simultaneously. Our data suggest that the amygdala plays an important role in the evaluation of emotional stimuli and in the decision to escape negative and harmful stimuli.
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Affiliation(s)
- Haruhiko Iwaoki
- Cognitive Neuroscience Section, Primate Research Institute, Kyoto University, Inuyama, Aichi 484-8506, Japan
| | - Katsuki Nakamura
- Cognitive Neuroscience Section, Primate Research Institute, Kyoto University, Inuyama, Aichi 484-8506, Japan
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17
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Kulason S, Ratnanather JT, Miller MI, Kamath V, Hua J, Yang K, Ma M, Ishizuka K, Sawa A. A comparative neuroimaging perspective of olfaction and higher-order olfactory processing: on health and disease. Semin Cell Dev Biol 2022; 129:22-30. [PMID: 34462249 PMCID: PMC9900497 DOI: 10.1016/j.semcdb.2021.08.009] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.3] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/11/2021] [Accepted: 08/18/2021] [Indexed: 02/08/2023]
Abstract
Olfactory dysfunction is often the earliest indicator of disease in a range of neurological and psychiatric disorders. One tempting working hypothesis is that pathological changes in the peripheral olfactory system where the body is exposed to many adverse environmental stressors may have a causal role for the brain alteration. Whether and how the peripheral pathology spreads to more central brain regions may be effectively studied in rodent models, and there is successful precedence in experimental models for Parkinson's disease. It is of interest to study whether a similar mechanism may underlie the pathology of psychiatric illnesses, such as schizophrenia. However, direct comparison between rodent models and humans includes challenges under light of comparative neuroanatomy and experimental methodologies used in these two distinct species. We believe that neuroimaging modality that has been the main methodology of human brain studies may be a useful viewpoint to address and fill the knowledge gap between rodents and humans in this scientific question. Accordingly, in the present review article, we focus on brain imaging studies associated with olfaction in healthy humans and patients with neurological and psychiatric disorders, and if available those in rodents. We organize this review article at three levels: 1) olfactory bulb (OB) and peripheral structures of the olfactory system, 2) primary olfactory cortical and subcortical regions, and 3) associated higher-order cortical regions. This research area is still underdeveloped, and we acknowledge that further validation with independent cohorts may be needed for many studies presented here, in particular those with human subjects. Nevertheless, whether and how peripheral olfactory disturbance impacts brain function is becoming even a hotter topic in the ongoing COVID-19 pandemic, given the risk of long-term changes of mental status associated with olfactory infection of SARS-CoV-2. Together, in this review article, we introduce this underdeveloped but important research area focusing on its implications in neurological and psychiatric disorders, with several pioneered publications.
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Affiliation(s)
- Sue Kulason
- Center for Imaging Science, Johns Hopkins University, Baltimore, MD, USA; Institute for Computational Medicine, Johns Hopkins University, Baltimore, MD, USA; Department of Biomedical Engineering, Johns Hopkins University, Baltimore, MD, USA
| | - J Tilak Ratnanather
- Center for Imaging Science, Johns Hopkins University, Baltimore, MD, USA; Institute for Computational Medicine, Johns Hopkins University, Baltimore, MD, USA; Department of Biomedical Engineering, Johns Hopkins University, Baltimore, MD, USA
| | - Michael I Miller
- Center for Imaging Science, Johns Hopkins University, Baltimore, MD, USA; Institute for Computational Medicine, Johns Hopkins University, Baltimore, MD, USA; Department of Biomedical Engineering, Johns Hopkins University, Baltimore, MD, USA
| | - Vidyulata Kamath
- Department of Psychiatry, Johns Hopkins School of Medicine, Baltimore, MD, USA
| | - Jun Hua
- Department of Radiology and Radiological Science, Johns Hopkins University School of Medicine, Baltimore, MD, USA; F.M. Kirby Research Center for Functional Brain Imaging, Kennedy Krieger Institute, Baltimore, MD, USA
| | - Kun Yang
- Department of Psychiatry, Johns Hopkins School of Medicine, Baltimore, MD, USA; Johns Hopkins Schizophrenia Center, Baltimore, MD, USA
| | - Minghong Ma
- Department of Neuroscience, University of Pennsylvania Perelman School of Medicine, Philadelphia, PA, USA
| | - Koko Ishizuka
- Department of Psychiatry, Johns Hopkins School of Medicine, Baltimore, MD, USA; Johns Hopkins Schizophrenia Center, Baltimore, MD, USA
| | - Akira Sawa
- Department of Biomedical Engineering, Johns Hopkins University, Baltimore, MD, USA; Department of Psychiatry, Johns Hopkins School of Medicine, Baltimore, MD, USA; Johns Hopkins Schizophrenia Center, Baltimore, MD, USA; Department of Neuroscience, Johns Hopkins School of Medicine, Baltimore, MD, USA; Department of Mental Health, Johns Hopkins Bloomberg School of Public Health, Baltimore, MD, USA.
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18
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Ramadan B, Cabeza L, Cramoisy S, Houdayer C, Andrieu P, Millot JL, Haffen E, Risold PY, Peterschmitt Y. Beneficial effects of prolonged 2-phenylethyl alcohol inhalation on chronic distress-induced anxio-depressive-like phenotype in female mice. Biomed Pharmacother 2022; 151:113100. [PMID: 35597115 DOI: 10.1016/j.biopha.2022.113100] [Citation(s) in RCA: 6] [Impact Index Per Article: 2.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 03/17/2022] [Revised: 05/10/2022] [Accepted: 05/10/2022] [Indexed: 11/02/2022] Open
Abstract
Chronic distress-induced hypothalamic-pituitary-adrenal axis deregulations have been associated with the development of neuropsychiatric disorders such as anxiety and depression. Currently available drugs treating such pathological conditions have limited efficacy and diverse side effects, revealing the need of new safer strategies. Aromatic plant-based compounds are largely used in herbal medicine due to their therapeutic properties on mood, physiology, and general well-being. The purpose of this study was to investigate the effects of 2-phenylethyl alcohol (PEA), one of the pharmacologically active constituents of rose essential oil, on chronic corticosterone (CORT)-induced behavioral and neurobiological changes in female mice. Animals followed a prolonged PEA inhalation exposure (30 min per day) for 15 consecutive days prior to behavioral evaluation with open-field, forced swim and novelty-suppressed feeding tests. CORT treatment induced an anxio-depressive-like phenotype, evidenced by a reduced locomotor activity in the open-field, and an increased latency to feed in the novelty-suppressed feeding paradigms. To elucidate the neural correlates of our behavioral results, immunohistochemistry was further performed to provide a global map of neural activity based on cerebral cFos expression. The altered feeding behavior was accompanied by a significant decrease in the number of cFos-positive cells in the olfactory bulb, and altered functional brain connectivity as shown by cross-correlation-based network analysis. CORT-induced behavioral and neurobiological alterations were reversed by prolonged PEA inhalation, suggesting a therapeutic action that allows regulating the activity of neural circuits involved in sensory, emotional and feeding behaviors. These findings might contribute to better understand the therapeutic potential of PEA on anxio-depressive symptoms.
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Affiliation(s)
- Bahrie Ramadan
- Laboratoire de Recherches Intégratives en Neurosciences et Psychologie Cognitive UR-LINC 481, Université de Franche-Comté, Université de B ourgogne - Franche-Comté, Besançon, France.
| | - Lidia Cabeza
- Laboratoire de Recherches Intégratives en Neurosciences et Psychologie Cognitive UR-LINC 481, Université de Franche-Comté, Université de B ourgogne - Franche-Comté, Besançon, France
| | - Stéphanie Cramoisy
- Laboratoire de Recherches Intégratives en Neurosciences et Psychologie Cognitive UR-LINC 481, Université de Franche-Comté, Université de B ourgogne - Franche-Comté, Besançon, France
| | - Christophe Houdayer
- Laboratoire de Recherches Intégratives en Neurosciences et Psychologie Cognitive UR-LINC 481, Université de Franche-Comté, Université de B ourgogne - Franche-Comté, Besançon, France
| | - Patrice Andrieu
- Laboratoire de Recherches Intégratives en Neurosciences et Psychologie Cognitive UR-LINC 481, Université de Franche-Comté, Université de B ourgogne - Franche-Comté, Besançon, France
| | - Jean-Louis Millot
- Laboratoire de Recherches Intégratives en Neurosciences et Psychologie Cognitive UR-LINC 481, Université de Franche-Comté, Université de B ourgogne - Franche-Comté, Besançon, France
| | - Emmanuel Haffen
- Laboratoire de Recherches Intégratives en Neurosciences et Psychologie Cognitive UR-LINC 481, Université de Franche-Comté, Université de B ourgogne - Franche-Comté, Besançon, France; Service de Psychiatrie de l'Adulte, Centre Hospitalier Universitaire de Besançon CHU, Besançon, France; Centre d'Investigation Clinique, CIC-INSERM-1431, Centre Hospitalier Universitaire de Besançon CHU, Besançon, France
| | - Pierre-Yves Risold
- Laboratoire de Recherches Intégratives en Neurosciences et Psychologie Cognitive UR-LINC 481, Université de Franche-Comté, Université de B ourgogne - Franche-Comté, Besançon, France
| | - Yvan Peterschmitt
- Laboratoire de Recherches Intégratives en Neurosciences et Psychologie Cognitive UR-LINC 481, Université de Franche-Comté, Université de B ourgogne - Franche-Comté, Besançon, France.
