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Brigante G, Lazzaretti C, Ahmad A, Colzani M, Vignali F, Zoli M, Simoni M. The aporetic dialogues of Modena on gender differences: Is it all about testosterone? Episode II: Empathy. Andrology 2025. [PMID: 40220326 DOI: 10.1111/andr.70037] [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: 12/05/2024] [Revised: 03/05/2025] [Accepted: 03/22/2025] [Indexed: 04/14/2025]
Abstract
The exploration of gender differences in non-andrological fields was the core focus of a series of discussions, which took place at the Endocrinology Unit in Modena, Italy in the form of the aporetic dialogue of ancient Greece. This second episode reports the transcript of the actual debate on testosterone's role in defining empathic behavior in males and females. The two groups of discussants sustained that empathic gender differences may rely either on testosterone exposure (group 1) or on other factors (group 2). The first group supported the hypothesis that females are more empathic than males due to reduced exposure to fetal testosterone, which correlates with higher empathic scores at all ages and lower sensitivity to testosterone in adulthood. This hypothesis is also supported by evolutionary mechanisms and evidence in animal ethology. Conversely, the second group affirmed that gender differences rely on structural diversities in brain organization, hormonal factors such as vasopressin, oxytocin, and cortisol, as well as sociological aspects. An expert in neurophysiology, acting as a referee, moderated the discussion and decided whether the two theories were equivalent or one was predominant.
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Affiliation(s)
- Giulia Brigante
- Unit of Endocrinology, Department of Biomedical, Metabolic and Neural Sciences, University of Modena and Reggio Emilia, Modena, Italy
- Unit of Endocrinology, Department of Medical Specialties, Azienda Ospedaliero-Universitaria of Modena, Modena, Italy
| | - Clara Lazzaretti
- Unit of Endocrinology, Department of Biomedical, Metabolic and Neural Sciences, University of Modena and Reggio Emilia, Modena, Italy
| | - Ali Ahmad
- Unit of Endocrinology, Department of Biomedical, Metabolic and Neural Sciences, University of Modena and Reggio Emilia, Modena, Italy
| | - Massimiliano Colzani
- Unit of Endocrinology, Department of Biomedical, Metabolic and Neural Sciences, University of Modena and Reggio Emilia, Modena, Italy
| | - Filippo Vignali
- Unit of Endocrinology, Department of Biomedical, Metabolic and Neural Sciences, University of Modena and Reggio Emilia, Modena, Italy
| | - Michele Zoli
- Department of Biomedical, Metabolic and Neural Sciences, Center for Neuroscience and Neurotechnology, University of Modena and Reggio Emilia, Modena, Italy
| | - Manuela Simoni
- Unit of Endocrinology, Department of Biomedical, Metabolic and Neural Sciences, University of Modena and Reggio Emilia, Modena, Italy
- Unit of Endocrinology, Department of Medical Specialties, Azienda Ospedaliero-Universitaria of Modena, Modena, Italy
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2
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Beccherle M, Scandola M. How pain and body representations transform each other: A narrative review. J Neuropsychol 2025; 19 Suppl 1:26-41. [PMID: 39233655 PMCID: PMC11923728 DOI: 10.1111/jnp.12390] [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: 11/30/2023] [Accepted: 08/15/2024] [Indexed: 09/06/2024]
Abstract
Pain, as a multidimensional and subjective experience, intertwines with various aspects of body representation, involving sensory, affective and motivational components. This review explores the bidirectional relationship between pain and body representations, emphasizing the impact of the sense of ownership on pain perception, the transformative impact of pain on motor imagery, the effects associated with vicarious pain perception on body representations and the role of pain in the maintenance of body representations in specific clinical conditions. Literature indicates complex interactions between pain and body representations, with the sense of ownership inducing analgesic effects in some cases and hyperalgesia in others, contingent upon factors such as the appearance of the affected limb. Pain sensations inform the body on which actions might be executed without harm, and which are potentially dangerous. This information impacts on motor imagery too, showing reduced motor imagery and increased reaction times in tasks where motor imagery involves the painful body parts. Finally, contrary to the conventional view, according to which pain impairs body representation, evidence suggests that pain can serve as an informative somatosensory index, preserving or even enhancing the representation of the absent or affected body parts. This bidirectional relationship highlights the dynamic and multifaceted nature of the interplay between pain and body representations, offering insights into the adaptive nature of the central nervous system in response to perceived bodily states.
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Affiliation(s)
| | - Michele Scandola
- NPSY.Lab‐VR, Department of Human SciencesUniversity of VeronaVeronaItaly
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3
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Cenka K, Spaccasassi C, Petkovic S, Pezzetta R, Arcara G, Avenanti A. Temporal dynamics of implicit moral evaluation: From empathy for pain to mentalizing processes. Neuropsychologia 2024; 205:109033. [PMID: 39515579 DOI: 10.1016/j.neuropsychologia.2024.109033] [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: 06/06/2024] [Revised: 10/01/2024] [Accepted: 11/02/2024] [Indexed: 11/16/2024]
Abstract
To understand how we evaluate harm to others, it is crucial to consider the offender's intent and the victim's suffering. Previous research investigating event-related potentials (ERPs) during moral evaluation has been limited by small sample sizes and a priori selection of electrodes and time windows that may bias the results. To overcome these limitations, we examined ERPs in 66 healthy human adults using a data-driven analytic approach involving cluster-based permutation tests. Participants performed an implicit moral evaluation task requiring to observe scenarios depicting intentional harm (IHS), accidental harm (AHS), and neutral actions (NAS) while judging whether each scenario was set indoors or outdoors. Our results revealed two distinct clusters, peaking at ∼170 and ∼250 ms, showing differences between harm scenarios (IHS and AHS) and NAS, suggesting rapid processing of the victim's physical outcome. The difference between IHS and AHS scenarios emerged later, at ∼400 ms, potentially reflecting subsequent evaluation of the agent's intentions. Source analysis showed that brain regions associated with empathy for pain were associated with the earlier peaks at ∼170 and ∼250 ms, while the modulation of the activity of the mentalizing network was presented at ∼250 and ∼400 ms. These findings advance our understanding of the neural mechanisms underlying implicit moral evaluation. Notably, they provide electrocortical new insights for models of implicit moral evaluation, suggesting an early neural response linked to empathy for pain, with subsequent integration of empathy response with mentalizing processes, followed by later cognitive evaluations, likely reflecting the assessment of the agent's moral responsibility.
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Affiliation(s)
- Kamela Cenka
- Centro Studi e ricerche in Neuroscienze Cognitive, Dipartimento di Psicologia "Renzo Canestrari", Alma Mater Studiorum Università di Bologna, Cesena Campus, Cesena, Italy.
| | - Chiara Spaccasassi
- Centro Studi e ricerche in Neuroscienze Cognitive, Dipartimento di Psicologia "Renzo Canestrari", Alma Mater Studiorum Università di Bologna, Cesena Campus, Cesena, Italy
| | - Stella Petkovic
- Centro Studi e ricerche in Neuroscienze Cognitive, Dipartimento di Psicologia "Renzo Canestrari", Alma Mater Studiorum Università di Bologna, Cesena Campus, Cesena, Italy; Sapienza, University of Rome and CLN2S@SAPIENZA, Istituto Italiano di Tecnologia, Rome, Italy
| | | | | | - Alessio Avenanti
- Centro Studi e ricerche in Neuroscienze Cognitive, Dipartimento di Psicologia "Renzo Canestrari", Alma Mater Studiorum Università di Bologna, Cesena Campus, Cesena, Italy; Centro de Investigación en Neuropsicología y Neurociencias Cognitivas, Universidad Católica del Maule, Talca, Chile.
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4
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Duan G, Wang Y, Hou H, Li T. Effect of cognitive-behavioral therapy-based physical play intervention on empathic ability of children with intellectual disabilities. Sci Rep 2024; 14:30171. [PMID: 39627349 PMCID: PMC11615206 DOI: 10.1038/s41598-024-80066-1] [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: 06/07/2024] [Accepted: 11/14/2024] [Indexed: 12/06/2024] Open
Abstract
Purpose The purpose of this study was to investigate the potential of cognitive-behavioral therapy-based sports game intervention in enhancing empathy abilities among children with intellectual developmental disorder. Methods Thirty-one children aged 7-8, diagnosed with intellectual developmental disorder and attending mainstream schools, were enlisted for this study. They were randomly allocated to either the experimental group (n = 17) or the control group (n = 19). Both groups participated in regular physical activities of similar frequency and consistency throughout the study duration. Additionally, the experimental group underwent an 18-week cognitive-behavioral therapy-based sports game intervention. The Griffith Empathy Measure (GEM) questionnaire was administered to comprehensively evaluate the impact of the intervention program on the participants'empathy abilities. Results No statistically significant discrepancies were observed in the total scores and factor scores of the GEM pre-test between the experimental and control groups (GEM pre-test: p = 0.974 > 0.05). However, following the intervention, the experimental group exhibited notably higher total scores and factor scores in the GEM post-test compared to their pre-test scores, and these scores were significantly higher than those of the control group post-test scores. Conclusion Cognitive-behavioral therapy-based sports game intervention can effectively promote the development of empathy abilities in children with intellectual developmental disorder.
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Affiliation(s)
- Guanting Duan
- Minzu University of China College of P.E, Beijing, 100081, China
| | - Yisiqi Wang
- Foshan Hanwen foreign language school, Foshan, China
| | - HuiSheng Hou
- Minzu University of China College of P.E, Beijing, 100081, China.
| | - Tian Li
- Minzu University of China College of P.E, Beijing, 100081, China
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5
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Butti N, Urgesi C, Makris S, McGlone FP, Montirosso R, Cazzato V. Neurophysiological evidence of motor contribution to vicarious affective touch. Cereb Cortex 2024; 34:bhae441. [PMID: 39505571 PMCID: PMC11540462 DOI: 10.1093/cercor/bhae441] [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: 06/18/2024] [Revised: 09/09/2024] [Accepted: 10/21/2024] [Indexed: 11/08/2024] Open
Abstract
Understanding observed interpersonal touch, particularly the so-called affective touch targeting the CT fibers, is essential for social interactions. Research has documented that observing other people being touched activates the same cortical areas involved in direct tactile experiences. However, observing interpersonal touch also activates an inner simulation of the movements in the observer's motor system. Given the social and affective significance of CT-optimal touch, the present study tested the hypothesis that observing stroking touches targeting or not targeting the CT fibers system might distinctly influence motor resonance to vicarious touch. With this aim, we used single-pulse transcranial magnetic stimulation and motor-evoked potentials recording while participants observed video clips of interpersonal touch events at different stroking velocities. We found a modulation of motor system activity, particularly a decrease in corticospinal excitability, when observing CT-optimal touch as opposed to non-CT-optimal velocities, a mechanism that might aid in understanding the touchee's feelings during vicarious interpersonal touch. Moreover, participants with higher reliance on bodily cues to be emotionally aware showed greater motor suppression for CT-optimal compared to non-CT-optimal velocities. These results shed light on the complex interplay between motor and somatosensory systems in social touch perception and emphasize the importance of affective touch in human social interactions.
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Affiliation(s)
- Niccolò Butti
- Scientific Institute, IRCCS E. Medea, 0-3 Center for the at-Risk Infant, Via Don Luigi Monza 20, 23842 Bosisio Parini (LC), Italy
- PhD Program in Neural and Cognitive Sciences, Department of Life Sciences, University of Trieste, Via Licio Giorgieri 5, 34127 Trieste, Italy
| | - Cosimo Urgesi
- Scientific Institute, IRCCS E. Medea, Pasian di Prato, Via Cialdini 29, 33037 Pasian di Prato (UD), Italy
- Laboratory of Cognitive Neuroscience, Department of Languages and Literatures, Communication, Education and Society, University of Udine, Via Margreth 3, 33100 Udine, Italy
| | - Stergios Makris
- Department of Psychology and Research Centre for Arts and Wellbeing, Edge Hill University, St Helens Road, Ormskirk, Lancashire L39 4QP, United Kingdom
| | - Francis P McGlone
- Faculty of Science & Engineering, School of Life Sciences, Manchester Metropolitan University, All Saints Building, Manchester M15 6BH, United Kingdom
- School of Science, Department of Neuroscience and Biomedical Engineering, Aalto University, Otakaari 24, 02150 Espoo, Finland
| | - Rosario Montirosso
- Scientific Institute, IRCCS E. Medea, 0-3 Center for the at-Risk Infant, Via Don Luigi Monza 20, 23842 Bosisio Parini (LC), Italy
| | - Valentina Cazzato
- School of Psychology, Faculty of Health, Liverpool John Moores University, Tom Reilly Building, Byrom Street, Liverpool L3 3AF, United Kingdom
- Department of Cognitive, Psychological and Pedagogical Sciences, and Cultural Studies, University of Messina, Via Concezione 6, 98121 Messina, Italy
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6
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Lisi MP, Fusaro M, Aglioti SM. Visual perspective and body ownership modulate vicarious pain and touch: A systematic review. Psychon Bull Rev 2024; 31:1954-1980. [PMID: 38429591 PMCID: PMC11543731 DOI: 10.3758/s13423-024-02477-5] [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] [Accepted: 02/04/2024] [Indexed: 03/03/2024]
Abstract
We conducted a systematic review investigating the influence of visual perspective and body ownership (BO) on vicarious brain resonance and vicarious sensations during the observation of pain and touch. Indeed, the way in which brain reactivity and the phenomenological experience can be modulated by blurring the bodily boundaries of self-other distinction is still unclear. We screened Scopus and WebOfScience, and identified 31 articles, published from 2000 to 2022. Results show that assuming an egocentric perspective enhances vicarious resonance and vicarious sensations. Studies on synaesthetes suggest that vicarious conscious experiences are associated with an increased tendency to embody fake body parts, even in the absence of congruent multisensory stimulation. Moreover, immersive virtual reality studies show that the type of embodied virtual body can affect high-order sensations such as appropriateness, unpleasantness, and erogeneity, associated with the touched body part and the toucher's social identity. We conclude that perspective plays a key role in the resonance with others' pain and touch, and full-BO over virtual avatars allows investigation of complex aspects of pain and touch perception which would not be possible in reality.