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19
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Noto T, Zhou G, Yang Q, Lane G, Zelano C. Human Primary Olfactory Amygdala Subregions Form Distinct Functional Networks, Suggesting Distinct Olfactory Functions. Front Syst Neurosci 2021; 15:752320. [PMID: 34955769 PMCID: PMC8695617 DOI: 10.3389/fnsys.2021.752320] [Citation(s) in RCA: 16] [Impact Index Per Article: 4.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 08/02/2021] [Accepted: 11/08/2021] [Indexed: 12/02/2022] Open
Abstract
Three subregions of the amygdala receive monosynaptic projections from the olfactory bulb, making them part of the primary olfactory cortex. These primary olfactory areas are located at the anterior-medial aspect of the amygdala and include the medial amygdala (MeA), cortical amygdala (CoA), and the periamygdaloid complex (PAC). The vast majority of research on the amygdala has focused on the larger basolateral and basomedial subregions, which are known to be involved in implicit learning, threat responses, and emotion. Fewer studies have focused on the MeA, CoA, and PAC, with most conducted in rodents. Therefore, our understanding of the functions of these amygdala subregions is limited, particularly in humans. Here, we first conducted a review of existing literature on the MeA, CoA, and PAC. We then used resting-state fMRI and unbiased k-means clustering techniques to show that the anatomical boundaries of human MeA, CoA, and PAC accurately parcellate based on their whole-brain resting connectivity patterns alone, suggesting that their functional networks are distinct, relative both to each other and to the amygdala subregions that do not receive input from the olfactory bulb. Finally, considering that distinct functional networks are suggestive of distinct functions, we examined the whole-brain resting network of each subregion and speculated on potential roles that each region may play in olfactory processing. Based on these analyses, we speculate that the MeA could potentially be involved in the generation of rapid motor responses to olfactory stimuli (including fight/flight), particularly in approach/avoid contexts. The CoA could potentially be involved in olfactory-related reward processing, including learning and memory of approach/avoid responses. The PAC could potentially be involved in the multisensory integration of olfactory information with other sensory systems. These speculations can be used to form the basis of future studies aimed at clarifying the olfactory functions of these under-studied primary olfactory areas.
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Affiliation(s)
- Torben Noto
- Department of Neurology, Feinberg School of Medicine, Northwestern University, Chicago, IL, United States
| | - Guangyu Zhou
- Department of Neurology, Feinberg School of Medicine, Northwestern University, Chicago, IL, United States
| | - Qiaohan Yang
- Department of Neurology, Feinberg School of Medicine, Northwestern University, Chicago, IL, United States
| | - Gregory Lane
- Department of Neurology, Feinberg School of Medicine, Northwestern University, Chicago, IL, United States
| | - Christina Zelano
- Department of Neurology, Feinberg School of Medicine, Northwestern University, Chicago, IL, United States
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20
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Torske A, Koch K, Eickhoff S, Freiherr J. Localizing the human brain response to olfactory stimulation: A meta-analytic approach. Neurosci Biobehav Rev 2021; 134:104512. [PMID: 34968523 DOI: 10.1016/j.neubiorev.2021.12.035] [Citation(s) in RCA: 16] [Impact Index Per Article: 4.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/01/2021] [Revised: 11/18/2021] [Accepted: 12/20/2021] [Indexed: 11/28/2022]
Abstract
The human sense of smell and the ability to detect and distinguish odors allows for the extraction of valuable information from the environment, thereby driving human behavior. Not only can the sense of smell help to monitor the safety of inhaled air, but it can also help to evaluate the edibility of food. Therefore, in an effort to further our understanding of the human sense of smell, the aim of this meta-analysis was to provide the scientific community with activation probability maps of the functional anatomy of the olfactory system, in addition to separate activation maps for specific odor categories (pleasant, food, and aversive odors). The activation likelihood estimation (ALE) method was utilized to quantify all relevant and available data to perform a formal statistical analysis on the inter-study concordance of various odor categories. A total of 81 studies (108 contrasts, 1053 foci) fulfilled our inclusion criteria. Significant ALE peaks were observed in all odor categories in brain areas typically associated with the functional neuroanatomy of olfaction including the piriform cortex, amygdala, insula, and orbitofrontal cortex, amongst others. Additional contrast analyses indicate clear differences in neural activation patterns between odor categories.
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Affiliation(s)
- A Torske
- Department of Diagnostic and Interventional Neuroradiology, School of Medicine, Technical University of Munich, Germany; Neuroimaging Center (TUM-NIC), Klinikum rechts der Isar, Technical University of Munich, Munich, Germany; Graduate School of Systemic Neurosciences, Ludwig Maximilians Universität München, Martinsried, Germany
| | - K Koch
- Department of Diagnostic and Interventional Neuroradiology, School of Medicine, Technical University of Munich, Germany; Neuroimaging Center (TUM-NIC), Klinikum rechts der Isar, Technical University of Munich, Munich, Germany; Graduate School of Systemic Neurosciences, Ludwig Maximilians Universität München, Martinsried, Germany
| | - S Eickhoff
- Institute of Systems Neuroscience, Medical Faculty, Heinrich Heine University Düsseldorf, Düsseldorf, Germany; Institute of Neuroscience and Medicine, Brain & Behaviour (INM-7), Research Centre Jülich, Jülich, Germany
| | - J Freiherr
- Department of Psychiatry and Psychotherapy, Friedrich-Alexander-Universität Erlangen-Nürnberg, Erlangen, Germany; Institute for Process Engineering and Packaging IVV, Sensory Analytics and Technologies, Fraunhofer Freising, Germany.
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21
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Kim AJ, Grégoire L, Anderson BA. Value-Biased Competition in the Auditory System of the Brain. J Cogn Neurosci 2021; 34:180-191. [PMID: 34673958 DOI: 10.1162/jocn_a_01785] [Citation(s) in RCA: 2] [Impact Index Per Article: 0.5] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/04/2022]
Abstract
Attentional capture by previously reward-associated stimuli has predominantly been measured in the visual domain. Recently, behavioral studies of value-driven attention have demonstrated involuntary attentional capture by previously reward-associated sounds, emulating behavioral findings within the visual domain and suggesting a common mechanism of attentional capture by value across sensory modalities. However, the neural correlates of the modulatory role of learned value on the processing of auditory information has not been examined. Here, we conducted a neuroimaging study on human participants using a previously established behavioral paradigm that measures value-driven attention in an auditory target identification task. We replicate behavioral findings of both voluntary prioritization and involuntary attentional capture by previously reward-associated sounds. When task-relevant, the selective processing of high-value sounds is supported by reduced activation in the dorsal attention network of the visual system (FEF, intraparietal sulcus, right middle frontal gyrus), implicating cross-modal processes of biased competition. When task-irrelevant, in contrast, high-value sounds evoke elevated activation in posterior parietal cortex and are represented with greater fidelity in the auditory cortex. Our findings reveal two distinct mechanisms of prioritizing reward-related auditory signals, with voluntary and involuntary modes of orienting that are differently manifested in biased competition.
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22
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Callara AL, Greco A, Frasnelli J, Rho G, Vanello N, Scilingo EP. Cortical network and connectivity underlying hedonic olfactory perception. J Neural Eng 2021; 18. [PMID: 34547740 DOI: 10.1088/1741-2552/ac28d2] [Citation(s) in RCA: 8] [Impact Index Per Article: 2.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 11/26/2020] [Accepted: 09/21/2021] [Indexed: 12/15/2022]
Abstract
Objective.The emotional response to olfactory stimuli implies the activation of a complex cascade of events triggered by structures lying in the limbic system. However, little is known about how this activation is projected up to cerebral cortex and how different cortical areas dynamically interact each other.Approach.In this study, we acquired EEG from human participants performing a passive odor-perception task with odorants conveying positive, neutral and negative valence. A novel methodological pipeline integrating global field power (GFP), independent component analysis (ICA), dipole source localization was applied to estimate effective connectivity in the challenging scenario of single-trial low-synchronized stimulation.Main results.We identified the brain network and the neural paths, elicited at different frequency bands, i.e.θ(4-7Hz),α(8-12Hz)andβ(13-30Hz), involved in odor valence processing. This brain network includes the orbitofrontal cortex (OFC), the cingulate gyrus (CgG), the superior temporal gyrus (STG), the posterior cingulate cortex/precuneus (PCC/PCu) and the parahippocampal gyrus (PHG). It was analyzed using a time-varying multivariate autoregressive model to resolve time-frequency causal interactions. Specifically, the OFC acts as the main node for odor perception and evaluation of pleasant and unpleasant stimuli, whereas no specific path was observed for a neutral stimulus.Significance.The results introduce new evidences on the role of the OFC during hedonic perception and underpin its specificity during the odor valence assessment. Our findings suggest that, after the odor onset different, bidirectional interactions occur between the OFC and other brain regions associated with emotion recognition/categorization and memory according to the stimulus valence. This outcome unveils how the hedonic olfactory network dynamically changes based on odor valence.
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Affiliation(s)
- Alejandro Luis Callara
- Research Center 'E. Piaggio', School of Engineering, University of Pisa, Largo Lucio Lazzarino 1, 56122 Pisa, Italy.,Dipartimento di Ingegneria dell'Informazione, University of Pisa, Via G. Caruso 16, 56122 Pisa, Italy
| | - Alberto Greco
- Research Center 'E. Piaggio', School of Engineering, University of Pisa, Largo Lucio Lazzarino 1, 56122 Pisa, Italy.,Dipartimento di Ingegneria dell'Informazione, University of Pisa, Via G. Caruso 16, 56122 Pisa, Italy
| | - Johannes Frasnelli
- Département d'anatomie, Université du Québec à Trois-Rivières, 3351, boul. des Forges, C.P. 500, G9A 5H7
- Local 3439 L.-P, Trois-Rivières, Québec, Canada
| | - Gianluca Rho
- Dipartimento di Ingegneria dell'Informazione, University of Pisa, Via G. Caruso 16, 56122 Pisa, Italy
| | - Nicola Vanello
- Research Center 'E. Piaggio', School of Engineering, University of Pisa, Largo Lucio Lazzarino 1, 56122 Pisa, Italy.,Dipartimento di Ingegneria dell'Informazione, University of Pisa, Via G. Caruso 16, 56122 Pisa, Italy
| | - Enzo Pasquale Scilingo
- Research Center 'E. Piaggio', School of Engineering, University of Pisa, Largo Lucio Lazzarino 1, 56122 Pisa, Italy.,Dipartimento di Ingegneria dell'Informazione, University of Pisa, Via G. Caruso 16, 56122 Pisa, Italy
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23
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Van der Burg E, Toet A, Brouwer AM, Van Erp JBF. Serial Dependence of Emotion Within and Between Stimulus Sensory Modalities. Multisens Res 2021; 35:1-22. [PMID: 34592713 DOI: 10.1163/22134808-bja10064] [Citation(s) in RCA: 4] [Impact Index Per Article: 1.0] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 06/28/2021] [Accepted: 09/16/2021] [Indexed: 11/19/2022]
Abstract
How we perceive the world is not solely determined by what we sense at a given moment in time, but also by what we processed recently. Here we investigated whether such serial dependencies for emotional stimuli transfer from one modality to another. Participants were presented a random sequence of emotional sounds and images and instructed to rate the valence and arousal of each stimulus (Experiment 1). For both ratings, we conducted an intertrial analysis, based on whether the rating on the previous trial was low or high. We found a positive serial dependence for valence and arousal regardless of the stimulus modality on two consecutive trials. In Experiment 2, we examined whether passively perceiving a stimulus is sufficient to induce a serial dependence. In Experiment 2, participants were instructed to rate the stimuli only on active trials and not on passive trials. The participants were informed that the active and passive trials were presented in alternating order, so that they were able to prepare for the task. We conducted an intertrial analysis on active trials, based on whether the rating on the previous passive trial (determined in Experiment 1) was low or high. For both ratings, we again observed positive serial dependencies regardless of the stimulus modality. We conclude that the emotional experience triggered by one stimulus affects the emotional experience for a subsequent stimulus regardless of their sensory modalities, that this occurs in a bottom-up fashion, and that this can be explained by residual activation in the emotional network in the brain.
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Affiliation(s)
- Erik Van der Burg
- Brain and Cognition, University of Amsterdam, 1012 WX Amsterdam, The Netherlands
- TNO, Human Factors, Kampweg 55, 3769 DE Soesterberg, The Netherlands
| | - Alexander Toet
- TNO, Human Factors, Kampweg 55, 3769 DE Soesterberg, The Netherlands
| | | | - Jan B F Van Erp
- TNO, Human Factors, Kampweg 55, 3769 DE Soesterberg, The Netherlands
- Research Group Human Media Interaction, University of Twente, 7522 NB Enschede, The Netherlands
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24
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Courrèges S, Aboulaasri R, Bhatara A, Bardel MH. Crossmodal Interactions Between Olfaction and Touch Affecting Well-Being and Perception of Cosmetic Creams. Front Psychol 2021; 12:703531. [PMID: 34484055 PMCID: PMC8414979 DOI: 10.3389/fpsyg.2021.703531] [Citation(s) in RCA: 2] [Impact Index Per Article: 0.5] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 04/30/2021] [Accepted: 07/20/2021] [Indexed: 11/13/2022] Open
Abstract
In the present series of studies, we investigated crossmodal perception of odor and texture. In four studies, participants tried two textures of face creams, one high viscosity (HV) and one low viscosity (LV), each with one of three levels of added odor (standard level, half of standard, or base [no added odor]), and then reported their levels of well-being. They also reported their perceptions of the face creams, including liking (global liking of the product, liking of its texture) and “objective” evaluations on just about right (JAR) scales (texture and visual appearance evaluations). In Study 1, women in France tried the creams on their hands, as they would when testing them in a store, and in Study 2, a second group of French women tried the creams on their faces, as they would at home. In Studies 3 and 4, these same two procedures were repeated in China. Results showed that both odor and texture had effects on well-being, liking, and JAR ratings, including interaction effects. Though effects varied by country and context (hand or face), the addition of odor to the creams generally increased reports of well-being, global liking and texture liking, in some cases affecting the “objective” evaluations of texture. This is one of the first investigations of crossmodal olfactory and tactile perception's impacts on well-being, and it reinforces previous literature showing the importance of olfaction on well-being.
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Affiliation(s)
- Sandra Courrèges
- Beauty Research and Performance, Innovation Research and Development Department, CHANEL Fragrance and Beauty, Pantin, France
| | | | | | - Marie-Héloïse Bardel
- Beauty Research and Performance, Innovation Research and Development Department, CHANEL Fragrance and Beauty, Pantin, France
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25
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Jo HG, Wudarczyk O, Leclerc M, Regenbogen C, Lampert A, Rothermel M, Habel U. Effect of odor pleasantness on heat-induced pain: An fMRI study. Brain Imaging Behav 2021; 15:1300-1312. [PMID: 32770446 DOI: 10.1007/s11682-020-00328-0] [Citation(s) in RCA: 5] [Impact Index Per Article: 1.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 01/07/2023]
Abstract
Odor modulates the experience of pain, but the neural basis of how the two sensory modalities, olfaction and pain, are linked in the central nervous system is far from clear. In this study, we investigated the mechanisms by which the brain modulates the pain experience under concurrent odorant stimulation. We conducted an fMRI study using a 2 × 3 factorial design, in which one of two temperatures (warm, hot) and one of three types of odors (pleasant, unpleasant, no odor) were presented simultaneously. "Hot" temperatures were individually determined as those perceived as painful (mean temperature = 46.9 °C). The non-painful "warm" temperature was set to 40 °C. Participants rated hot compared to warm stimuli as more intense and unpleasant, especially in the presence of an unpleasant odor. Parametric modeling on the intensity ratings activated the pain network, covering brain regions activated by the hot stimuli. The presence of an odor, irrespective of its valence, activated the amygdalae. In addition, the amygdalae showed stimulus-dependent functional couplings with the right supramarginal gyrus and with the left superior frontal gyrus. The coupling between the right amygdala and the left superior frontal gyrus was related to the intensity and unpleasantness ratings of the pain experience. Our results suggest that these functional connections may reflect the integrating process of the two sensory modalities, enabling olfactory influence on the pain experience.
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Affiliation(s)
- Han-Gue Jo
- Department of Psychiatry, Psychotherapy and Psychosomatics, Medical Faculty, RWTH Aachen University, Aachen, Germany. .,JARA-Institute Brain Structure Function Relationship (INM-10), Research Center Jülich and RWTH Aachen University, Jülich, Germany. .,School of Computer, Information and Communication Engineering, Kunsan National University, Gunsan, South Korea.
| | - Olga Wudarczyk
- Department of Psychiatry, Psychotherapy and Psychosomatics, Medical Faculty, RWTH Aachen University, Aachen, Germany.,Department of Psychology, Humboldt-Universität zu Berlin, Berlin, Germany.,Cluster of Excellence Science of Intelligence, Technische Universität Berlin and Humboldt Universität zu Berlin, 10587, Berlin, Germany
| | - Marcel Leclerc
- Department of Psychiatry, Psychotherapy and Psychosomatics, Medical Faculty, RWTH Aachen University, Aachen, Germany
| | - Christina Regenbogen
- Department of Psychiatry, Psychotherapy and Psychosomatics, Medical Faculty, RWTH Aachen University, Aachen, Germany.,JARA-Institute Brain Structure Function Relationship (INM-10), Research Center Jülich and RWTH Aachen University, Jülich, Germany.,Department of Clinical Neuroscience, Karolinska Institutet, Stockholm, Sweden
| | - Angelika Lampert
- Institute of Physiology, Medical Faculty, RWTH Aachen University, Aachen, Germany
| | - Markus Rothermel
- Department of Chemosensation, AG Neuromodulation, Institute for Biology II, RWTH Aachen University, Aachen, Germany
| | - Ute Habel
- Department of Psychiatry, Psychotherapy and Psychosomatics, Medical Faculty, RWTH Aachen University, Aachen, Germany.,JARA-Institute Brain Structure Function Relationship (INM-10), Research Center Jülich and RWTH Aachen University, Jülich, Germany
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26
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27
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Lasschuijt MP, de Graaf K, Mars M. Effects of Oro-Sensory Exposure on Satiation and Underlying Neurophysiological Mechanisms-What Do We Know So Far? Nutrients 2021; 13:nu13051391. [PMID: 33919044 PMCID: PMC8143001 DOI: 10.3390/nu13051391] [Citation(s) in RCA: 19] [Impact Index Per Article: 4.8] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 02/01/2021] [Revised: 04/12/2021] [Accepted: 04/13/2021] [Indexed: 11/16/2022] Open
Abstract
The mouth is the first part of the gastrointestinal tract. During mastication sensory signals from the mouth, so-called oro-sensory exposure, elicit physiological signals that affect satiation and food intake. It has been established that a longer duration of oro-sensory exposure leads to earlier satiation. In addition, foods with more intense sweet or salty taste induce earlier satiation compared to foods that are equally palatable, but with lower taste intensity. Oro-sensory exposure to food affects satiation by direct signaling via the brainstem to higher cortical regions involved in taste and reward, including the nucleus accumbens and the insula. There is little evidence that oro-sensory exposure affects satiation indirectly through either hormone responses or gastric signals. Critical brain areas for satiation, such as the brainstem, should be studied more intensively to better understand the neurophysiological mechanisms underlying the process of satiation. Furthermore, it is essential to increase the understanding of how of highly automated eating behaviors, such as oral processing and eating rate, are formed during early childhood. A better understanding of the aforementioned mechanisms provides fundamental insight in relation to strategies to prevent overconsumption and the development of obesity in future generations.