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Affiliation(s)
- Matteo P Lisi
- CLN2S@Sapienza, Fondazione Istituto Italiano di Tecnologia (IIT) and Department of Psychology, Sapienza University of Rome, Viale Regina Elena 291, 00161, Rome, Italy.
- IRCCS, Santa Lucia Foundation, Via Ardeatina 306, 00179, Rome, Italy.
| | - Martina Fusaro
- CLN2S@Sapienza, Fondazione Istituto Italiano di Tecnologia (IIT) and Department of Psychology, Sapienza University of Rome, Viale Regina Elena 291, 00161, Rome, Italy
- IRCCS, Santa Lucia Foundation, Via Ardeatina 306, 00179, Rome, Italy
| | - Salvatore Maria Aglioti
- CLN2S@Sapienza, Fondazione Istituto Italiano di Tecnologia (IIT) and Department of Psychology, Sapienza University of Rome, Viale Regina Elena 291, 00161, Rome, Italy
- IRCCS, Santa Lucia Foundation, Via Ardeatina 306, 00179, Rome, Italy
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7
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Rütgen M, Lamm C. Dissecting shared pain representations to understand their behavioral and clinical relevance. Neurosci Biobehav Rev 2024; 163:105769. [PMID: 38879099 DOI: 10.1016/j.neubiorev.2024.105769] [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: 04/11/2024] [Revised: 05/29/2024] [Accepted: 06/11/2024] [Indexed: 06/22/2024]
Abstract
Accounts of shared representations posit that the experience of pain and pain empathy rely on similar neural mechanisms. Experimental research employing novel analytical and methodological approaches has made significant advances in both the identification and targeted manipulation of such shared experiences and their neural underpinnings. This revealed that painful experiences can be shared on different representational levels, from pain-specific to domain-general features, such as negative affect and its regulation. In view of direct links between such representations and social behaviors such as prosocial behavior, conditions characterized by aberrant pain processing may come along with heavy impairments in the social domain, depending on the affected representational level. This has wide potential implications in light of the high prevalence of pain-related clinical conditions, their management, and the overuse of pain medication. In this review and opinion paper, we aim to chart the path toward a better understanding of the link between shared affect and prosocial behavior.
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Affiliation(s)
- Markus Rütgen
- Department of Clinical Neuroscience, Karolinska Institutet, Solna, Sweden.
| | - Claus Lamm
- Social, Cognitive and Affective Neuroscience Unit, Department of Cognition, Emotion, and Methods in Psychology, Faculty of Psychology, University of Vienna, Vienna, Austria; Vienna Cognitive Science Hub, University of Vienna, Vienna, Austria.
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8
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Tan H, Zeng X, Ni J, Liang K, Xu C, Zhang Y, Wang J, Li Z, Yang J, Han C, Gao Y, Yu X, Han S, Meng F, Ma Y. Intracranial EEG signals disentangle multi-areal neural dynamics of vicarious pain perception. Nat Commun 2024; 15:5203. [PMID: 38890380 PMCID: PMC11189531 DOI: 10.1038/s41467-024-49541-1] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/03/2023] [Accepted: 06/07/2024] [Indexed: 06/20/2024] Open
Abstract
Empathy enables understanding and sharing of others' feelings. Human neuroimaging studies have identified critical brain regions supporting empathy for pain, including the anterior insula (AI), anterior cingulate (ACC), amygdala, and inferior frontal gyrus (IFG). However, to date, the precise spatio-temporal profiles of empathic neural responses and inter-regional communications remain elusive. Here, using intracranial electroencephalography, we investigated electrophysiological signatures of vicarious pain perception. Others' pain perception induced early increases in high-gamma activity in IFG, beta power increases in ACC, but decreased beta power in AI and amygdala. Vicarious pain perception also altered the beta-band-coordinated coupling between ACC, AI, and amygdala, as well as increased modulation of IFG high-gamma amplitudes by beta phases of amygdala/AI/ACC. We identified a necessary combination of neural features for decoding vicarious pain perception. These spatio-temporally specific regional activities and inter-regional interactions within the empathy network suggest a neurodynamic model of human pain empathy.
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Affiliation(s)
- Huixin Tan
- State Key Laboratory of Cognitive Neuroscience and Learning Beijing Normal University, Beijing, China
- IDG/McGovern Institute for Brain Research, Beijing Normal University, Beijing, China
- Beijing Key Laboratory of Brain Imaging and Connectomics, Beijing Normal University, Beijing, China
| | - Xiaoyu Zeng
- State Key Laboratory of Cognitive Neuroscience and Learning Beijing Normal University, Beijing, China
- IDG/McGovern Institute for Brain Research, Beijing Normal University, Beijing, China
- Beijing Key Laboratory of Brain Imaging and Connectomics, Beijing Normal University, Beijing, China
| | - Jun Ni
- State Key Laboratory of Cognitive Neuroscience and Learning Beijing Normal University, Beijing, China
- IDG/McGovern Institute for Brain Research, Beijing Normal University, Beijing, China
- Beijing Key Laboratory of Brain Imaging and Connectomics, Beijing Normal University, Beijing, China
| | - Kun Liang
- Beijing Tiantan Hospital, Capital Medical University, Beijing, China
| | - Cuiping Xu
- Department of Functional Neurosurgery, Xuanwu Hospital, Capital Medical University, Beijing, China
| | - Yanyang Zhang
- Department of Neurosurgery, Chinese PLA General Hospital, Beijing, China
| | - Jiaxin Wang
- State Key Laboratory of Cognitive Neuroscience and Learning Beijing Normal University, Beijing, China
- IDG/McGovern Institute for Brain Research, Beijing Normal University, Beijing, China
- Beijing Key Laboratory of Brain Imaging and Connectomics, Beijing Normal University, Beijing, China
| | - Zizhou Li
- State Key Laboratory of Cognitive Neuroscience and Learning Beijing Normal University, Beijing, China
- IDG/McGovern Institute for Brain Research, Beijing Normal University, Beijing, China
- Beijing Key Laboratory of Brain Imaging and Connectomics, Beijing Normal University, Beijing, China
| | - Jiaxin Yang
- State Key Laboratory of Cognitive Neuroscience and Learning Beijing Normal University, Beijing, China
- IDG/McGovern Institute for Brain Research, Beijing Normal University, Beijing, China
- Beijing Key Laboratory of Brain Imaging and Connectomics, Beijing Normal University, Beijing, China
| | - Chunlei Han
- Beijing Tiantan Hospital, Capital Medical University, Beijing, China
| | - Yuan Gao
- Beijing Tiantan Hospital, Capital Medical University, Beijing, China
| | - Xinguang Yu
- Department of Neurosurgery, Chinese PLA General Hospital, Beijing, China
| | - Shihui Han
- School of Psychological and Cognitive Sciences, PKU-IDG/McGovern Institute for Brain Research, Peking University, Beijing, China
| | - Fangang Meng
- Beijing Tiantan Hospital, Capital Medical University, Beijing, China.
- Chinese Institute for Brain Research, Beijing, China.
| | - Yina Ma
- State Key Laboratory of Cognitive Neuroscience and Learning Beijing Normal University, Beijing, China.
- IDG/McGovern Institute for Brain Research, Beijing Normal University, Beijing, China.
- Beijing Key Laboratory of Brain Imaging and Connectomics, Beijing Normal University, Beijing, China.
- Chinese Institute for Brain Research, Beijing, China.
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9
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Wu T, Zheng H, Zheng G, Huo T, Han S. Do we empathize humanoid robots and humans in the same way? Behavioral and multimodal brain imaging investigations. Cereb Cortex 2024; 34:bhae248. [PMID: 38884282 DOI: 10.1093/cercor/bhae248] [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: 01/30/2024] [Revised: 05/24/2024] [Accepted: 05/25/2024] [Indexed: 06/18/2024] Open
Abstract
Humanoid robots have been designed to look more and more like humans to meet social demands. How do people empathize humanoid robots who look the same as but are essentially different from humans? We addressed this issue by examining subjective feelings, electrophysiological activities, and functional magnetic resonance imaging signals during perception of pain and neutral expressions of faces that were recognized as patients or humanoid robots. We found that healthy adults reported deceased feelings of understanding and sharing of humanoid robots' compared to patients' pain. Moreover, humanoid robot (vs. patient) identities reduced long-latency electrophysiological responses and blood oxygenation level-dependent signals in the left temporoparietal junction in response to pain (vs. neutral) expressions. Furthermore, we showed evidence that humanoid robot identities inhibited a causal input from the right ventral lateral prefrontal cortex to the left temporoparietal junction, contrasting the opposite effect produced by patient identities. These results suggest a neural model of modulations of empathy by humanoid robot identity through interactions between the cognitive and affective empathy networks, which provides a neurocognitive basis for understanding human-robot interactions.
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Affiliation(s)
- Taoyu Wu
- School of Psychological and Cognitive Sciences, PKU-IDG/McGovern Institute for Brain Research, Beijing Key Laboratory of Behavior and Mental Health, Peking University, Beijing, China
| | - Huang Zheng
- School of Psychological and Cognitive Sciences, PKU-IDG/McGovern Institute for Brain Research, Beijing Key Laboratory of Behavior and Mental Health, Peking University, Beijing, China
| | - Guo Zheng
- School of Psychological and Cognitive Sciences, PKU-IDG/McGovern Institute for Brain Research, Beijing Key Laboratory of Behavior and Mental Health, Peking University, Beijing, China
| | - Tengbin Huo
- School of Psychological and Cognitive Sciences, PKU-IDG/McGovern Institute for Brain Research, Beijing Key Laboratory of Behavior and Mental Health, Peking University, Beijing, China
| | - Shihui Han
- School of Psychological and Cognitive Sciences, PKU-IDG/McGovern Institute for Brain Research, Beijing Key Laboratory of Behavior and Mental Health, Peking University, Beijing, China
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Scandola M, Beccherle M, Togni R, Caffini G, Ferrari F, Aglioti SM, Moro V. Topographic mapping of the sensorimotor qualities of empathic reactivity: A psychophysiological study in people with spinal cord injuries. Psychophysiology 2024; 61:e14547. [PMID: 38372443 DOI: 10.1111/psyp.14547] [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: 06/12/2023] [Revised: 01/03/2024] [Accepted: 02/04/2024] [Indexed: 02/20/2024]
Abstract
The experience of empathy for pain is underpinned by sensorimotor and affective dimensions which, although interconnected, are at least in part behaviorally and neurally distinct. Spinal cord injuries (SCI) induce a massive, below-lesion level, sensorimotor body-brain disconnection. This condition may make it possible to test whether sensorimotor deprivation alters specific dimensions of empathic reactivity to observed pain. To explore this issue, we asked SCI people with paraplegia and healthy controls to observe videos of painful or neutral stimuli administered to a hand (intact) or a foot (deafferented). The stimuli were displayed by means of a virtual reality set-up and seen from a first person (1PP) or third person (3PP) visual perspective. A number of measures were recorded ranging from explicit behaviors like explicit verbal reports on the videos, to implicit measures of muscular activity (like EMG from the corrugator and zygomatic muscles that may represent a proxy of sensorimotor empathy) and of autonomic reactivity (like the electrodermal response and Respiratory Sinus Arrhythmia that may represent a general proxy of affective empathy). While no across group differences in explicit verbal reports about the pain stimuli were found, SCI people exhibited reduced facial muscle reactivity to the stimuli applied to the foot (but not the hand) seen from the 1PP. Tellingly, the corrugator activity correlated with SCI participants' neuropathic pain. There were no across group differences in autonomic reactivity suggesting that SCI lesions may affect sensorimotor dimensions connected to empathy for pain.