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28
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Mancini M, Cherubino P, Cartocci G, Martinez A, Borghini G, Guastamacchia E, di Flumeri G, Rossi D, Modica E, Menicocci S, Lupo V, Trettel A, Babiloni F. Forefront Users' Experience Evaluation by Employing Together Virtual Reality and Electroencephalography: A Case Study on Cognitive Effects of Scents. Brain Sci 2021; 11:256. [PMID: 33670698 PMCID: PMC7922691 DOI: 10.3390/brainsci11020256] [Citation(s) in RCA: 6] [Impact Index Per Article: 1.5] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/19/2021] [Revised: 02/12/2021] [Accepted: 02/13/2021] [Indexed: 01/02/2023] Open
Abstract
Scents have the ability to affect peoples' mental states and task performance with to different extents. It has been widely demonstrated that the lemon scent, included in most all-purpose cleaners, elicits stimulation and activation, while the lavender scent elicits relaxation and sedative effects. The present study aimed at investigating and fostering a novel approach to evaluate users' experience with respect to scents' effects through the joint employment of Virtual Reality and users' neurophysiological monitoring, in particular Electroencephalography. In particular, this study, involving 42 participants, aimed to compare the effects of lemon and lavender scents on the deployment of cognitive resources during a daily life experience consisting in a train journey carried out in virtual reality. Our findings showed a significant higher request of cognitive resources during the processing of an informative message for subjects exposed to the lavender scent with respect to the lemon exposure. No differences were found between lemon and lavender conditions on the self-reported items of pleasantness and involvement; as this study demonstrated, the employment of the lavender scent preserves the quality of the customer experience to the same extent as the more widely used lemon scent.
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Affiliation(s)
- Marco Mancini
- BrainSigns Srl, Via Lungotevere Michelangelo, 9, 00192 Rome, Italy; (P.C.); (G.C.); (A.M.); (G.B.); (E.G.); (G.d.F.); (S.M.); (V.L.); (A.T.); (F.B.)
- Department of Economics, Management and Business Law, University of Bari Aldo Moro (UniBa), Via Camillo Rosalba, 53, 70124 Bari, Italy
| | - Patrizia Cherubino
- BrainSigns Srl, Via Lungotevere Michelangelo, 9, 00192 Rome, Italy; (P.C.); (G.C.); (A.M.); (G.B.); (E.G.); (G.d.F.); (S.M.); (V.L.); (A.T.); (F.B.)
- Department of Molecular Medicine, Sapienza University of Rome, Viale Regina Elena, 291, 00161 Rome, Italy
| | - Giulia Cartocci
- BrainSigns Srl, Via Lungotevere Michelangelo, 9, 00192 Rome, Italy; (P.C.); (G.C.); (A.M.); (G.B.); (E.G.); (G.d.F.); (S.M.); (V.L.); (A.T.); (F.B.)
- Department of Molecular Medicine, Sapienza University of Rome, Viale Regina Elena, 291, 00161 Rome, Italy
| | - Ana Martinez
- BrainSigns Srl, Via Lungotevere Michelangelo, 9, 00192 Rome, Italy; (P.C.); (G.C.); (A.M.); (G.B.); (E.G.); (G.d.F.); (S.M.); (V.L.); (A.T.); (F.B.)
- Department of Communication and Social Research, Sapienza University of Rome, Via Salaria, 113, 00198 Rome, Italy
| | - Gianluca Borghini
- BrainSigns Srl, Via Lungotevere Michelangelo, 9, 00192 Rome, Italy; (P.C.); (G.C.); (A.M.); (G.B.); (E.G.); (G.d.F.); (S.M.); (V.L.); (A.T.); (F.B.)
- Department of Molecular Medicine, Sapienza University of Rome, Viale Regina Elena, 291, 00161 Rome, Italy
- IRCCS Fondazione Santa Lucia, Neuroelectrical Imaging and BCI Lab, Via Ardeatina 306, 00179 Rome, Italy
| | - Elena Guastamacchia
- BrainSigns Srl, Via Lungotevere Michelangelo, 9, 00192 Rome, Italy; (P.C.); (G.C.); (A.M.); (G.B.); (E.G.); (G.d.F.); (S.M.); (V.L.); (A.T.); (F.B.)
| | - Gianluca di Flumeri
- BrainSigns Srl, Via Lungotevere Michelangelo, 9, 00192 Rome, Italy; (P.C.); (G.C.); (A.M.); (G.B.); (E.G.); (G.d.F.); (S.M.); (V.L.); (A.T.); (F.B.)
- Department of Molecular Medicine, Sapienza University of Rome, Viale Regina Elena, 291, 00161 Rome, Italy
- IRCCS Fondazione Santa Lucia, Neuroelectrical Imaging and BCI Lab, Via Ardeatina 306, 00179 Rome, Italy
| | - Dario Rossi
- Department of Anatomical, Histological, Forensic & Orthopedic Sciences, Sapienza University of Rome, Piazzale Aldo Moro, 5, 00185 Rome, Italy; (D.R.); (E.M.)
| | - Enrica Modica
- Department of Anatomical, Histological, Forensic & Orthopedic Sciences, Sapienza University of Rome, Piazzale Aldo Moro, 5, 00185 Rome, Italy; (D.R.); (E.M.)
| | - Stefano Menicocci
- BrainSigns Srl, Via Lungotevere Michelangelo, 9, 00192 Rome, Italy; (P.C.); (G.C.); (A.M.); (G.B.); (E.G.); (G.d.F.); (S.M.); (V.L.); (A.T.); (F.B.)
| | - Viviana Lupo
- BrainSigns Srl, Via Lungotevere Michelangelo, 9, 00192 Rome, Italy; (P.C.); (G.C.); (A.M.); (G.B.); (E.G.); (G.d.F.); (S.M.); (V.L.); (A.T.); (F.B.)
| | - Arianna Trettel
- BrainSigns Srl, Via Lungotevere Michelangelo, 9, 00192 Rome, Italy; (P.C.); (G.C.); (A.M.); (G.B.); (E.G.); (G.d.F.); (S.M.); (V.L.); (A.T.); (F.B.)
| | - Fabio Babiloni
- BrainSigns Srl, Via Lungotevere Michelangelo, 9, 00192 Rome, Italy; (P.C.); (G.C.); (A.M.); (G.B.); (E.G.); (G.d.F.); (S.M.); (V.L.); (A.T.); (F.B.)
- Department of Molecular Medicine, Sapienza University of Rome, Viale Regina Elena, 291, 00161 Rome, Italy
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Baccarani A, Brand G, Dacremont C, Valentin D, Brochard R. The influence of stimulus concentration and odor intensity on relaxing and stimulating perceived properties of odors. Food Qual Prefer 2021. [DOI: 10.1016/j.foodqual.2020.104030] [Citation(s) in RCA: 14] [Impact Index Per Article: 3.5] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 12/01/2022]
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30
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Kermen F, Mandairon N, Chalençon L. Odor hedonics coding in the vertebrate olfactory bulb. Cell Tissue Res 2021; 383:485-493. [PMID: 33515292 PMCID: PMC7873110 DOI: 10.1007/s00441-020-03372-w] [Citation(s) in RCA: 5] [Impact Index Per Article: 1.3] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/04/2020] [Accepted: 11/29/2020] [Indexed: 12/21/2022]
Abstract
Whether an odorant is perceived as pleasant or unpleasant (hedonic value) governs a range of crucial behaviors: foraging, escaping danger, and social interaction. Despite its importance in olfactory perception, little is known regarding how odor hedonics is represented and encoded in the brain. Here, we review recent findings describing how odorant hedonic value is represented in the first olfaction processing center, the olfactory bulb. We discuss how olfactory bulb circuits might contribute to the coding of innate and learned odorant hedonics in addition to the odorant's physicochemical properties.
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Affiliation(s)
- Florence Kermen
- Department of Biology, Faculty of Natural Sciences, Norwegian University of Science and Technology, 7030, Trondheim, Norway.
| | - Nathalie Mandairon
- CNRS. UMR 5292: INSERM, U1028: Lyon Neuroscience Research Center Neuroplasticity and Neuropathology of Olfactory Perception Team, University Lyon, University Lyon1, F-69000, Villeurbanne, France
| | - Laura Chalençon
- CNRS. UMR 5292: INSERM, U1028: Lyon Neuroscience Research Center Neuroplasticity and Neuropathology of Olfactory Perception Team, University Lyon, University Lyon1, F-69000, Villeurbanne, France
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Carlson H, Leitão J, Delplanque S, Cayeux I, Sander D, Vuilleumier P. Sustained effects of pleasant and unpleasant smells on resting state brain activity. Cortex 2020; 132:386-403. [PMID: 33039687 DOI: 10.1016/j.cortex.2020.06.017] [Citation(s) in RCA: 7] [Impact Index Per Article: 1.4] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 02/11/2020] [Revised: 06/17/2020] [Accepted: 06/19/2020] [Indexed: 10/23/2022]
Abstract
Research suggests that transient emotional episodes produces sustained effects on psychological functions and brain activity during subsequent resting state. In this fMRI study we investigated whether transient emotions induced by smells could impact brain connectivity at rest in a valence-specific manner. The results suggest a sustained reconfiguration of parts of the default mode network which become more connected with areas implicated in olfactory processing, emotional learning, and action control. We found lingering effects of odorants on subsequent resting state that predominantly involved connections of the precuneus with a network comprising the insula, amygdala, medial orbital gyrus. Unpleasant smells in particular predicted greater coupling between insula, hippocampal structures, and prefrontal cortex, possible reflecting enhanced aversive learning and avoidance motivation. More broadly, our study illustrates a novel approach to characterize the impact of smells on brain function and differentiate the neural signatures of their valence, during task-free rest conditions.
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Affiliation(s)
- Heather Carlson
- Laboratory of Behavioral Neurology and Imaging of Cognition, Dept. of Neurosciences, University Medical Center, University of Geneva, Switzerland; Swiss Center for Affective Sciences, University of Geneva, Switzerland.
| | - Joana Leitão
- Laboratory of Behavioral Neurology and Imaging of Cognition, Dept. of Neurosciences, University Medical Center, University of Geneva, Switzerland; Swiss Center for Affective Sciences, University of Geneva, Switzerland
| | - Sylvain Delplanque
- Swiss Center for Affective Sciences, University of Geneva, Switzerland; Laboratory for the Study of Emotion Elicitation and Expression, Department of Psychology, University of Geneva
| | | | - David Sander
- Swiss Center for Affective Sciences, University of Geneva, Switzerland; Laboratory for the Study of Emotion Elicitation and Expression, Department of Psychology, University of Geneva
| | - Patrik Vuilleumier
- Laboratory of Behavioral Neurology and Imaging of Cognition, Dept. of Neurosciences, University Medical Center, University of Geneva, Switzerland; Swiss Center for Affective Sciences, University of Geneva, Switzerland
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32
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Seet MS, Amin MR, Abbasi NI, Hamano J, Chaudhury A, Bezerianos A, Faghih RT, Thakor NV, Dragomir A. Olfactory-induced Positive Affect and Autonomic Response as a Function of Hedonic and Intensity Attributes of Fragrances. ANNUAL INTERNATIONAL CONFERENCE OF THE IEEE ENGINEERING IN MEDICINE AND BIOLOGY SOCIETY. IEEE ENGINEERING IN MEDICINE AND BIOLOGY SOCIETY. ANNUAL INTERNATIONAL CONFERENCE 2020; 2020:3170-3173. [PMID: 33018678 DOI: 10.1109/embc44109.2020.9176095] [Citation(s) in RCA: 4] [Impact Index Per Article: 0.8] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Subscribe] [Scholar Register] [Indexed: 11/05/2022]
Abstract
Olfactory perception is intrinsically tied to emotional processing, in both behavior and neurophysiology. Despite advances in olfactory-affective neuroscience, it is unclear how separate attributes of odor stimuli contribute to olfactoryinduced emotions, especially within the positive segment of the hedonic dimension to avoid potential cross-valence confounds. In this study, we examined how pleasantness and intensity of fragrances relate to different grades of positive affect. Our results show that greater odor pleasantness and intensity are independently associated with stronger positive affect. Pleasantness has a greater influence than intensity in evoking a positive vs. neutral affect, whereas intensity is more impactful than pleasantness in evoking an extreme positive vs. positive response. Autonomic response, as assessed by the galvanic skin response (GSR) was found to decrease with increasing pleasantness but not intensity. This clarifies how olfactory and affective processing induce significant downstream effects in peripheral physiology and self-reported affective experience, pertinent to the thriving field of olfactory neuromarkerting.
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Han P, Weber C, Hummel T. Brain response to intranasal trimethylamine stimulation: A preliminary human fMRI study. Neurosci Lett 2020; 735:135166. [PMID: 32574795 DOI: 10.1016/j.neulet.2020.135166] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 04/21/2020] [Revised: 06/04/2020] [Accepted: 06/15/2020] [Indexed: 11/29/2022]
Abstract
The trace amine-associated receptors (TAARs) are a second class of olfactory receptors in humans. They are activated by volatile amines, including pheromone-like odors. However, in humans the neural processing of TAAR-associated signals is not known. Using functional magnetic resonance imaging, the current study investigated brain activation following intra-nasal stimulation with trimethylamine (TMA), an agonist of human TAAR5, and three "canonical" odors with varied valence (an unpleasant odor [n-butanol], a neutral to unpleasant odor [civet musk], and a pleasant odor [phenyl ethyl alcohol]) in 12 healthy young participants. Our hypothesis driven analysis showed that TMA induced a trend for stronger left amygdala activation as compared to the other odors (Family-Wise Error corrected p = 0.08). Whole-brain exploratory analyses revealed superior activation of the cerebellum and caudate to TMA compared to canonical odors, and stronger activation of the anterior cingulate and somatosensory regions (postcentral gyrus and mid cingulate) in response to canonical odors compared to TMA. The current results provide initial evidence on differential central processes of a TAAR mediated stimulus compared to odors targeting canonical olfactory receptors. Future research are needed to elucidate the physiological and psychological relevance of TAARs in humans.
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Affiliation(s)
- Pengfei Han
- Interdisciplinary Center on Smell and Taste, Department of Otorhinolaryngology, TU Dresden, Dresden, Germany; Faculty of Psychology, Southwest University, Chongqing, China; The Key Laboratory of Cognition and Personality, Ministry of Education, Chongqing, China.
| | - Catharina Weber
- Interdisciplinary Center on Smell and Taste, Department of Otorhinolaryngology, TU Dresden, Dresden, Germany
| | - Thomas Hummel
- Interdisciplinary Center on Smell and Taste, Department of Otorhinolaryngology, TU Dresden, Dresden, Germany
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Koide-Majima N, Nakai T, Nishimoto S. Distinct dimensions of emotion in the human brain and their representation on the cortical surface. Neuroimage 2020; 222:117258. [PMID: 32798681 DOI: 10.1016/j.neuroimage.2020.117258] [Citation(s) in RCA: 4] [Impact Index Per Article: 0.8] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 12/13/2019] [Revised: 08/02/2020] [Accepted: 08/05/2020] [Indexed: 12/24/2022] Open
Abstract
We experience a rich variety of emotions in daily life, and a fundamental goal of affective neuroscience is to determine how these emotions are represented in the brain. Recent psychological studies have used naturalistic stimuli (e.g., movies) to reveal high dimensional representational structures of diverse daily-life emotions. However, relatively little is known about how such diverse emotions are represented in the brain because most of the affective neuroscience studies have used only a small number of controlled stimuli. To reveal that, we measured functional MRI to obtain blood-oxygen-level-dependent (BOLD) responses from human subjects while they watched emotion-inducing audiovisual movies over a period of 3 hours. For each of the one-second movie scenes, we annotated the movies with respect to 80 emotions selected based on a wide range of previous emotion literature. By quantifying canonical correlations between the emotion ratings and the BOLD responses, the results suggest that around 25 distinct dimensions (ranging from 18 to 36 and being subject-dependent) of the emotion ratings contribute to emotion representations in the brain. For demonstrating how the 80 emotion categories were represented in the cortical surface, we visualized a continuous semantic space of the emotion representation and mapped it on the cortical surface. We found that the emotion categories were changed from unimodal to transmodal regions on the cortical surface. This study presents a cortical representation of a rich variety of emotion categories, which covers many of the emotional experiences of daily living.
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Affiliation(s)
| | - Tomoya Nakai
- Center for Information and Neural Networks (CiNet), National Institute of Information and Communications Technology, Osaka, Japan; Graduate School of Frontier Biosciences, Osaka University, Osaka, Japan
| | - Shinji Nishimoto
- Center for Information and Neural Networks (CiNet), National Institute of Information and Communications Technology, Osaka, Japan; Graduate School of Frontier Biosciences, Osaka University, Osaka, Japan; Graduate School of Medicine, Osaka University, Osaka, Japan.
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35
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Liu Y, Toet A, Krone T, van Stokkum R, Eijsman S, van Erp JBF. A network model of affective odor perception. PLoS One 2020; 15:e0236468. [PMID: 32730278 PMCID: PMC7392242 DOI: 10.1371/journal.pone.0236468] [Citation(s) in RCA: 3] [Impact Index Per Article: 0.6] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 08/31/2019] [Accepted: 07/07/2020] [Indexed: 01/10/2023] Open
Abstract
The affective appraisal of odors is known to depend on their intensity (I), familiarity (F), detection threshold (T), and on the baseline affective state of the observer. However, the exact nature of these relations is still largely unknown. We therefore performed an observer experiment in which participants (N = 52) smelled 40 different odors (varying widely in hedonic valence) and reported the intensity, familiarity and their affective appraisal (valence and arousal: V and A) for each odor. Also, we measured the baseline affective state (valence and arousal: BV and BA) and odor detection threshold of the participants. Analyzing the results for pleasant and unpleasant odors separately, we obtained two models through network analysis. Several relations that have previously been reported in the literature also emerge in both models (the relations between F and I, F and V, I and A; I and V, BV and T). However, there are also relations that do not emerge (between BA and V, BV and I, and T and I) or that appear with a different polarity (the relation between F and A for pleasant odors). Intensity (I) has the largest impact on the affective appraisal of unpleasant odors, while F significantly contributes to the appraisal of pleasant odors. T is only affected by BV and has no effect on other variables. This study is a first step towards an integral study of the affective appraisal of odors through network analysis. Future studies should also include other factors that are known to influence odor appraisal, such as age, gender, personality, and culture.