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Affiliation(s)
- Michele Scandola
- NPSY.Lab-VR, Department of Human Sciences, University of Verona, Verona, Italy
| | - Maddalena Beccherle
- NPSY.Lab-VR, Department of Human Sciences, University of Verona, Verona, Italy
- CLN2S@Sapienza, Istituto Italiano di Tecnologia, Department of Psychology, Sapienza University of Rome, Rome, Italy
| | | | - Giulia Caffini
- NPSY.Lab-VR, Department of Human Sciences, University of Verona, Verona, Italy
| | | | - Salvatore Maria Aglioti
- CLN2S@Sapienza, Istituto Italiano di Tecnologia, Department of Psychology, Sapienza University of Rome, Rome, Italy
- Fondazione Santa Lucia, IRCCS Rome, Rome, Italy
| | - Valentina Moro
- NPSY.Lab-VR, Department of Human Sciences, University of Verona, Verona, Italy
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11
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Ben Adiva Y, Genzer S, Perry A. Beyond physical sensations: investigating empathy and prosocial behavior in vicarious pain responders. Soc Cogn Affect Neurosci 2024; 19:nsae039. [PMID: 38910333 PMCID: PMC11220461 DOI: 10.1093/scan/nsae039] [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: 04/09/2024] [Revised: 05/21/2024] [Accepted: 06/23/2024] [Indexed: 06/25/2024] Open
Abstract
Empathy, the capacity to share others' emotional experiences, has been proposed as a key motivation for altruistic behavior in both humans and animals. Sharing another's emotional experience may generate a self-embodied simulation of their emotional state, fostering understanding and promoting prosocial behavior. Vicarious pain responders report sensing physical pain when observing others in pain. Whether this ability extends to emotional experiences remains unexplored. Using both questionnaires and ecologically valid behavioral tasks, we explored whether vicarious pain responders differ from nonresponders in empathic abilities and prosocial behavior. Participants watched video clips of people describing a negative emotional life event. We operationalized several empathic abilities and responses (empathic accuracy, affective synchrony, emotional reaction, and empathic motivation) based on participants' and targets' responses during and after watching the videos. Participants were also engaged in a donation task measuring tendency for prosocial behavior. Findings reveal that compared to nonresponders, vicarious pain responders exhibit enhanced empathic accuracy, intensified emotional reactions to others' emotional pain, and a greater motivation to communicate with the target. This study marks the first behavioral evidence showcasing vicarious pain responders' empathic abilities, reactions, and motivation in response to nonphysical pain of others, expanding our knowledge of this phenomenon and its association with broader empathic abilities.
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Affiliation(s)
- Yoad Ben Adiva
- Department of Psychology, Hebrew University of Jerusalem, Jerusalem 9190501, Israel
| | - Shir Genzer
- Department of Psychology, Hebrew University of Jerusalem, Jerusalem 9190501, Israel
| | - Anat Perry
- Department of Psychology, Hebrew University of Jerusalem, Jerusalem 9190501, Israel
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12
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Pang C, Zhou Y, Han S. Temporal Unfolding of Racial Ingroup Bias in Neural Responses to Perceived Dynamic Pain in Others. Neurosci Bull 2024; 40:157-170. [PMID: 37635197 PMCID: PMC10838865 DOI: 10.1007/s12264-023-01102-0] [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: 01/18/2023] [Accepted: 06/13/2023] [Indexed: 08/29/2023] Open
Abstract
In this study, we investigated how empathic neural responses unfold over time in different empathy networks when viewing same-race and other-race individuals in dynamic painful conditions. We recorded magnetoencephalography signals from Chinese adults when viewing video clips showing a dynamic painful (or non-painful) stimulation to Asian and White models' faces to trigger painful (or neutral) expressions. We found that perceived dynamic pain in Asian models modulated neural activities in the visual cortex at 100 ms-200 ms, in the orbitofrontal and subgenual anterior cingulate cortices at 150 ms-200 ms, in the anterior cingulate cortex around 250 ms-350 ms, and in the temporoparietal junction and middle temporal gyrus around 600 ms after video onset. Perceived dynamic pain in White models modulated activities in the visual, anterior cingulate, and primary sensory cortices after 500 ms. Our findings unraveled earlier dynamic activities in multiple neural circuits in response to same-race (vs other-race) individuals in dynamic painful situations.
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Affiliation(s)
- Chenyu Pang
- School of Psychological and Cognitive Sciences, PKU-IDG/McGovern Institute for Brain Research, Beijing Key Laboratory of Behavior and Mental Health, Peking University, Beijing, 100081, China
| | - Yuqing Zhou
- CAS Key Laboratory of Behavioral Science, Institute of Psychology, Chinese Academy of Sciences, Beijing, 100101, China
- Department of Psychology, University of Chinese Academy of Sciences, Beijing, 100049, China
| | - Shihui Han
- School of Psychological and Cognitive Sciences, PKU-IDG/McGovern Institute for Brain Research, Beijing Key Laboratory of Behavior and Mental Health, Peking University, Beijing, 100081, China.
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13
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Mauchand M, Armony JL, Pell MD. The vocal side of empathy: neural correlates of pain perception in spoken complaints. Soc Cogn Affect Neurosci 2023; 19:nsad075. [PMID: 38102388 PMCID: PMC10752465 DOI: 10.1093/scan/nsad075] [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: 07/11/2023] [Revised: 11/07/2023] [Accepted: 12/11/2023] [Indexed: 12/17/2023] Open
Abstract
In the extensive neuroimaging literature on empathy for pain, few studies have investigated how this phenomenon may relate to everyday social situations such as spoken interactions. The present study used functional Magnetic Resonance Imaging (fMRI) to assess how complaints, as vocal expressions of pain, are empathically processed by listeners and how these empathic responses may vary based on speakers' vocal expression and cultural identity. Twenty-four French participants listened to short utterances describing a painful event, which were either produced in a neutral-sounding or complaining voice by both in-group (French) and out-group (French Canadian) speakers. Results suggest that the perception of suffering from a complaining voice increased activity in the emotional voice areas, composed of voice-sensitive temporal regions interacting with prefrontal cortices and the amygdala. The Salience and Theory of Mind networks, associated with affective and cognitive aspects of empathy, also showed prosody-related activity and specifically correlated with behavioral evaluations of suffering by listeners. Complaints produced by in- vs out-group speakers elicited sensorimotor and default mode activity, respectively, suggesting accent-based changes in empathic perspective. These results, while reaffirming the role of key networks in tasks involving empathy, highlight the importance of vocal expression information and social categorization processes when perceiving another's suffering during social interactions.
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Affiliation(s)
- Maël Mauchand
- School of Communication Sciences and Disorders, McGill University, Montréal, QC H3A1G1, Canada
- Centre for Research on Brain, Language, and Music (CRBLM), Montréal, QC H3G2A8, Canada
- Swiss Center for Affective Sciences, University of Geneva, Geneva 1202, Switzerland
| | - Jorge L Armony
- Centre for Research on Brain, Language, and Music (CRBLM), Montréal, QC H3G2A8, Canada
- Douglas Mental Health University Institute, Verdun, QC H4H1R3, Canada
- Department of Psychiatry, McGill University, Montréal, QC H3A1A1, Canada
| | - Marc D Pell
- School of Communication Sciences and Disorders, McGill University, Montréal, QC H3A1G1, Canada
- Centre for Research on Brain, Language, and Music (CRBLM), Montréal, QC H3G2A8, Canada
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14
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Rizzo G, Martino D, Avanzino L, Avenanti A, Vicario CM. Social cognition in hyperkinetic movement disorders: a systematic review. Soc Neurosci 2023; 18:331-354. [PMID: 37580305 DOI: 10.1080/17470919.2023.2248687] [Citation(s) in RCA: 3] [Impact Index Per Article: 1.5] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 07/30/2022] [Revised: 07/10/2023] [Accepted: 08/09/2023] [Indexed: 08/16/2023]
Abstract
Numerous lines of research indicate that our social brain involves a network of cortical and subcortical brain regions that are responsible for sensing and controlling body movements. However, it remains unclear whether movement disorders have a systematic impact on social cognition. To address this question, we conducted a systematic review examining the influence of hyperkinetic movement disorders (including Huntington disease, Tourette syndrome, dystonia, and essential tremor) on social cognition. Following the PRISMA guidelines and registering the protocol in the PROSPERO database (CRD42022327459), we analyzed 50 published studies focusing on theory of mind (ToM), social perception, and empathy. The results from these studies provide evidence of impairments in ToM and social perception in all hyperkinetic movement disorders, particularly during the recognition of negative emotions. Additionally, individuals with Huntington's Disease and Tourette syndrome exhibit empathy disorders. These findings support the functional role of subcortical structures (such as the basal ganglia and cerebellum), which are primarily responsible for movement disorders, in deficits related to social cognition.
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Affiliation(s)
- Gaetano Rizzo
- Dipartimento di Scienze Cognitive, Psicologiche, Pedagogiche e degli studi culturali, Università di Messina, Messina, Italy
| | - Davide Martino
- Department of Clinical Neurosciences, Hotchkiss Brain Institute, Alberta Children's Hospital Research Institute, University of Calgary, Calgary, Alberta, Canada
| | - Laura Avanzino
- Department of Experimental Medicine, Section of Human Physiology, University of Genoa, Genoa, Italy
| | - Alessio Avenanti
- Centro studi e ricerche in Neuroscienze Cognitive, Dipartimento di Psicologia "Renzo Canestrari", Campus di Cesena, Alma Mater Studiorum Università di Bologna, Cesena, Italy
- Centro de Investigación en Neuropsicología y Neurociencias Cognitivas, Universidad Católica del Maule, Talca, Chile
| | - Carmelo Mario Vicario
- Dipartimento di Scienze Cognitive, Psicologiche, Pedagogiche e degli studi culturali, Università di Messina, Messina, Italy
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15
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Kalénine S, Decroix J. The pain hidden in your hands: Facial expression of pain reduces the influence of goal-related information in action recognition. Neuropsychologia 2023; 189:108658. [PMID: 37574186 DOI: 10.1016/j.neuropsychologia.2023.108658] [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: 02/01/2023] [Revised: 07/09/2023] [Accepted: 08/08/2023] [Indexed: 08/15/2023]
Abstract
The involvement of the sensorimotor system in the perception of painful actions has been repeatedly demonstrated. Yet the cognitive processes corresponding to sensorimotor activations have not been identified. In particular, the respective role of higher-level and lower-level action representations such as goals and grips in the recognition of painful actions is not clear. Previous research has shown that in a neutral context, higher-level action representations (goals) are prioritized over lower-level action representations (grips) and guide action recognition. The present study evaluates to what extent the general priority given to goal-related information in the processing of visual actions can be modulated by a context of pain. We used the action violation paradigm developed by van Elk et al. (2008). In the present action tasks, participants had to judge whether the grip or the goal of object-directed actions displayed in photographs was correct or not. The actress in the photograph could show either a neutral facial expression or a facial expression of pain. In the control task, they had to judge whether the actress expressed pain. In the action tasks, goals influenced grip judgements more than grips influenced goal judgements overall, corroborating the priority given to goal-related information previously reported. Critically, the impact of irrelevant goal-related information on the identification of incorrect grips disappeared in the pain context. Moreover, judgements in the control task were similarly influenced by grip and goal-related information. Results suggest that a context of pain reduces the reliance on higher-level action for action judgments. Findings provide novel directions regarding the cognitive and brain mechanisms involved in action processing in painful situations and support pluralist views of action understanding.
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Affiliation(s)
- Solène Kalénine
- Univ. Lille, CNRS, UMR 9193 - SCALab - Sciences Cognitives et Sciences Affectives, F-59000, Lille, France.
| | - Jérémy Decroix
- Univ. Lille, CNRS, UMR 9193 - SCALab - Sciences Cognitives et Sciences Affectives, F-59000, Lille, France
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16
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Fiori F, Ciricugno A, Cattaneo Z, Ferrari C. The Impact of the Perception of Primary Facial Emotions on Corticospinal Excitability. Brain Sci 2023; 13:1291. [PMID: 37759892 PMCID: PMC10527337 DOI: 10.3390/brainsci13091291] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.5] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 08/07/2023] [Revised: 09/01/2023] [Accepted: 09/04/2023] [Indexed: 09/29/2023] Open
Abstract
The link between emotional experience and motor body responses has long been acknowledged. A well-established approach to exploring the effect of the perception of emotional stimuli on the motor system is measuring variations in the excitability of the corticospinal tract (CSE) through motor-evoked potentials (MEP) elicited via transcranial magnetic stimulation (TMS). Previous evidence has indicated a selective increase in MEP amplitude while participants view emotional stimuli, such as emotional facial expressions, compared to neutral cues. However, it is still not clear whether this effect depends on the specific emotional meaning conveyed by the stimulus. In the present study, we explored whether viewing faces expressing the primary emotions compared to faces with a neutral expression affects individuals' CSE, measured using TMS-elicited MEPs. Specifically, we elicited MEPs from the left motor cortex (M1) while participants passively viewed the same faces expressing either anger, fear, disgust, happiness, sadness, surprise, and no emotion (in different blocks). We found that the observation of fearful, angry, disgusted, and happy facial expressions was associated with a significant increase in the MEPs' amplitude compared to neutral facial expressions, with a comparable enhancement in the CSE occurring across these emotions. In turn, viewing sad and surprised faces did not modulate the CSE. Overall, our findings suggest that only facial expressions that signal (real or potential) danger or a rewarding stimulus, but not emotional facial expressions per se, are capable of activating action-related mechanisms.