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Affiliation(s)
- Yingxuan Liu
- Perceptual and Cognitive Systems, TNO, Soesterberg, The Netherlands
| | - Alexander Toet
- Perceptual and Cognitive Systems, TNO, Soesterberg, The Netherlands
| | - Tanja Krone
- Risk Analysis for Products in Development RAPID, TNO, Zeist, The Netherlands
| | - Robin van Stokkum
- Risk Analysis for Products in Development RAPID, TNO, Zeist, The Netherlands
| | - Sophia Eijsman
- Perceptual and Cognitive Systems, TNO, Soesterberg, The Netherlands
| | - Jan B. F. van Erp
- Perceptual and Cognitive Systems, TNO, Soesterberg, The Netherlands
- Research Group Human Media Interaction, University of Twente, Enschede, The Netherlands
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Lane G, Zhou G, Noto T, Zelano C. Assessment of direct knowledge of the human olfactory system. Exp Neurol 2020; 329:113304. [PMID: 32278646 DOI: 10.1016/j.expneurol.2020.113304] [Citation(s) in RCA: 29] [Impact Index Per Article: 5.8] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/03/2019] [Revised: 01/13/2020] [Accepted: 04/08/2020] [Indexed: 12/31/2022]
Affiliation(s)
- Gregory Lane
- Northwestern University Feinberg School of Medicine, Department of Neurology, 303 E Chicago Ave, Chicago, IL 60611, USA.
| | - Guangyu Zhou
- Northwestern University Feinberg School of Medicine, Department of Neurology, 303 E Chicago Ave, Chicago, IL 60611, USA.
| | - Torben Noto
- Northwestern University Feinberg School of Medicine, Department of Neurology, 303 E Chicago Ave, Chicago, IL 60611, USA
| | - Christina Zelano
- Northwestern University Feinberg School of Medicine, Department of Neurology, 303 E Chicago Ave, Chicago, IL 60611, USA
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Abstract
Neurons that synthesize and release 5-hydroxytryptamine (5-HT; serotonin) express a core set of genes that establish and maintain this neurotransmitter phenotype and distinguish these neurons from other brain cells. Beyond a shared 5-HTergic phenotype, these neurons display divergent cellular properties in relation to anatomy, morphology, hodology, electrophysiology and gene expression, including differential expression of molecules supporting co-transmission of additional neurotransmitters. This diversity suggests that functionally heterogeneous subtypes of 5-HT neurons exist, but linking subsets of these neurons to particular functions has been technically challenging. We discuss recent data from molecular genetic, genomic and functional methods that, when coupled with classical findings, yield a reframing of the 5-HT neuronal system as a conglomeration of diverse subsystems with potential to inspire novel, more targeted therapies for clinically distinct 5-HT-related disorders.
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38
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Lin H, Müller-Bardorff M, Gathmann B, Brieke J, Mothes-Lasch M, Bruchmann M, Miltner WHR, Straube T. Stimulus arousal drives amygdalar responses to emotional expressions across sensory modalities. Sci Rep 2020; 10:1898. [PMID: 32024891 PMCID: PMC7002496 DOI: 10.1038/s41598-020-58839-1] [Citation(s) in RCA: 14] [Impact Index Per Article: 2.8] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/23/2019] [Accepted: 12/23/2019] [Indexed: 11/08/2022] Open
Abstract
The factors that drive amygdalar responses to emotionally significant stimuli are still a matter of debate - particularly the proneness of the amygdala to respond to negatively-valenced stimuli has been discussed controversially. Furthermore, it is uncertain whether the amygdala responds in a modality-general fashion or whether modality-specific idiosyncrasies exist. Therefore, the present functional magnetic resonance imaging (fMRI) study systematically investigated amygdalar responding to stimulus valence and arousal of emotional expressions across visual and auditory modalities. During scanning, participants performed a gender judgment task while prosodic and facial emotional expressions were presented. The stimuli varied in stimulus valence and arousal by including neutral, happy and angry expressions of high and low emotional intensity. Results demonstrate amygdalar activation as a function of stimulus arousal and accordingly associated emotional intensity regardless of stimulus valence. Furthermore, arousal-driven amygdalar responding did not depend on the visual and auditory modalities of emotional expressions. Thus, the current results are consistent with the notion that the amygdala codes general stimulus relevance across visual and auditory modalities irrespective of valence. In addition, whole brain analyses revealed that effects in visual and auditory areas were driven mainly by high intense emotional facial and vocal stimuli, respectively, suggesting modality-specific representations of emotional expressions in auditory and visual cortices.
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Affiliation(s)
- Huiyan Lin
- Institute of Applied Psychology, School of Public Administration, Guangdong University of Finance, 510521, Guangzhou, China.
- Institute of Medical Psychology and Systems Neuroscience, University of Muenster, 48149, Muenster, Germany.
| | - Miriam Müller-Bardorff
- Institute of Medical Psychology and Systems Neuroscience, University of Muenster, 48149, Muenster, Germany
| | - Bettina Gathmann
- Institute of Medical Psychology and Systems Neuroscience, University of Muenster, 48149, Muenster, Germany
| | - Jaqueline Brieke
- Institute of Medical Psychology and Systems Neuroscience, University of Muenster, 48149, Muenster, Germany
| | - Martin Mothes-Lasch
- Institute of Medical Psychology and Systems Neuroscience, University of Muenster, 48149, Muenster, Germany
| | - Maximilian Bruchmann
- Institute of Medical Psychology and Systems Neuroscience, University of Muenster, 48149, Muenster, Germany
| | - Wolfgang H R Miltner
- Department of Clinical Psychology, Friedrich Schiller University of Jena, 07743, Jena, Germany
| | - Thomas Straube
- Institute of Medical Psychology and Systems Neuroscience, University of Muenster, 48149, Muenster, Germany
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A methodological investigation of a flexible surface MRI coil to obtain functional signals from the human olfactory bulb. J Neurosci Methods 2020; 335:108624. [PMID: 32032715 DOI: 10.1016/j.jneumeth.2020.108624] [Citation(s) in RCA: 3] [Impact Index Per Article: 0.6] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/03/2019] [Revised: 01/21/2020] [Accepted: 02/03/2020] [Indexed: 11/21/2022]
Abstract
BACKGROUND Mammalian olfaction begins with transduction in olfactory receptors, continues with extensive processing in the olfactory bulb, and culminates in cortical representation. Most rodent studies on the functional neuroanatomy of olfaction have concentrated on the olfactory bulb, yet whether this structure is tuned only to basic chemical features of odorants or also to higher-order perceptual features is unclear. NEW METHOD Whereas studies of the human brain can typically uncover involvement of higher-order feature extraction, this has not been possible in the case of the olfactory bulb, inaccessible to fMRI. The present study examined whether a novel method of acquisition using a facial coil could overcome this limitation. RESULTS A series of experiments provided preliminary evidence of odor-driven responses in the human olfactory bulb, and found that these responses differed between individuals. COMPARISON WITH EXISTING METHODS AND CONCLUSIONS The present preliminary technical achievement renders possible to design novel human odor fMRI studies by considering the olfactory system from the olfactory bulb to associative areas.
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40
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Anatomical imaging of the piriform cortex in epilepsy. Exp Neurol 2019; 320:113013. [DOI: 10.1016/j.expneurol.2019.113013] [Citation(s) in RCA: 19] [Impact Index Per Article: 3.2] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 02/04/2019] [Revised: 06/08/2019] [Accepted: 07/15/2019] [Indexed: 11/23/2022]
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Mantel M, Ferdenzi C, Roy JM, Bensafi M. Individual Differences as a Key Factor to Uncover the Neural Underpinnings of Hedonic and Social Functions of Human Olfaction: Current Findings from PET and fMRI Studies and Future Considerations. Brain Topogr 2019; 32:977-986. [PMID: 31564029 DOI: 10.1007/s10548-019-00733-9] [Citation(s) in RCA: 11] [Impact Index Per Article: 1.8] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/01/2019] [Accepted: 09/18/2019] [Indexed: 01/20/2023]
Abstract
The hedonic and social dimensions of olfactory perception are characterized by a great diversity across people. Whereas the cerebral processing underlying these aspects of odor perception have been widely explored in the last decades, very few brain imaging studies considered individual differences. This lack of consideration weakens the current models in the field, where the paradigm of universality is the norm. The present review is aimed at examining this issue. Through a synthetic summary, we will first present past studies suggesting that (1) hedonics are represented consistently throughout the olfactory system from primary to secondary areas, with a progressive cognitive modulation and integration with other senses, (2) social dimension of odors may be represented in a distinct pathway involving social and attentional networks. In a second, and more critical part, we will highlight the importance of individual differences for the cerebral study of human olfaction.
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Affiliation(s)
- Marylou Mantel
- Lyon Neuroscience Research Center, University Claude Bernard of Lyon, CNRS, INSERM, Lyon, France.
- Ecole Normale Supérieure de Lyon, Lyon, France.
- Centre Hospitalier Le Vinatier, CRNL, CNRS UMR5292 - Inserm U1028 - UCBL, Bâtiment 462 - Neurocampus, 95 boulevard Pinel, 69675, Bron Cedex, France.
| | - Camille Ferdenzi
- Lyon Neuroscience Research Center, University Claude Bernard of Lyon, CNRS, INSERM, Lyon, France
| | | | - Moustafa Bensafi
- Lyon Neuroscience Research Center, University Claude Bernard of Lyon, CNRS, INSERM, Lyon, France.
- Centre Hospitalier Le Vinatier, CRNL, CNRS UMR5292 - Inserm U1028 - UCBL, Bâtiment 462 - Neurocampus, 95 boulevard Pinel, 69675, Bron Cedex, France.