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Affiliation(s)
- Francesca Fiori
- Research Unit of Neurophysiology and Neuroengineering of Human-Technology Interaction (NeXTlab), Department of Medicine, Campus Bio-Medico University, 00128 Roma, Italy;
| | - Andrea Ciricugno
- Social Experimental Psychology Unit, IRCCS Mondino Foundation, 27100 Pavia, Italy; (A.C.); (C.F.)
- Department of Brain and Behavioral Sciences, University of Pavia, 27100 Pavia, Italy
| | - Zaira Cattaneo
- Social Experimental Psychology Unit, IRCCS Mondino Foundation, 27100 Pavia, Italy; (A.C.); (C.F.)
- Department of Human and Social Sciences, University of Bergamo, 24129 Bergamo, Italy
| | - Chiara Ferrari
- Social Experimental Psychology Unit, IRCCS Mondino Foundation, 27100 Pavia, Italy; (A.C.); (C.F.)
- Department of Humanities, University of Pavia, 27100 Pavia, Italy
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17
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Zebarjadi N, Levy J. Neural shifts in alpha rhythm's dual functioning during empathy maturation. Brain Behav 2023; 13:e3110. [PMID: 37334437 PMCID: PMC10498088 DOI: 10.1002/brb3.3110] [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: 12/16/2022] [Revised: 05/18/2023] [Accepted: 05/19/2023] [Indexed: 06/20/2023] Open
Abstract
INTRODUCTION Empathy is a social-cognitive process that operates by relying mainly on the suppression of the cortical alpha rhythm. This phenomenon has been evidenced in dozens of electrophysiological studies targeting adult human subjects. Yet, recent neurodevelopmental studies indicated that at a younger age, empathy involves reversed brain responses (e.g., alpha enhancement patterns). In this multimodal study, we capture neural activity at the alpha range, and hemodynamic response and target subjects at approximately 20 years old as a unique time window in development that allows investigating both low-alpha suppression and high-alpha enhancement. We aim to further investigate the functional role of low-alpha power suppression and high-alpha power enhancement during empathy development. METHODS Brain data from 40 healthy individuals were recorded in two consecutive sessions of magnetoencephalography (MEG) and functional magnetic resonance imaging (fMRI) while subjects perceived vicarious physical pain or no pain. RESULTS MEG revealed that the alpha pattern shift during empathy happens in an all-or-none pattern: power enhancement before 18 and suppression after 18 years of age. Additionally, MEG and fMRI highlight a correspondence between high-alpha power increase and blood-oxygen-level-dependent (BOLD) decrease before 18, but low-alpha power decrease and BOLD increase after 18. Importantly, this neurodevelopmental transition was not revealed by four other measures: self-reported (a) ratings of the task stimuli, (b) ratings of naturalistic vignettes of vicarious pain, (c) trait empathy, or neural data from (d) a control neuroimaging task. DISCUSSION Findings suggest that at the critical age of around 18, empathy is underpinned by an all-or-none transition from high-alpha power enhancement and functional inhibition to low-alpha power suppression and functional activation in particular brain regions, possibly indicating a marker of maturation in empathic ability. This work advances a recent neurodevelopmental line of studies and provides insight into the functional maturation of empathy at the coming of age.
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Affiliation(s)
- Niloufar Zebarjadi
- Department of Neuroscience and Biomedical EngineeringAalto UniversityEspooFinland
| | - Jonathan Levy
- Department of Neuroscience and Biomedical EngineeringAalto UniversityEspooFinland
- Baruch Ivcher School of PsychologyReichman UniversityHerzliyaIsrael
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18
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Kaczmarska M. Valuing embodiment: insights from dance practice among people living with dementia. Front Neurol 2023; 14:1174157. [PMID: 37342779 PMCID: PMC10277497 DOI: 10.3389/fneur.2023.1174157] [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: 02/25/2023] [Accepted: 05/08/2023] [Indexed: 06/23/2023] Open
Abstract
There is a growing appreciation for the ability of person-centered arts-based approaches to extend multiple domains of brain health of people living with dementia. Dance is a multi-modal artistic engagement which has positive impacts on cognition, mobility and the emotional and social aspects of brain health. Although research into multiple domains of brain health among older adults and people living with dementia is promising, several gaps remain, specifically in understanding the benefits of co-creative and improvisational dance practices. Collaborative research between dancers, researchers, people living with dementia and care partners is needed to design and evaluate future research on dance and to determine relevance and usability. Furthermore, the respective praxes and experience of researchers, dance artists and people living with dementia contribute distinctly and uniquely to the identification and the assignment of value to dance in the context of the lives of people living with dementia. In this manuscript the author, a community-based dance artist, creative aging advocate and Atlantic Fellow for Equity in Brain Health, discusses current challenges and gaps in the understanding of the value of dance for and with people living with dementia and how transdisciplinary collaboration between neuroscientists, dance artists and people living with dementia can advance collective comprehension and implementation of dance practice.
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Affiliation(s)
- Magda Kaczmarska
- Global Brain Health Institute, San Francisco, CA, United States
- Foundation Dementia Action Alliance Poland, Sopot, Poland
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19
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McCommon SA, Turk B, Roach A, Jelsone-Swain L. Acetaminophen changes Mu rhythm power related to pain empathy. Neuropsychologia 2023; 184:108544. [PMID: 36948452 DOI: 10.1016/j.neuropsychologia.2023.108544] [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: 05/12/2022] [Revised: 01/30/2023] [Accepted: 03/14/2023] [Indexed: 03/24/2023]
Abstract
Empathy is an intricate ability that entails the subjective feeling and understanding of emotions someone else may be experiencing. Acetaminophen, the active ingredient found in Tylenol, is among the most common pain medications consumed. There is new evidence, however, that suggests this common analgesic may also dampen empathic processes. However, no previous study has investigated the effect acetaminophen may have on pain empathy or mu power during a pain empathy task. Therefore, participants were randomly assigned to either an experimental (acetaminophen) or control (sugar) group in a double-blinded experimental research design aimed to measure mu power (using EEG) and behavioral responses to painful and non-painful images. Participants in the experimental group were administered 1000 mg of acetaminophen, and it was verified that participants were unaware which group they were assigned. We found that mu suppression was greater in the acetaminophen group, which was strongest at electrode C3. Additionally, mu power differences between painful and non-painful images were related to trait empathy, and mu power during the painful images were positively correlated with empathy scores. Results from this study suggest that in addition to reducing physical pain, acetaminophen may also change the brain response when perceiving others in pain. The implications of these findings could possibly lead to changes in how we prescribe and administer this common drug.
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Affiliation(s)
- Sara Anne McCommon
- Department of Psychology University of South Carolina Aiken, 471 University Parkway, Aiken, SC, 29801, USA
| | - Brooke Turk
- Department of Psychology University of South Carolina Aiken, 471 University Parkway, Aiken, SC, 29801, USA
| | - Alexandra Roach
- Department of Psychology University of South Carolina Aiken, 471 University Parkway, Aiken, SC, 29801, USA
| | - Laura Jelsone-Swain
- Department of Psychology University of South Carolina Aiken, 471 University Parkway, Aiken, SC, 29801, USA.
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20
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Vickers BD, Seidler RD, Stansfield RB, Weissman DH, Preston SD. Altruistic responses to the most vulnerable involve sensorimotor processes. Front Psychiatry 2023; 14:1140986. [PMID: 36970269 PMCID: PMC10036353 DOI: 10.3389/fpsyt.2023.1140986] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 01/09/2023] [Accepted: 02/23/2023] [Indexed: 03/12/2023] Open
Abstract
IntroductionWhy do people help strangers? Prior research suggests that empathy motivates bystanders to respond to victims in distress. However, this work has revealed relatively little about the role of the motor system in human altruism, even though altruism is thought to have originated as an active, physical response to close others in immediate need. We therefore investigated whether a motor preparatory response contributes to costly helping.MethodsTo accomplish this objective, we contrasted three charity conditions that were more versus less likely to elicit an active motor response, based on the Altruistic Response Model. These conditions described charities that (1) aided neonates versus adults, (2) aided victims requiring immediate versus preparatory support, and (3) provided heroic versus nurturant aid. We hypothesized that observing neonates in immediate need would elicit stronger brain activation in motor-preparatory regions.ResultsConsistent with an evolutionary, caregiving-based theory of altruism, participants donated the most to charities that provided neonates with immediate, nurturant aid. Critically, this three-way donation interaction was associated with increased BOLD signal and gray matter volume in motor-preparatory regions, which we identified in an independent motor retrieval task.DiscussionThese findings advance the field of altruism by shifting the spotlight from passive emotional states toward action processes that evolved to protect the most vulnerable members of our group.
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Affiliation(s)
- Brian D. Vickers
- Department of Psychology, University of Michigan, Ann Arbor, MI, United States
| | - Rachael D. Seidler
- Department of Psychology, University of Michigan, Ann Arbor, MI, United States
- University of Michigan School of Kinesiology, Ann Arbor, MI, United States
| | - R. Brent Stansfield
- Department of Medical Education, University of Michigan, Ann Arbor, MI, United States
| | - Daniel H. Weissman
- Department of Psychology, University of Michigan, Ann Arbor, MI, United States
| | - Stephanie D. Preston
- Department of Psychology, University of Michigan, Ann Arbor, MI, United States
- *Correspondence: Stephanie D. Preston,
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21
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Antico L, Corradi-Dell’Acqua C. Far from the eyes, far from the heart: COVID-19 confinement dampened sensitivity to painful facial features. Q J Exp Psychol (Hove) 2023; 76:554-567. [PMID: 35388721 PMCID: PMC9936438 DOI: 10.1177/17470218221094772] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.5] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/17/2022]
Abstract
In the last 2 years, governments of many countries imposed heavy social restrictions to contain the spread of the COVID-19 virus, with consequent increase of bad mood, distress, or depression for the people involved. Few studies investigated the impact of these restrictive measures on individual social proficiency, and specifically the processing of emotional facial information, leading to mixed results. The present research aimed at investigating systematically whether, and to which extent, social isolation influences the processing of facial expressions. To this end, we manipulated the social exclusion experimentally through the well-known Cyberball game (within-subject factor), and we exploited the occurrence of the lockdown for the Swiss COVID-19 first wave by recruiting participants before and after being restricted at home (grouping factor). We then tested whether either form of social segregation influenced the processing of pain, disgust, or neutral expressions, across multiple tasks probing access to different components of affective facial responses (state-specific, shared across states). We found that the lockdown (but not game-induced exclusion) affected negatively the processing of pain-specific information, without influencing other components of the affective facial response related to disgust or broad unpleasantness. In addition, participants recruited after the confinement reported lower scores in empathy questionnaires. These results suggest that social isolation affected negatively individual sensitivity to other people's affect and, with specific reference to the processing of facial expressions, the processing of pain-diagnostic information.
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Affiliation(s)
- Lia Antico
- Lia Antico, Theory of Pain Laboratory, Department of Psychology, Faculty of Psychology and Educational Sciences, University of Geneva, Campus Biotech, Chemin des mines 9, 1211 Geneva, Switzerland.
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22
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Galang CM, Obhi SS. Empathic pain observation does not influence automatic imitation in an online setting. Exp Brain Res 2023; 241:263-276. [PMID: 36494458 DOI: 10.1007/s00221-022-06508-2] [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: 06/08/2022] [Accepted: 11/10/2022] [Indexed: 12/14/2022]
Abstract
Previous research has shown that empathic pain observation can lead to motor facilitation in the form of faster reaction times. However, it is unclear whether participants are focusing on the others' pain or simply focusing on their own discomfort/distress (from watching the videos) during the task. This is an important issue as self- vs other-oriented focusing plays a key role in empathic processing. To address this issue, we combined empathic pain observation with the automatic imitation task (AIT). Previous work has shown that AIT effects are smaller after experiencing pain, which has been interpreted as the result of the experience of pain leading to a self-oriented focus. If empathic pain observation similarly leads to a self-oriented focus, then we should expect similar AIT results after pain observation (smaller AIT effects); however, if it instead leads to an other-oriented focus, then we should see the opposite (larger AIT effects). Although we found initial evidence for the latter hypothesis (Experiment 1), subsequent failed replications suggests that we do not have sufficient evidence to claim that pain observation influences automatic imitation one way or the other (Experiment 2 and 3). We discuss some possible reasons for finding null results in these experiments and suggest future avenues of research to better elucidate this topic.