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42
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Coquery N, Menneson S, Meurice P, Janvier R, Etienne P, Noirot V, Val-Laillet D. fMRI-Based Brain Responses to Olfactory Stimulation with Two Putatively Orexigenic Functional Food Ingredients at Two Different Concentrations in the Pig Model. J Food Sci 2019; 84:2666-2673. [PMID: 31441517 DOI: 10.1111/1750-3841.14772] [Citation(s) in RCA: 6] [Impact Index Per Article: 1.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 02/04/2019] [Revised: 07/10/2019] [Accepted: 07/19/2019] [Indexed: 11/29/2022]
Abstract
Natural plant extracts are increasingly used as functional feed ingredients in animal husbandry and food ingredients in human alternative medicine to improve welfare and health. We investigated in 20 growing pigs via functional magnetic resonance imaging (fMRI) the brain blood oxygen level-dependent (BOLD) responses to olfactory stimulation with two sensory functional feed ingredients, A and B, at two different concentrations. Functional ingredient A contained extracts from Citrus sinensis (60% to 80%), and ingredient B contained a mixture of extracts Oreganum vulgarae (40% to 55%) and Cymbopogon flexuosus (20% to 25%). Increased concentration of ingredients induced a higher activation in reward and cognitive areas compared to lower concentrations. Moreover, considering both ingredients at the highest concentration, the ingredient A elicited higher brain responses in brain areas involved in hedonism/pleasantness compared to ingredient B, and more specifically in the caudate nucleus and orbitofrontal cortex. Our findings shed new light in the scope of emotion regulation through olfactory modulation via sensory functional ingredients, which opens the way to further preclinical studies in animal models and translational research in the context of nutrition, welfare, and health. PRACTICAL APPLICATION: Functional food/feed ingredients are gaining interest for improving health and welfare in humans and animals. Besides representing an alternative to antibiotics for example, food ingredients and their sensory characteristics might have a positive impact on emotions and consequently on well-being. Functional brain imaging in large animals such as in the pig model is a promising approach to investigate the central and behavioural effects of food ingredients, and determine the most effective blends and concentrations to modulate internal and emotional states.
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Affiliation(s)
- Nicolas Coquery
- INRA, INSERM, Univ. Rennes, Nutrition Metabolisms and Cancer, NuMeCan, Rennes, France
| | - Sophie Menneson
- INRA, INSERM, Univ. Rennes, Nutrition Metabolisms and Cancer, NuMeCan, Rennes, France.,Phodé, Terssac, France
| | - Paul Meurice
- INRA, INSERM, Univ. Rennes, Nutrition Metabolisms and Cancer, NuMeCan, Rennes, France
| | - Régis Janvier
- INRA, INSERM, Univ. Rennes, Nutrition Metabolisms and Cancer, NuMeCan, Rennes, France
| | | | | | - David Val-Laillet
- INRA, INSERM, Univ. Rennes, Nutrition Metabolisms and Cancer, NuMeCan, Rennes, France
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Grisendi T, Reynaud O, Clarke S, Da Costa S. Processing pathways for emotional vocalizations. Brain Struct Funct 2019; 224:2487-2504. [DOI: 10.1007/s00429-019-01912-x] [Citation(s) in RCA: 4] [Impact Index Per Article: 0.7] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 04/03/2019] [Accepted: 06/12/2019] [Indexed: 01/06/2023]
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Koehler L, Fournel A, Albertowski K, Roessner V, Gerber J, Hummel C, Hummel T, Bensafi M. Impaired Odor Perception in Autism Spectrum Disorder Is Associated with Decreased Activity in Olfactory Cortex. Chem Senses 2019; 43:627-634. [PMID: 30219913 DOI: 10.1093/chemse/bjy051] [Citation(s) in RCA: 40] [Impact Index Per Article: 6.7] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 01/23/2023] Open
Abstract
Autism Spectrum Disorders (ASDs) are characterized by atypical sensory functioning in the visual, tactile, and auditory systems. Although less explored, olfactory changes have been reported in ASD patients. To explore these changes on a neural level, 18 adults with ASD and 18 healthy neurotypical controls were examined in a 2-phase study. Participants were first tested for odor threshold and odor identification. Then, (i) structural magnetic resonance (MR) images of the olfactory bulb were acquired, and (ii) a functional MR imaging olfaction study was conducted. ASD patients exhibited decreased function for odor thresholds and odor identification; this was accompanied by a relatively decreased activation in the piriform cortex. In conclusion, these findings suggest, that the known alterations in olfaction in ASD are rooted in the primary olfactory cortex.
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Affiliation(s)
- L Koehler
- Smell & Taste Clinic, Department of Otorhinolaryngology, "Technische Universität Dresden," Fetscherstraße, Dresden, Germany
| | - A Fournel
- CNRS, UMR5292, Lyon Neuroscience Research Center, University Lyon, France
| | - K Albertowski
- Department of Child and Adolescent Psychiatry and Psychotherapy, "Technische Universität Dresden," Fetscherstraße, Dresden, Germany
| | - V Roessner
- Department of Child and Adolescent Psychiatry and Psychotherapy, "Technische Universität Dresden," Fetscherstraße, Dresden, Germany
| | - J Gerber
- Department of Neuroradiology, "Technische Universität Dresden," Fetscherstraße, Dresden, Germany
| | - C Hummel
- Smell & Taste Clinic, Department of Otorhinolaryngology, "Technische Universität Dresden," Fetscherstraße, Dresden, Germany
| | - T Hummel
- Smell & Taste Clinic, Department of Otorhinolaryngology, "Technische Universität Dresden," Fetscherstraße, Dresden, Germany
| | - M Bensafi
- CNRS, UMR5292, Lyon Neuroscience Research Center, University Lyon, France
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Abstract
The senses of taste and smell developed early in evolution and are of high ecological and clinical relevance in humans. Chemosensory systems function, in large part, as hazard avoidance systems, thereby ensuring survival. Moreover, they play a critical role in nutrition and in determining the flavor of foods and beverages. Their dysfunction has been shown to be a key element of early stages of a number of diseases, including Alzheimer's and Parkinson's diseases. Advanced neuroimaging methods provide a unique means for understanding, in vivo, neural and psychological processing of smell, taste, and flavor, and how diseases can impact such processing. This chapter provides, from a neuroimaging perspective, a comprehensive overview of the anatomy and physiology involved in the odor and taste processing in the central nervous system. Some methodological challenges associated with chemosensory neuroimaging research are discussed. Multisensory integration, the mechanisms that enable holistic sensory experiences, is emphasized.
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Affiliation(s)
- Jonas K Olofsson
- Gösta Ekman Laboratory, Department of Psychology, Stockholm University, Stockholm, Sweden.
| | - Jessica Freiherr
- Department of Psychiatry and Psychotherapy, University Hospital, Friedrich Alexander University Erlangen-Nürnberg, Erlangen, Germany
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Abstract
Acupuncture is an ancient therapy with a variety of different explanatory models. A cascade of physiological effects has been reported, both in the peripheral and the central nervous system, following the insertion of a needle or light tapping of the skin. Clinical trials testing the specific claims of acupuncture have generally tried to focus on testing the efficacy of applying specific techniques and/or specified points. However, different conditions may respond differently to different modes of stimulation. Recently, it was demonstrated that both superficial and deep needling (with de qi/Hibiki) resulted in amelioration of patellofemoral pain and unpleasantness. The pleasurable aspect of the acupuncture experience has largely been ignored as it has been considered secondary to its pain alleviating effects. This aspect of acupuncture treatment is likely to be related to activation of self-appraisal and the reward system. When a patient seeks a therapist there are expectations of a specific effect. These expectations are partly based on self-relevant phenomena and self-referentia introspection and constitute the preference. Also, when asked about the effect of the treatment, processes that orientate pre-attentive anticipatory or mnemonic information and processes that mediate self-reflection and recollection are integrated together with sensory detection to enable a decision about the patient's perception of the effect of acupuncture treatment. These ‘self-appraisal’ processes are dependent on two integrated networks: a ventral medial prefrontal cortex paralimbic limbic ‘affective’ pathway and a dorsal medial prefrontal cortex cortical hippocampal ‘cognitive’ pathway. The limbic structures are implicated in the reward system and play a key role in most diseases and illness responses including chronic pain and depression, regulating mood and neuromodulatory responses (eg sensory, autonomic, and endocrine). The pleasurable and neuromodulatory aspects of acupuncture as well as ‘placebo needling’ may partly be explained by the activation or deactivation of limbic structures including the hippocampus, amygdala, and their connections with the hypothalamus. In patients with patellofemoral pain, the effects of superficial and deep needling remained for six months. These long term pain-alleviating effects have been attributed to activation of pain inhibiting systems in cortical and subcortical pathways. When considering long term effects the cortical cerebellar system needs to be taken into account. The cortical cerebellar system is probably central to the development of neural models that learn and eventually stimulate routinely executed (eg motor skills) and long term (eg pain alleviation) cognitive processes. These higher order cognitive processes are initially mediated in prefrontal cortical loci but later shift control iteratively to internal cerebellar representations of these processes. Possibly part of the long term healing effects of acupuncture may be attributed to changes in the cerebellar system thereby sparing processing load in cortical and subcortical areas. As cortical and subcortical structures are activated and/or de-activated following stimulation of receptors in the skin, disregarding site, ‘placebo or sham needling’ does not exist and conclusions drawn on the basis that it is an inert control are invalid. ‘Self’ may be seen as a shifting illusion, ceaselessly constructed and deconstructed, and the effect of acupuncture may reflect its status (as well as that of the therapist).
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Affiliation(s)
- Thomas Lundeberg
- Rehabilitation Medicine, UniversityClinic, Danderyds Hospital, Stockholm, Sweden.