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Affiliation(s)
- Carl Michael Galang
- Social Brain, Body and Action Lab, Department of Psychology, Neuroscience and Behaviour, McMaster University, Hamilton, Canada. .,Social Intelligence Lab, Institute for Psychology and The Berlin School of Mind and Brain, Humboldt University of Berlin, Berlin, Germany.
| | - Sukhvinder S Obhi
- Social Brain, Body and Action Lab, Department of Psychology, Neuroscience and Behaviour, McMaster University, Hamilton, Canada.
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23
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Walsh MJM, Pagni B, Monahan L, Delaney S, Smith CJ, Baxter L, Braden BB. Sex-related brain connectivity correlates of compensation in adults with autism: insights into female protection. Cereb Cortex 2022; 33:316-329. [PMID: 35212373 PMCID: PMC9837609 DOI: 10.1093/cercor/bhac069] [Citation(s) in RCA: 6] [Impact Index Per Article: 2.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 11/16/2021] [Revised: 01/31/2022] [Accepted: 02/01/2022] [Indexed: 01/19/2023] Open
Abstract
The male preponderance in autism spectrum disorder (ASD) led to the hypothesis that aspects of female biology are protective against ASD. Females with ASD (ASD-F) report more compensatory behaviors (i.e. "camouflaging") to overcome ASD-related social differences, which may be a mechanism of protection. No studies have examined sex-related brain pathways supporting camouflaging in ASD-F, despite its potential to inform mechanisms underlying the ASD sex bias. We used functional connectivity (FC) to investigate "sex-atypical" and "sex-typical" FC patterns linked to camouflaging in adults with ASD and examined multimodal coherence of findings via structural connectometry. Exploratory associations with cognitive/emotional functioning examined the adaptive nature of FC patterns. We found (i) "sex-atypical" FC patterns linked to camouflaging in the hypothalamus and precuneus and (ii) "sex-typical" patterns in the right anterior cingulate and anterior parahippocampus. Higher hypothalamic FC with a limbic reward cluster also correlated with better cognitive control/emotion recognition. Structural connectometry validated FC results with consistent brain pathways/effect patterns implicated in ASD-F. In summary, "male-typical" and "female-typical" brain connectivity patterns support camouflaging in ASD-F in circuits implicated in reward, emotion, and memory retrieval. "Sex-atypical" results are consistent with fetal steroidogenic/neuroinflammatory hypotheses. However, female genetics/biology may contribute to "female-typical" patterns implicated in camouflaging.
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Affiliation(s)
- Melissa J M Walsh
- College of Health Solutions, Arizona State University, Tempe, AZ 85281, USA
| | - Broc Pagni
- College of Health Solutions, Arizona State University, Tempe, AZ 85281, USA
| | - Leanna Monahan
- College of Health Solutions, Arizona State University, Tempe, AZ 85281, USA
| | - Shanna Delaney
- College of Health Solutions, Arizona State University, Tempe, AZ 85281, USA
| | | | | | - B Blair Braden
- College of Health Solutions, Arizona State University, Tempe, AZ 85281, USA
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24
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The bodily fundament of empathy: The role of action, nonaction-oriented, and interoceptive body representations. Psychon Bull Rev 2022:10.3758/s13423-022-02231-9. [PMID: 36510091 DOI: 10.3758/s13423-022-02231-9] [Citation(s) in RCA: 3] [Impact Index Per Article: 1.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Accepted: 11/27/2022] [Indexed: 12/14/2022]
Abstract
Mental representations with bodily contents or in various bodily formats have been suggested to play a pivotal role in social cognition, including empathy. However, there is a lack of systematic studies investigating, in the same sample of participants and using an individual differences approach, whether and to what extent the sensorimotor, perceptual, and interoceptive representations of the body could fulfill an explanatory role in the empathic abilities.To address this goal, we carried out two studies in which healthy adults were given measures of interoceptive sensibility (IS), action (aBR), and nonaction-oriented body representations (NaBR), and affective, cognitive, and motor empathy. A higher tendency to be self-focused on interoceptive signals predicted higher affective, cognitive, and motor empathy levels. A better performance in tasks probing aBR and NaBR predicted, respectively, higher motor and cognitive empathy levels.These findings support the view that the various facets of the empathic response are differently grounded in the body since they diversely involve representations with a different bodily format.Individual differences in the focus on one's internal body state representation can directly modulate all the components of the empathic experience. Instead, a body representation used interpersonally to represent both one's own body and others' bodies, in particular in its spatial specificity, could be necessary to accurately understand other people's minds (cognitive empathy), while a sensorimotor body representation used to represent both one's own body and others' bodies actions, could be fundamental for the self-awareness of feelings expressed in actions (motor empathy).
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Flechsenhar A, Kanske P, Krach S, Korn C, Bertsch K. The (un)learning of social functions and its significance for mental health. Clin Psychol Rev 2022; 98:102204. [PMID: 36216722 DOI: 10.1016/j.cpr.2022.102204] [Citation(s) in RCA: 9] [Impact Index Per Article: 3.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 08/09/2021] [Revised: 08/11/2022] [Accepted: 09/23/2022] [Indexed: 01/27/2023]
Abstract
Social interactions are dynamic, context-dependent, and reciprocal events that influence prospective strategies and require constant practice and adaptation. This complexity of social interactions creates several research challenges. We propose a new framework encouraging future research to investigate not only individual differences in capacities relevant for social functioning and their underlying mechanisms, but also the flexibility to adapt or update one's social abilities. We suggest three key capacities relevant for social functioning: (1) social perception, (2) sharing emotions or empathizing, and (3) mentalizing. We elaborate on how adaptations in these capacities may be investigated on behavioral and neural levels. Research on these flexible adaptations of one's social behavior is needed to specify how humans actually "learn to be social". Learning to adapt implies plasticity of the relevant brain networks involved in the underlying social processes, indicating that social abilities are malleable for different contexts. To quantify such measures, researchers need to find ways to investigate learning through dynamic changes in adaptable social paradigms and examine several factors influencing social functioning within the three aformentioned social key capacities. This framework furthers insight concerning individual differences, provides a holistic approach to social functioning, and may improve interventions for ameliorating social abilities in patients.
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Affiliation(s)
- Aleya Flechsenhar
- Department Clinical Psychology and Psychotherapy, Ludwig-Maximilians-University Munich, Germany.
| | - Philipp Kanske
- Institute of Clinical Psychology and Psychotherapy, Technische Universität Dresden, Germany
| | - Sören Krach
- Department of Psychiatry and Psychotherapy, University of Lübeck, Germany
| | - Christoph Korn
- Section Social Neuroscience, Department of General Psychiatry, Center for Psychosocial Medicine, Heidelberg University, Heidelberg, Germany
| | - Katja Bertsch
- Department Clinical Psychology and Psychotherapy, Ludwig-Maximilians-University Munich, Germany; NeuroImaging Core Unit Munich (NICUM), University Hospital LMU, Munich, Germany; Department of General Psychiatry, Center for Psychosocial Medicine, Heidelberg University, Heidelberg, Germany
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26
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The influence of agent’s gender on observer’s response in different action contexts. CURRENT PSYCHOLOGY 2022. [DOI: 10.1007/s12144-022-03980-5] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/15/2022]
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27
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Williams R, Trentini C. Two modes of being together: The levels of intersubjectivity and human relatedness in neuroscience and psychoanalytic thinking. Front Hum Neurosci 2022; 16:981366. [PMID: 36158615 PMCID: PMC9494563 DOI: 10.3389/fnhum.2022.981366] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 06/29/2022] [Accepted: 08/10/2022] [Indexed: 11/30/2022] Open
Abstract
The notion of intersubjectivity has achieved a primary status in contemporary psychoanalytic debate, stimulating new theoretical proposals as well as controversies. This paper presents an overview of the main contributions on inter-subjectivity in the field of neurosciences. In humans as well as-probably-in other species, the ability for emotional resonance is guaranteed early in development. Based on this capacity, a primary sense of connectedness is established that can be defined inter-subjective in that it entails sharing affective states and intentions with caregivers. We propose to define such a form of inter-subjectivity as contingent, since the infant's early abilities for resonance do not imply the more generalized capacity to permanently conceive of the relationship outside the realm of current interactions and the infant-caregiver's mutual correspondence of internal states. This form of connection, hence, results in a self-referential, bodily, and affectively codified, context- and time dependent, like-me experience of interactions. The gradual maturation of brain structures and processes as well as interactive experiences allow proper intersubjectivity exchanges, grounded on new intentional and representational capacities, to evolve. In this more mature form of intersubjectivity, the individual is allowed to conceive of her own psychic space both as distinct and as possibly connected with the other's contents and experience, even in the absence of current behavioral indicators of such correspondence. This multi-layered model of intersubjectivity, which is embraced by current neuroscience research, seems to allow for new interpretations of psychoanalytic models of human relatedness based upon classic clinical observations.
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Affiliation(s)
- Riccardo Williams
- Department of Dynamic and Clinical Psychology, and Health Studies, Sapienza University of Rome, Rome, Italy
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28
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Li X, Lou W, Zhang W, Tong RKY, Hu L, Peng W. Ongoing first-hand pain facilitates somatosensory resonance but inhibits affective sharing in empathy for pain. Neuroimage 2022; 263:119599. [PMID: 36049698 DOI: 10.1016/j.neuroimage.2022.119599] [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: 02/04/2022] [Revised: 08/05/2022] [Accepted: 08/28/2022] [Indexed: 10/31/2022] Open
Abstract
Alterations of empathy for others' pain among patients with chronic pain remained inconsistent. Here, applying a capsaicin-based ongoing pain model on healthy participants, this study investigated how ongoing first-hand pain influences empathic reactions to vicarious pain stimuli. Healthy participants were randomly treated with topical capsaicin cream (capsaicin group) or hand cream (control group) on the left forearm. Video clips showing limbs in painful and non-painful situations were used to induce empathic responses. The capsaicin group showed greater empathic neural responses in the right primary somatosensory cortex (S1) than the control group but smaller responses in the left anterior insula (AI) accompanied with smaller empathic pain-intensity ratings. Notably, the intensity of ongoing pain negatively correlated with empathy-related neural responses in the left AI. Inter-subject phase synchronization analysis was used to assess stimulus-dependent dynamic functional connectivity within or between brain regions engaged in pain empathy. The capsaicin group showed greater empathy-related neural synchronization within S1 and between S1 and AI, but less synchronization within AI and between AI and MCC. Behaviorally, the differential inter-subject pain-intensity rating alignment between painful and non-painful videos was more positive for the capsaicin group than for the control group, and this effect was partially mediated by the inter-subject neural synchronization between S1 and AI. These results suggest that ongoing first-hand pain facilitates neural activation and synchronization within brain regions associated with empathy-related somatosensory resonance at the cost of inhibiting activation and synchronization within brain regions engaged in empathy-related affective sharing.
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Affiliation(s)
- Xiaoyun Li
- School of Psychology, Shenzhen University, Shenzhen, China
| | - Wutao Lou
- Department of Biomedical Engineering, The Chinese University of Hong Kong, Hong Kong, China
| | - Wenyun Zhang
- School of Psychology, Shenzhen University, Shenzhen, China
| | - Raymond Kai-Yu Tong
- Department of Biomedical Engineering, The Chinese University of Hong Kong, Hong Kong, China
| | - Li Hu
- CAS Key Laboratory of Mental Health, Institute of Psychology, Chinese Academy of Sciences, Beijing, China; Department of Psychology, University of Chinese Academy of Sciences, Beijing, China
| | - Weiwei Peng
- School of Psychology, Shenzhen University, Shenzhen, China.
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29
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Spaccasassi C, Zanon M, Borgomaneri S, Avenanti A. Mu rhythm and corticospinal excitability capture two different frames of motor resonance: A TMS/EEG co-registration study. Cortex 2022; 154:197-211. [DOI: 10.1016/j.cortex.2022.04.019] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.3] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 11/19/2021] [Revised: 03/28/2022] [Accepted: 04/18/2022] [Indexed: 11/03/2022]
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30
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De Pascalis V, Vecchio A. The influence of EEG oscillations, heart rate variability changes, and personality on self-pain and empathy for pain under placebo analgesia. Sci Rep 2022; 12:6041. [PMID: 35410362 PMCID: PMC9001726 DOI: 10.1038/s41598-022-10071-9] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.3] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 12/05/2021] [Accepted: 04/01/2022] [Indexed: 12/30/2022] Open
Abstract
We induced placebo analgesia (PA), a phenomenon explicitly attenuating the self-pain feeling, to assess whether this resulted in reduced empathy pain when witnessing a confederate undergoing such pain experience. We recorded EEG and electrocardiogram during a painful Control and PA treatment in healthy adults who rated their experienced pain and empathy for pain. We derived HRV changes and, using wavelet analysis of non-phase-locked event-related EEG oscillations, EEG spectral power differences for self-pain and other-pain conditions. First-hand PA reduced self-pain and self-unpleasantness, whereas we observed only a slight decrease in other unpleasantness. We derived linear combinations of HRV and EEG band power changes significantly associated with self-pain and empathy for pain changes using PCAs. Lower Behavioral Inhibition System scores predicted self-pain reduction through the mediating effect of a relative HR-slowing and a decreased midline ϑ-band (4-8 Hz) power factor moderated by lower Fight-Flight-Freeze System trait scores. In the other-pain condition, we detected a direct positive influence of Total Empathic Ability on the other-pain decline with a mediating role of the midline β2-band (22-30 Hz) power reduction. These findings suggest that PA modulation of first-hand versus other pain relies on functionally different physiological processes involving different personality traits.
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Affiliation(s)
- Vilfredo De Pascalis
- Department of Psychology, Sapienza Foundation, Sapienza University of Rome, Via dei Marsi, 78, 00185, Rome, Italy.
| | - Arianna Vecchio
- Department of Psychology, Sapienza Foundation, Sapienza University of Rome, Via dei Marsi, 78, 00185, Rome, Italy
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31
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Hartmann M, Falconer CJ, Kaelin-Lang A, Müri RM, Mast FW. Imagined paralysis reduces motor cortex excitability. Psychophysiology 2022; 59:e14069. [PMID: 35393640 PMCID: PMC9539708 DOI: 10.1111/psyp.14069] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/05/2020] [Revised: 12/16/2021] [Accepted: 03/26/2022] [Indexed: 11/27/2022]
Abstract
Mental imagery is a powerful capability that engages similar neurophysiological processes that underlie real sensory and motor experiences. Previous studies show that motor cortical excitability can increase during mental imagery of actions. In this study, we focused on possible inhibitory effects of mental imagery on motor functions. We assessed whether imagined arm paralysis modulates motor cortical excitability in healthy participants, as measured by motor evoked potentials (MEPs) of the hand induced by near-threshold transcranial magnetic stimulation (TMS) over the primary motor cortex hand area. We found lower MEP amplitudes during imagined arm paralysis when compared to imagined leg paralysis or baseline stimulation without paralysis imagery. These results show that purely imagined bodily constraints can selectively inhibit basic motor corticospinal functions. The results are discussed in the context of motoric embodiment/disembodiment.
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Affiliation(s)
- Matthias Hartmann
- Department of Psychology, University of Bern, Bern, Switzerland.,Faculty of Psychology, UniDistance Suisse, Brig, Switzerland
| | - Caroline J Falconer
- Department of Psychology, University of Bern, Bern, Switzerland.,Department of Clinical Educational and Health Psychology, University College London, London, UK
| | - Alain Kaelin-Lang
- Department of Neurology, University Hospital, University of Bern, Bern, Switzerland.,Department of BioMedical Research, University Hospital, University of Bern, Bern, Switzerland.,Neurocenter of Southern Switzerland, Regional Hospital of Lugano, Lugano, Switzerland.,Faculty of Biomedical Sciences, Università della Svizzera Italiana, Lugano, Switzerland
| | - René M Müri
- Department of Neurology, University Hospital, University of Bern, Bern, Switzerland.,Department of BioMedical Research, University Hospital, University of Bern, Bern, Switzerland
| | - Fred W Mast
- Department of Psychology, University of Bern, Bern, Switzerland
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32
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Ebisch SJH, Scalabrini A, Northoff G, Mucci C, Sergi MR, Saggino A, Aquino A, Alparone FR, Perrucci MG, Gallese V, Di Plinio S. Intrinsic Shapes of Empathy: Functional Brain Network Topology Encodes Intersubjective Experience and Awareness Traits. Brain Sci 2022; 12:brainsci12040477. [PMID: 35448008 PMCID: PMC9024660 DOI: 10.3390/brainsci12040477] [Citation(s) in RCA: 7] [Impact Index Per Article: 2.3] [Reference Citation Analysis] [Abstract] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 03/08/2022] [Revised: 03/31/2022] [Accepted: 04/02/2022] [Indexed: 02/04/2023] Open
Abstract
Trait empathy is an essential personality feature in the intricacy of typical social inclinations of individuals. Empathy is likely supported by multilevel neuronal network functioning, whereas local topological properties determine network integrity. In the present functional MRI study (N = 116), we aimed to trace empathic traits to the intrinsic brain network architecture. Empathy was conceived as composed of two dimensions within the concept of pre-reflective, intersubjective understanding. Vicarious experience consists of the tendency to resonate with the feelings of other individuals, whereas intuitive understanding refers to a natural awareness of others’ emotional states. Analyses of graph theoretical measures of centrality showed a relationship between the fronto-parietal network and psychometric measures of vicarious experience, whereas intuitive understanding was associated with sensorimotor and subcortical networks. Salience network regions could constitute hubs for information processing underlying both dimensions. The network properties related to empathy dimensions mainly concern inter-network information flow. Moreover, interaction effects implied several sex differences in the relationship between functional network organization and trait empathy. These results reveal that distinct intrinsic topological network features explain individual differences in separate dimensions of intersubjective understanding. The findings could help understand the impact of brain damage or stimulation through alterations of empathy-related network integrity.
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Affiliation(s)
- Sjoerd J. H. Ebisch
- Department of Neuroscience, Imaging and Clinical Sciences (DNISC), G. d’Annunzio University of Chieti-Pescara, 66100 Chieti, Italy; (A.A.); (F.R.A.); (M.G.P.); (S.D.P.)
- Institute of Advanced Biomedical Technologies (ITAB), G. d’Annunzio University of Chieti-Pescara, Via Luigi Polacchi 11, 66100 Chieti, Italy
- Correspondence:
| | - Andrea Scalabrini
- Department of Psychological, Health and Territorial Sciences (DiSPuTer), G. d’Annunzio University of Chieti-Pescara, 66100 Chieti, Italy;
| | - Georg Northoff
- The Royal’s Institute of Mental Health Research, University of Ottawa, Ottawa, ON K1N 6N5, Canada;
- Brain and Mind Research Institute, Centre for Neural Dynamics, Faculty of Medicine, University of Ottawa, Ottawa, ON K1N 6N5, Canada
- Mental Health Centre, Zhejiang University School of Medicine, Hangzhou 310030, China
- Centre for Cognition and Brain Disorders, Hangzhou Normal University, Hangzhou 310030, China
- TMU Research Centre for Brain and Consciousness, Shuang Hospital, Taipei Medical University, Taipei 110, Taiwan
- Graduate Institute of Humanities in Medicine, Taipei Medical University, Taipei 110, Taiwan
| | - Clara Mucci
- Department of Human and Social Sciences, University of Bergamo, 24129 Bergamo, Italy;
| | - Maria Rita Sergi
- Department of Medicine and Aging Sciences, G. d’Annunzio University of Chieti-Pescara, 66100 Chieti, Italy; (M.R.S.); (A.S.)
| | - Aristide Saggino
- Department of Medicine and Aging Sciences, G. d’Annunzio University of Chieti-Pescara, 66100 Chieti, Italy; (M.R.S.); (A.S.)
| | - Antonio Aquino
- Department of Neuroscience, Imaging and Clinical Sciences (DNISC), G. d’Annunzio University of Chieti-Pescara, 66100 Chieti, Italy; (A.A.); (F.R.A.); (M.G.P.); (S.D.P.)
| | - Francesca R. Alparone
- Department of Neuroscience, Imaging and Clinical Sciences (DNISC), G. d’Annunzio University of Chieti-Pescara, 66100 Chieti, Italy; (A.A.); (F.R.A.); (M.G.P.); (S.D.P.)
| | - Mauro Gianni Perrucci
- Department of Neuroscience, Imaging and Clinical Sciences (DNISC), G. d’Annunzio University of Chieti-Pescara, 66100 Chieti, Italy; (A.A.); (F.R.A.); (M.G.P.); (S.D.P.)
- Institute of Advanced Biomedical Technologies (ITAB), G. d’Annunzio University of Chieti-Pescara, Via Luigi Polacchi 11, 66100 Chieti, Italy
| | - Vittorio Gallese
- Unit of Neuroscience, Department of Medicine and Surgery, University of Parma, 43121 Parma, Italy;
| | - Simone Di Plinio
- Department of Neuroscience, Imaging and Clinical Sciences (DNISC), G. d’Annunzio University of Chieti-Pescara, 66100 Chieti, Italy; (A.A.); (F.R.A.); (M.G.P.); (S.D.P.)
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Bembich S, Saksida A, Mastromarino S, Travan L, Di Risio G, Cont G, Demarini S. Empathy at birth: Mother's cortex synchronizes with that of her newborn in pain. Eur J Neurosci 2022; 55:1519-1531. [PMID: 35266192 PMCID: PMC9314789 DOI: 10.1111/ejn.15641] [Citation(s) in RCA: 6] [Impact Index Per Article: 2.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/24/2021] [Revised: 01/07/2022] [Accepted: 03/02/2022] [Indexed: 11/26/2022]
Abstract
Early neonatal relation with the caregiver is vital for newborn survival and for the promotion of an appropriate neural development. The aim of this study was to assess if the empathic cortical response of a mother to her baby's pain is synchronized with the neonatal cortical response to the painful stimulation. We used hyperscanning, a functional neuroimaging approach that allows studying functional synchronization between two brains. Sixteen mother-newborn dyads were recruited. Maternal and neonatal cortical activities were simultaneously monitored, by near-infrared spectroscopy, during a heel prick performed on the baby and observed by the mother. Multiple paired t test was used to identify cortical activation, and wavelet transform coherence method was used to explore possible synchronization between the maternal and neonatal cortical areas. Activations were observed in mother's parietal cortex, bilaterally, and in newborn's superior motor/somatosensory cortex. The main functional synchronization analysis showed that mother's left parietal cortex activity cross-correlated with that of her newborn's superior motor/somatosensory cortex. Such synchronization dynamically changed throughout assessment, becoming positively cross-correlated only after the leading role in synchronizing cortical activities was taken up by the newborn. Thus, maternal empathic cortical response to baby pain was guided by and synchronized to the newborn's cortical response to pain. We conclude that, in case of potential danger for the infant, brain areas involved in mother-newborn relationship appear to be already co-regulated at birth.
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Affiliation(s)
- Stefano Bembich
- Division of Neonatology and Neonatal Intensive Care Unit, Institute for Maternal and Child HealthIRCCS “Burlo Garofolo”TriesteItaly
| | - Amanda Saksida
- Division of Neonatology and Neonatal Intensive Care Unit, Institute for Maternal and Child HealthIRCCS “Burlo Garofolo”TriesteItaly
| | - Simona Mastromarino
- Division of Neonatology and Neonatal Intensive Care Unit, Institute for Maternal and Child HealthIRCCS “Burlo Garofolo”TriesteItaly
| | - Laura Travan
- Division of Neonatology and Neonatal Intensive Care Unit, Institute for Maternal and Child HealthIRCCS “Burlo Garofolo”TriesteItaly
| | - Giovanna Di Risio
- Division of Neonatology and Neonatal Intensive Care Unit, Institute for Maternal and Child HealthIRCCS “Burlo Garofolo”TriesteItaly
| | - Gabriele Cont
- Division of Neonatology and Neonatal Intensive Care Unit, Institute for Maternal and Child HealthIRCCS “Burlo Garofolo”TriesteItaly
| | - Sergio Demarini
- Division of Neonatology and Neonatal Intensive Care Unit, Institute for Maternal and Child HealthIRCCS “Burlo Garofolo”TriesteItaly
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34
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Huang L, Xu G, He J, Tian H, Zhou Z, Huang F, Liu Y, Sun M, Liang F. Bibliometric Analysis of Functional Magnetic Resonance Imaging Studies on Acupuncture Analgesia Over the Past 20 Years. J Pain Res 2021; 14:3773-3789. [PMID: 34916843 PMCID: PMC8670890 DOI: 10.2147/jpr.s340961] [Citation(s) in RCA: 18] [Impact Index Per Article: 4.5] [Reference Citation Analysis] [Abstract] [Key Words] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/29/2021] [Accepted: 11/19/2021] [Indexed: 11/23/2022] Open
Abstract
BACKGROUND Researches on the central mechanisms of acupuncture analgesia have been widely conducted worldwide. However, there is no bibliometric analysis of functional magnetic resonance imaging (fMRI) studies on acupuncture analgesia. This study visualized the current status, hot spots and frontiers of fMRI studies on acupuncture analgesia in the past 20 years to provide a theoretical basis for its clinical application. METHODS All publications were obtained from Science Citation Index-Expanded (SCI-E) of Web of Science (WOS). We used CiteSpace to analyze publications, journals, cited journals, authors, cited authors, institutions, countries, references, and keywords. We also analyzed collaborative network maps and co-occurrence network maps. RESULTS We retrieved a total of 797 articles. Regarding the volume of publications, the total number of annual publications showed a fluctuating but overall increasing trend. Evidence-based Complementary and Alternative Medicine (21 articles) was the most productive journal, and Pain (225 articles) was the most cited journal. The most productive author was Qin W (16 articles), and the most co-cited author was Hui KKS (111). The most prolific institution and country were Massachusetts General Hospital (34 articles) and USA (212 articles). "Pain" was the top-ranked for keyword frequency and centrality. "Functional connectivity" was the frontier hotspot for 2018-2021. CONCLUSION First, fMRI researches on acupuncture analgesia involved several countries (regions) and institutions, mainly located in the USA, China and Korea, and most of them were universities. In addition, the USA was a major contributor in this field. Second, in terms of disciplinary distribution, the literatures were mainly from clinical neurology, neuroscience, and radiology nuclear medicine medical imaging. Third, the keyword co-occurrence analysis showed that the hot keywords included pain, fMRI, and lower back pain. Fourth, through keyword clustering analysis, the hot disease was found to be lower back pain, and the hot contents were acupuncture specificity and frequency specificity. Fifth, a timeline analysis of the references identified that chronic low back pain and specificity will remain a hot topic for future research.