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Toet A, Kaneko D, Ushiama S, Hoving S, de Kruijf I, Brouwer AM, Kallen V, van Erp JBF. EmojiGrid: A 2D Pictorial Scale for the Assessment of Food Elicited Emotions. Front Psychol 2018; 9:2396. [PMID: 30546339 PMCID: PMC6279862 DOI: 10.3389/fpsyg.2018.02396] [Citation(s) in RCA: 38] [Impact Index Per Article: 5.4] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/04/2018] [Accepted: 11/13/2018] [Indexed: 12/24/2022] Open
Abstract
Research on food experience is typically challenged by the way questions are worded. We therefore developed the EmojiGrid: a graphical (language-independent) intuitive self-report tool to measure food-related valence and arousal. In a first experiment participants rated the valence and the arousing quality of 60 food images, using either the EmojiGrid or two independent visual analog scales (VAS). The valence ratings obtained with both tools strongly agree. However, the arousal ratings only agree for pleasant food items, but not for unpleasant ones. Furthermore, the results obtained with the EmojiGrid show the typical universal U-shaped relation between the mean valence and arousal that is commonly observed for a wide range of (visual, auditory, tactile, olfactory) affective stimuli, while the VAS tool yields a positive linear association between valence and arousal. We hypothesized that this disagreement reflects a lack of proper understanding of the arousal concept in the VAS condition. In a second experiment we attempted to clarify the arousal concept by asking participants to rate the valence and intensity of the taste associated with the perceived food items. After this adjustment the VAS and EmojiGrid yielded similar valence and arousal ratings (both showing the universal U-shaped relation between the valence and arousal). A comparison with the results from the first experiment showed that VAS arousal ratings strongly depended on the actual wording used, while EmojiGrid ratings were not affected by the framing of the associated question. This suggests that the EmojiGrid is largely self-explaining and intuitive. To test this hypothesis, we performed a third experiment in which participants rated food images using the EmojiGrid without an associated question, and we compared the results to those of the first two experiments. The EmojiGrid ratings obtained in all three experiments closely agree. We conclude that the EmojiGrid appears to be a valid and intuitive affective self-report tool that does not rely on written instructions and that can efficiently be used to measure food-related emotions.
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Affiliation(s)
- Alexander Toet
- Human Factors, Netherlands Organisation for Applied Scientific Research (TNO), Soesterberg, Netherlands
| | - Daisuke Kaneko
- Human Factors, Netherlands Organisation for Applied Scientific Research (TNO), Soesterberg, Netherlands.,Kikkoman Europe R&D Laboratory B.V., Wageningen, Netherlands
| | - Shota Ushiama
- Research and Development Department, Kikkoman Corporation, Noda, Japan
| | - Sofie Hoving
- Human Factors, Netherlands Organisation for Applied Scientific Research (TNO), Soesterberg, Netherlands
| | - Inge de Kruijf
- Human Factors, Netherlands Organisation for Applied Scientific Research (TNO), Soesterberg, Netherlands
| | - Anne-Marie Brouwer
- Human Factors, Netherlands Organisation for Applied Scientific Research (TNO), Soesterberg, Netherlands
| | - Victor Kallen
- Department of Microbiology and Systems Biology, Netherlands Organisation for Applied Scientific Research (TNO), Zeist, Netherlands
| | - Jan B F van Erp
- Human Factors, Netherlands Organisation for Applied Scientific Research (TNO), Soesterberg, Netherlands.,Research Group Human Media Interaction, University of Twente, Enschede, Netherlands
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The impact of severity, course and duration of depression on olfactory function. J Affect Disord 2018; 238:194-203. [PMID: 29886199 DOI: 10.1016/j.jad.2018.05.033] [Citation(s) in RCA: 28] [Impact Index Per Article: 4.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 02/09/2018] [Revised: 04/17/2018] [Accepted: 05/25/2018] [Indexed: 01/25/2023]
Abstract
BACKGROUND People with diagnosed depression often express a reduced olfactory capacity, although previous studies exhibited mixed results. However, research focused mainly on psychiatric inpatients and potential influence variables were rarely considered. We therefore examined the influence of severity, course and duration of depression on olfactory function. METHODS 101 out-patients with depressive disorders (mean age = 37.8y, SD = 12.6y; 64 women) underwent a detailed medical anamnesis, tests of olfactory threshold and identification and tests of cognitive function. The participants were grouped according to their severity, course and duration of depression. RESULTS While severity of depressive symptoms did not affect olfactory function, course and duration of depression did. Recurrent depressive disorders were associated with reduced odor identification, and the duration of disease was negatively related to odor threshold. Those results were partly explained by reported frequent colds, which were more prevalent among long lasting depressive patients, and by poor verbal fluency, which was more frequent among recurrent depression. LIMITATIONS The interpretation is limited by the cross-sectional research design that does not allow causal interpretation, and by the assessment of medical history which was based on patients´ reports. CONCLUSIONS Our results support the idea that depression is not uniformly related to olfactory impairment, but depends on duration and course of depression. The results generate the hypothesis that reduced olfactory identification is caused by cognitive impairment in recurrent depression. Moreover, the relation between olfactory threshold and depression might be partially caused by a cumulative damage of the olfactory epithelium after frequent respiratory diseases.
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Hamakawa M, Okamoto T. The effect of different emotional states on olfactory perception: A preliminary study. FLAVOUR FRAG J 2018. [DOI: 10.1002/ffj.3469] [Citation(s) in RCA: 3] [Impact Index Per Article: 0.4] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/10/2022]
Affiliation(s)
- Masayuki Hamakawa
- Graduate School of Systems Life Sciences; Kyushu University; Fukuoka Japan
- Research Fellow of Japan Society for the Promotion of Science; Tokyo Japan
| | - Tsuyoshi Okamoto
- Graduate School of Systems Life Sciences; Kyushu University; Fukuoka Japan
- Faculty of Arts and Science; Kyushu University; Fukuoka Japan
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Kronenbuerger M, Belenghi P, Ilgner J, Freiherr J, Hummel T, Neuner I. Olfactory functioning in adults with Tourette syndrome. PLoS One 2018; 13:e0197598. [PMID: 29874283 PMCID: PMC5991349 DOI: 10.1371/journal.pone.0197598] [Citation(s) in RCA: 11] [Impact Index Per Article: 1.6] [Reference Citation Analysis] [Abstract] [MESH Headings] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 12/04/2017] [Accepted: 05/04/2018] [Indexed: 01/19/2023] Open
Abstract
Tourette syndrome is a chronic tic disorder characterized by motor and vocal tics. Comorbidities such as attention deficit hyperactivity disorder and obsessive compulsive disorder can be found. The overlap between neuroanatomical regions and neurotransmitter systems in the olfactory system and the pathophysiology of Tourette syndrome let us hypothesize altered olfactory performance in Tourette syndrome. The main objective of this study was to systematically assess olfactory functioning in subjects with Tourette syndrome and to compare it to healthy controls. We assessed 28 adults with Tourette syndrome (age 33.1±9.4 years, disease duration 23.7±9.7 years) and 28 healthy controls (age 32.9±9.0 years) matched in regard to age, sex, education and smoking habits. The “Sniffin Sticks” test battery was applied to assess odor threshold, discrimination, and identification. Additionally, the combined score of the odor threshold test, the odor discrimination test and the odor identification test of the “Sniffin Sticks” test battery was calculated. Although it was not the primary aim of this study, we assessed whether tics and comorbidity could contribute to olfactory alterations in adults with Tourette syndrome. Therefore, clinical scores were used to assess severity of tics and co-morbidity such as attention deficit hyperactivity disorder, obsessive compulsive disorder, anxiety and depression in subjects with Tourette syndrome. Pathology of the nasal cavities was excluded with rhinoendoscopy. Independent sample t-tests were applied to compare performance in olfactory tests. In the case of statistically significant differences (critical p-value: 0.05), multiple linear regression analysis was carried out to explore whether tic severity, social impairment, co-morbidity or medical treatment had an impact on the differences found. Descriptive values are reported as mean ± standard deviation. Tourette syndrome subjects showed lower combined scores (Tourette syndrome subjects 31.9 ± 5.1 versus healthy controls 35.0 ± 3.1; p = 0.007), odor identification scores (Tourette syndrome subjects 12.4 ± 2.0 versus healthy controls 13.7 ± 1.4; p = 0.008) and odor discrimination scores (Tourette syndrome subjects 12.1 ± 2.1 versus healthy controls 13.2 ± 1.6; p = 0.041) in comparison to healthy subjects, while there was no difference in odor threshold (Tourette syndrome subjects 7.3 ± 2.7 versus healthy controls 8.1 ± 2.2; p = 0.22). Seven out of 28 Tourette syndrome subjects (25%) scored in the range of the age- and sex-dependent combined score for hyposmia, while two of 28 healthy controls (7%) had a similar low combined score. None of the participants were found to have functional anosmia. Multiple linear regression analyses suggest that social impairment may a predictor for low combined score and odor identification score in Tourette syndrome subjects (p = 0.003). Compared to healthy controls, altered olfaction in adults with Tourette syndrome was found in this study. Normal odor threshold level but lower scores at tasks involving supra-threshold odor concentrations point towards a central-nervous alteration in the processing of olfactory information in Tourette syndrome.
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Affiliation(s)
- Martin Kronenbuerger
- Department of Neurology, Johns Hopkins University, Baltimore, Maryland, United States of America
- Department of Neurology, RWTH Aachen University, Aachen, Germany
- Department of Neurology, University of Greifswald, Greifswald, Germany
- * E-mail:
| | - Patrizia Belenghi
- Department of Psychiatry, Psychotherapy and Psychosomatics, RWTH Aachen University, Aachen, Germany
| | - Justus Ilgner
- Department of Otorhinolaryngology and Plastic Head and Neck Surgery, RWTH Aachen University, Aachen, Germany
| | - Jessica Freiherr
- Department of Diagnostic and Interventional Neuroradiology, RWTH Aachen University, Aachen, Germany
| | - Thomas Hummel
- Department of Otorhinolaryngology, TU Dresden, Dresden, Germany
| | - Irene Neuner
- Department of Psychiatry, Psychotherapy and Psychosomatics, RWTH Aachen University, Aachen, Germany
- JARA—Translational Brain Medicine, Aachen, Germany
- Institute of Neuroscience and Medicine 4, Forschungszentrum, Jülich, Germany
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