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Affiliation(s)
- Liuyang Huang
- Acupuncture and Tuina School/The 3rd Teaching Hospital, Chengdu University of Traditional Chinese Medicine, Chengdu, Sichuan, People’s Republic of China
| | - Guixing Xu
- Acupuncture and Tuina School/The 3rd Teaching Hospital, Chengdu University of Traditional Chinese Medicine, Chengdu, Sichuan, People’s Republic of China
| | - Jiamei He
- Acupuncture and Tuina School/The 3rd Teaching Hospital, Chengdu University of Traditional Chinese Medicine, Chengdu, Sichuan, People’s Republic of China
| | - Hao Tian
- Acupuncture and Tuina School/The 3rd Teaching Hospital, Chengdu University of Traditional Chinese Medicine, Chengdu, Sichuan, People’s Republic of China
| | - Zhuo Zhou
- Acupuncture and Tuina School/The 3rd Teaching Hospital, Chengdu University of Traditional Chinese Medicine, Chengdu, Sichuan, People’s Republic of China
| | - Fengyuan Huang
- Acupuncture and Tuina School/The 3rd Teaching Hospital, Chengdu University of Traditional Chinese Medicine, Chengdu, Sichuan, People’s Republic of China
| | - Yilin Liu
- Acupuncture and Tuina School/The 3rd Teaching Hospital, Chengdu University of Traditional Chinese Medicine, Chengdu, Sichuan, People’s Republic of China
| | - Mingsheng Sun
- Acupuncture and Tuina School/The 3rd Teaching Hospital, Chengdu University of Traditional Chinese Medicine, Chengdu, Sichuan, People’s Republic of China
| | - Fanrong Liang
- Acupuncture and Tuina School/The 3rd Teaching Hospital, Chengdu University of Traditional Chinese Medicine/Clinical Research Center for Acupuncture and Moxibustion in Sichuan Province, Chengdu, Sichuan, People’s Republic of China
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35
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Zebarjadi N, Levy J. Neural shifts in alpha rhythm's dual functioning during empathy. Brain Behav 2021; 11:e2355. [PMID: 34536976 PMCID: PMC8613432 DOI: 10.1002/brb3.2355] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 04/27/2021] [Revised: 07/20/2021] [Accepted: 08/22/2021] [Indexed: 11/18/2022] Open
Abstract
INTRODUCTION Alpha oscillations are unique in their capacity to relay neuronal information through a dual-process named "gating by inhibition": rhythmic enhancement inhibits task-irrelevant regions while rhythmic suppression engages task-relevant regions in the brain. A social-cognitive process that operates by relying on the suppression of the alpha rhythm in the primary somatosensory cortex (S1) is the ability to generate empathy. This phenomenon has been evidenced in dozens of electrophysiological studies targeting adult human subjects. Yet, recent studies on the neurodevelopment of empathy indicate that in younger age, empathy does not involve alpha suppression in S1 but only enhancement. More interestingly, right before adulthood, this rhythm is still enhanced, but in a remarkable shift, a pattern of suppression emerges. In this registered magnetoencephalography (MEG) and functional magnetic resonance imaging (fMRI) study, we will capture frequency-decomposed neural activity particularly at the alpha range and its corresponding hemodynamic response and target subjects at around 20 years old as a unique time-window in development that allows investigating in parallel both low-alpha suppression and high-alpha enhancement. We aim to address two questions: (a) Does alpha power suppression in the S1 region during empathy correspond to BOLD increase in this region? (b) What is the functional role of alpha power enhancement during empathy development (BOLD signal increase or decrease)? Addressing these questions will particularly advance knowledge on the process of empathy in the brain, and the way in which it is underpinned by alpha oscillations. Moreover, examining these experimental outcomes can potentially lay the ground for future studies that would further examine the role of alpha oscillations in empathy during the course of development. METHODS Brain data of forty healthy individuals close to 20 years old will be recorded in two consecutive MEG and fMRI sessions while subjects observing physical pain versus neutral stimuli. Besides, each participant's subjective experiences wll be measred by questionnaires, interviews and rating of the stimuli.
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Affiliation(s)
- Niloufar Zebarjadi
- Department of Neuroscience and Biomedical Engineering, Aalto University, Espoo, Finland
| | - Jonathan Levy
- Department of Neuroscience and Biomedical Engineering, Aalto University, Espoo, Finland.,Baruch Ivcher School of Psychology, Interdisciplinary Center Herzliya, Herzliya, Israel
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36
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Harjunen VJ, Sjö P, Ahmed I, Saarinen A, Farmer H, Salminen M, Järvelä S, Ruonala A, Jacucci G, Ravaja N. Increasing Self-Other Similarity Modulates Ethnic Bias in Sensorimotor Resonance to Others' Pain. Soc Cogn Affect Neurosci 2021; 17:673-682. [PMID: 34669949 PMCID: PMC9250302 DOI: 10.1093/scan/nsab113] [Citation(s) in RCA: 7] [Impact Index Per Article: 1.8] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 03/25/2021] [Revised: 10/01/2021] [Accepted: 10/20/2021] [Indexed: 11/15/2022] Open
Abstract
The tendency to simulate the pain of others within our own sensorimotor systems is a vital component of empathy. However, this sensorimotor resonance is modulated by a multitude of social factors including similarity in bodily appearance, e.g. skin colour. The current study investigated whether increasing self-other similarity via virtual transfer to another colour body reduced ingroup bias in sensorimotor resonance. A sample of 58 white participants was momentarily transferred to either a black or a white body using virtual reality technology. We then employed electroencephalography (EEG) to examine event-related desynchronization (ERD) in the sensorimotor beta (13-23 Hz) oscillations while they viewed black, white, and violet photorealistic virtual agents being touched with a noxious or soft object. While the noxious treatment of a violet agent did not increase beta ERD, amplified beta ERD in response to black agent's noxious vs. soft treatment was found in perceivers transferred to black body. Transfer to the white body dismissed the effect. Further exploratory analysis implied that the pain-related beta ERD occurred only when the agent and the participant were of the same colour. The results suggest that even short-lasting changes in bodily resemblance can modulate sensorimotor resonance to others' perceived pain.
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Affiliation(s)
- Ville Johannes Harjunen
- Department of Psychology and Logopedics, Faculty of Medicine, University of Helsinki, Helsinki, Finland
| | - Petja Sjö
- Finnish Institute for Health and Welfare, Helsinki, Finland
| | - Imtiaj Ahmed
- Department of Computer Science, University of Helsinki, Helsinki, Finland
| | - Aino Saarinen
- Department of Psychology and Logopedics, Faculty of Medicine, University of Helsinki, Helsinki, Finland
| | - Harry Farmer
- School of Human Sciences, University of Greenwich, London, United Kingdom.,Institute of Cognitive Neuroscience, University College London, London, United Kingdom
| | - Mikko Salminen
- Gamification Group, Faculty of Information Technology and Communications, Tampere University, Tampere, Finland
| | - Simo Järvelä
- Department of Psychology and Logopedics, Faculty of Medicine, University of Helsinki, Helsinki, Finland.,Gamification Group, Faculty of Information Technology and Communications, Tampere University, Tampere, Finland
| | - Antti Ruonala
- Department of Computer Science, University of Helsinki, Helsinki, Finland
| | - Giulio Jacucci
- Department of Computer Science, University of Helsinki, Helsinki, Finland
| | - Niklas Ravaja
- Department of Psychology and Logopedics, Faculty of Medicine, University of Helsinki, Helsinki, Finland
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37
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Sowden S, Khemka D, Catmur C. Regulating mirroring of emotions A social-specific mechanism? Q J Exp Psychol (Hove) 2021; 75:1302-1313. [PMID: 34541953 PMCID: PMC9131398 DOI: 10.1177/17470218211049780] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/29/2022]
Abstract
There is evidence that humans mirror others’ emotional responses: brain responses to observed and experienced emotion overlap, and reaction time costs of observing others’ pain suggest that others’ emotional states interfere with our own. Such emotional mirroring requires regulation to prevent personal distress. However, currently it is unclear whether this “empathic interference effect” is uniquely social, arising only from the observation of human actors, or also from the observation of non-biological objects in “painful” states. Moreover, the degree to which this interference relates to individual differences in self-reported levels of empathy is yet to be revealed. We introduce a modified pain observation task, measuring empathic interference effects induced by observation of painful states applied to both biological and non-biological stimuli. An initial validation study (N = 50) confirmed that painful states applied to biological stimuli were rated explicitly as more painful than non-painful states applied to biological stimuli, and also than both painful and non-painful states applied to non-biological stimuli. Subsequently, across two independent discovery (N = 83) and replication (N = 80) samples, the task elicited slowing of response times during the observation of painful states when compared to non-painful states, but the magnitude of this effect did not differ between biological and non-biological stimuli. Little evidence was found for reliable relationships between empathic interference and self-reported empathy. Caution should therefore be taken in using the current task to pursue an individual differences approach to empathic interference, but the task shows promise for investigating the specificity of the mechanism involved in regulating emotional mirroring.
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Affiliation(s)
- Sophie Sowden
- School of Psychology, University of Birmingham, Birmingham, UK.,Department of Psychology, Institute of Psychiatry, Psychology & Neuroscience, King's College London, London, UK
| | - Divyush Khemka
- Department of Psychology, Institute of Psychiatry, Psychology & Neuroscience, King's College London, London, UK
| | - Caroline Catmur
- Department of Psychology, Institute of Psychiatry, Psychology & Neuroscience, King's College London, London, UK
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38
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Vecchio A, De Pascalis V. ERP Indicators of Self-Pain and Other Pain Reductions due to Placebo Analgesia Responding: The Moderating Role of the Fight-Flight-Freeze System. Brain Sci 2021; 11:brainsci11091192. [PMID: 34573212 PMCID: PMC8467887 DOI: 10.3390/brainsci11091192] [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: 08/13/2021] [Revised: 09/06/2021] [Accepted: 09/08/2021] [Indexed: 12/30/2022] Open
Abstract
This study evaluates the modulation of phasic pain and empathy for pain induced by placebo analgesia during pain and empathy for pain tasks. Because pain can be conceptualized as a dangerous stimulus that generates avoidance, we evaluated how approach and avoidance personality traits modulate pain and empathy for pain responses. We induced placebo analgesia to test whether this also reduces self-pain and other pain. Amplitude measures of the N1, P2, and P3 ERPs components, elicited by electric stimulations, were obtained during a painful control, as well as during a placebo treatment expected to induce placebo analgesia. The placebo treatment produced a reduction in pain and unpleasantness perceived, whereas we observed a decrease in the empathy unpleasantness alone during the empathy pain condition. The moderator effects of the fight-flight-freeze system (FFFS) in the relationships linking P2 and P3 amplitude changes with pain reduction were both significant among low to moderate FFFS values. These observations are consistent with the idea that lower FFFS (active avoidance) scores can predict placebo-induced pain reduction. Finally, in line with the revised Reinforcement Sensitivity Theory (r-RST), we can assume that phasic pain is an aversive stimulus activating the active-avoidance behavior to bring the system back to homeostasis.
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39
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Wu T, Han S. Neural mechanisms of modulations of empathy and altruism by beliefs of others' pain. eLife 2021; 10:e66043. [PMID: 34369378 PMCID: PMC8373377 DOI: 10.7554/elife.66043] [Citation(s) in RCA: 3] [Impact Index Per Article: 0.8] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 12/23/2020] [Accepted: 08/08/2021] [Indexed: 12/17/2022] Open
Abstract
Perceived cues signaling others' pain induce empathy which in turn motivates altruistic behavior toward those who appear suffering. This perception-emotion-behavior reactivity is the core of human altruism but does not always occur in real-life situations. Here, by integrating behavioral and multimodal neuroimaging measures, we investigate neural mechanisms underlying modulations of empathy and altruistic behavior by beliefs of others' pain (BOP). We show evidence that lack of BOP reduces subjective estimation of others' painful feelings and decreases monetary donations to those who show pain expressions. Moreover, lack of BOP attenuates neural responses to their pain expressions within 200 ms after face onset and modulates neural responses to others' pain in the insular, post-central, and frontal cortices. Our findings suggest that BOP provide a cognitive basis of human empathy and altruism and unravel the intermediate neural mechanisms.
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Affiliation(s)
- Taoyu Wu
- School of Psychological and Cognitive Sciences, PKU-IDG/MGovern Institute for Brain Research, Beijing Key Laboratory of Behavior and Mental Health, Peking UniversityBeijingChina
| | - Shihui Han
- School of Psychological and Cognitive Sciences, PKU-IDG/MGovern Institute for Brain Research, Beijing Key Laboratory of Behavior and Mental Health, Peking UniversityBeijingChina
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40
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Pamplona GSP, Salgado JAD, Staempfli P, Seifritz E, Gassert R, Ionta S. Illusory Body Ownership Affects the Cortical Response to Vicarious Somatosensation. Cereb Cortex 2021; 32:312-328. [PMID: 34240141 PMCID: PMC8754387 DOI: 10.1093/cercor/bhab210] [Citation(s) in RCA: 11] [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: 04/14/2021] [Revised: 06/08/2021] [Accepted: 06/09/2021] [Indexed: 12/30/2022] Open
Abstract
Fundamental human feelings such as body ownership (“this” body is “my” body) and vicariousness (first-person-like experience of events occurring to others) are based on multisensory integration. Behavioral links between body ownership and vicariousness have been shown, but the neural underpinnings remain largely unexplored. To fill this gap, we investigated the neural effects of altered body ownership on vicarious somatosensation. While recording functional brain imaging data, first, we altered participants’ body ownership by robotically delivering tactile stimulations (“tactile” stroking) in synchrony or not with videos of a virtual hand being brushed (“visual” stroking). Then, we manipulated vicarious somatosensation by showing videos of the virtual hand being touched by a syringe’s plunger (touch) or needle (pain). Only after the alteration of body ownership (synchronous visuo-tactile stroking) and specifically during late epochs of vicarious somatosensation, vicarious pain was associated with lower activation in premotor and anterior cingulate cortices with respect to vicarious touch. At the methodological level, the present study highlights the importance of the neural response’s temporal evolution. At the theoretical level, it shows that the higher-level (cognitive) impact of a lower-level (sensory) body-related processing (visuo-tactile) is not limited to body ownership but also extends to other psychological body-related domains, such as vicarious somatosensation.
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Affiliation(s)
- Gustavo S P Pamplona
- Sensory-Motor Lab (SeMoLa), Department of Ophthalmology-University of Lausanne, Jules Gonin Eye Hospital-Fondation Asile des Aveugles, Lausanne, Switzerland
- Rehabilitation Engineering Laboratory (RELab), Department of Health Sciences and Technology, ETH Zurich, Zurich, Switzerland
| | - Julio A D Salgado
- Rehabilitation Engineering Laboratory (RELab), Department of Health Sciences and Technology, ETH Zurich, Zurich, Switzerland
| | - Philipp Staempfli
- Department of Psychiatry, Psychotherapy, and Psychosomatics, Psychiatric Hospital of the University of Zurich, Zurich, Switzerland
| | - Erich Seifritz
- Department of Psychiatry, Psychotherapy, and Psychosomatics, Psychiatric Hospital of the University of Zurich, Zurich, Switzerland
| | - Roger Gassert
- Rehabilitation Engineering Laboratory (RELab), Department of Health Sciences and Technology, ETH Zurich, Zurich, Switzerland
| | - Silvio Ionta
- Address correspondence to Silvio Ionta, Fondation Asile des Aveugles, Av. de France 15, 1002 Lausanne, Switzerland.
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41
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Zebarjadi N, Adler E, Kluge A, Jääskeläinen IP, Sams M, Levy J. Rhythmic Neural Patterns During Empathy to Vicarious Pain: Beyond the Affective-Cognitive Empathy Dichotomy. Front Hum Neurosci 2021; 15:708107. [PMID: 34305559 PMCID: PMC8292834 DOI: 10.3389/fnhum.2021.708107] [Citation(s) in RCA: 5] [Impact Index Per Article: 1.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/11/2021] [Accepted: 06/14/2021] [Indexed: 12/30/2022] Open
Abstract
Empathy is often split into an affective facet for embodied simulation or sometimes sensorial processing, and a cognitive facet for mentalizing and perspective-taking. However, a recent neurophenomenological framework proposes a graded view on empathy (i.e., "Graded Empathy") that extends this dichotomy and considers multiple levels while integrating complex neural patterns and representations of subjective experience. In the current magnetoencephalography study, we conducted a multidimensional investigation of neural oscillatory modulations and their cortical sources in 44 subjects while observing stimuli that convey vicarious pain (vs no-pain) in a broad time window and frequency range to explore rich neural representations of pain empathy. Furthermore, we collected participants' subjective-experience of sensitivity to vicarious pain, as well as their self-reported trait levels of affective and cognitive empathy to examine the possible associations between neural mechanisms and subjective experiences and reports. While extending previous electrophysiological studies that mainly focused on alpha suppression, we found here four significant power modulation patterns corresponding to multiple facets of empathy: an early central (peaking in the paracentral sulcus) alpha (6-11 Hz) suppression pattern plausibly reflecting sensory processing, two early beta (15-23 Hz) suppression patterns in the mid-cingulate cortex (plausibly reflecting the affective component) and in the precuneus (plausibly reflecting the cognitive component), and a late anterior (peaking in the orbitofrontal cortex) alpha-beta (11-19 Hz) enhancement pattern (plausibly reflecting cognitive-control inhibitory response). Interestingly, the latter measure was negatively correlated with the subjective sensitivity to vicarious pain, thereby possibly revealing a novel inhibitory neural mechanism determining the subjective sensitivity to vicarious pain. Altogether, these multilevel findings cannot be accommodated by the dichotomous model of empathy (i.e., affective-cognitive), and provide empirical support to the Graded Empathy neurophenomenological framework. Furthermore, this work emphasizes the importance of examining multiple neural rhythms, their cortical generators, and reports of subjective-experience in the aim of elucidating the complex nature of empathy.
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Affiliation(s)
- Niloufar Zebarjadi
- Department of Neuroscience and Biomedical Engineering, Aalto University, Espoo, Finland
| | - Eliyahu Adler
- Department of Neuroscience and Biomedical Engineering, Aalto University, Espoo, Finland.,Department of Psychology, The Hebrew University of Jerusalem, Jerusalem, Israel
| | - Annika Kluge
- Department of Neuroscience and Biomedical Engineering, Aalto University, Espoo, Finland
| | - Iiro P Jääskeläinen
- Department of Neuroscience and Biomedical Engineering, Aalto University, Espoo, Finland.,International Laboratory of Social Neurobiology, Institute for Cognitive Neuroscience, Higher School of Economics, Moscow, Russia
| | - Mikko Sams
- Department of Neuroscience and Biomedical Engineering, Aalto University, Espoo, Finland.,MAGICS-Aalto, Aalto University, Espoo, Finland
| | - Jonathan Levy
- Department of Neuroscience and Biomedical Engineering, Aalto University, Espoo, Finland.,Baruch Ivcher School of Psychology, Interdisciplinary Center Herzliya, Herzliya, Israel
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42
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Increasing self-other bodily overlap increases sensorimotor resonance to others' pain. COGNITIVE AFFECTIVE & BEHAVIORAL NEUROSCIENCE 2021; 20:19-33. [PMID: 31190136 PMCID: PMC7012796 DOI: 10.3758/s13415-019-00724-0] [Citation(s) in RCA: 20] [Impact Index Per Article: 5.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Subscribe] [Scholar Register] [Indexed: 12/24/2022]
Abstract
Empathy for another person’s pain and feeling pain oneself seem to be accompanied by similar or shared neural responses. Such shared responses could be achieved by mapping the bodily states of others onto our own bodily representations. We investigated whether sensorimotor neural responses to the pain of others are increased when experimentally reducing perceived bodily distinction between the self and the other. Healthy adult participants watched video clips of the hands of ethnic ingroup or outgroup members being painfully penetrated by a needle syringe or touched by a cotton swab. Manipulating the video presentation to create a visuospatial overlap between the observer’s and the target’s hand increased the perceived bodily self-attribution of the target’s hand. For both ingroup and outgroup targets, this resulted in increased neural responses to the painful injections (compared with nonpainful contacts), as indexed by desynchronizations of central mu and beta scalp rhythms recorded using electroencephalography. Furthermore, these empathy-related neural activations were stronger in participants who reported stronger bodily self-attribution of the other person’s hand. Our findings provide further evidence that empathy for pain engages sensorimotor resonance mechanisms. They also indicate that reducing bodily self-other distinction may increase such resonance for ingroup as well as outgroup targets.
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43
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Peng W, Lou W, Huang X, Ye Q, Tong RKY, Cui F. Suffer together, bond together: Brain-to-brain synchronization and mutual affective empathy when sharing painful experiences. Neuroimage 2021; 238:118249. [PMID: 34116146 DOI: 10.1016/j.neuroimage.2021.118249] [Citation(s) in RCA: 17] [Impact Index Per Article: 4.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 04/05/2021] [Revised: 05/24/2021] [Accepted: 06/07/2021] [Indexed: 12/30/2022] Open
Abstract
Previous behavioral studies have shown that sharing painful experiences can strengthen social bonds and promote mutual prosociality, yet the neural mechanisms underlying this phenomenon remain unclear. We hypothesized that sharing a painful experience induces brain-to-brain synchronization and mutual empathy for each other's pain between pain-takers and pain-observers, which then leads to enhanced social bonding. To test this hypothesis, we adopted an electroencephalographic (EEG) hyper-scanning technique to assess neuronal and behavioral activity during a Pain-Sharing task in which high- or low-intensity pain stimulation was randomly delivered to one participant of a dyad on different experimental trials. Single-brain analysis showed that sensorimotor α-oscillation power was suppressed more when expecting high-intensity pain than when expecting low-intensity pain similarly for self-directed or partner-directed pain. Dual-brain analysis revealed that expecting high-intensity pain induced greater brain-to-brain synchronization of sensorimotor α-oscillation phases between pain-takers and pain-observers than did expecting low-intensity pain. Mediation analysis further revealed that brain-to-brain synchronization of sensorimotor α-oscillations mediated the effects of pain-stimulation intensity on mutual affective sharing for partner-directed pain. This mutual affective empathy during the task predicted the social bonding, as indexed by prosocial inclinations measured after the task. These results support the hypothesis that sharing a painful experience triggers emotional resonance between pairs of individuals through brain-to-brain synchronization of neuronal α-oscillations recorded over the sensorimotor cortex, and this emotional resonance further strengthens social bonds and motivates prosocial behavior within pairs of individuals.
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Affiliation(s)
- Weiwei Peng
- School of Psychology, Shenzhen University, Shenzhen, China; Shenzhen Key Laboratory of Affective and Social Cognitive Science, Shenzhen University, Shenzhen, China
| | - Wutao Lou
- Department of Biomedical Engineering, The Chinese University of Hong Kong, Hong Kong, China
| | - Xiaoxuan Huang
- School of Psychology, Shenzhen University, Shenzhen, China
| | - Qian Ye
- School of Psychology, Shenzhen University, Shenzhen, China
| | - Raymond Kai-Yu Tong
- Department of Biomedical Engineering, The Chinese University of Hong Kong, Hong Kong, China
| | - Fang Cui
- School of Psychology, Shenzhen University, Shenzhen, China; Shenzhen Key Laboratory of Affective and Social Cognitive Science, Shenzhen University, Shenzhen, China.
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44
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Hartmann H, Riva F, Rütgen M, Lamm C. Placebo Analgesia Does Not Reduce Empathy for Naturalistic Depictions of Others' Pain in a Somatosensory Specific Way. Cereb Cortex Commun 2021; 2:tgab039. [PMID: 34296184 PMCID: PMC8276832 DOI: 10.1093/texcom/tgab039] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.3] [Reference Citation Analysis] [Abstract] [Key Words] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/18/2021] [Revised: 05/18/2021] [Accepted: 05/26/2021] [Indexed: 01/10/2023] Open
Abstract
The shared representations account postulates that sharing another's pain recruits underlying brain functions also engaged during first-hand pain. Critically, direct causal evidence for this was mainly shown for affective pain processing, while the contribution of somatosensory processes to empathy remains controversial. This controversy may be explained, however, by experimental paradigms that did not direct attention towards a specific body part, or that did not employ naturalistic depictions of others' pain. In this preregistered functional magnetic resonance imaging study, we aimed to test whether causal manipulation of first-hand pain affects empathy for naturalistic depictions of pain in a somatosensory-matched manner. Forty-five participants underwent a placebo analgesia induction in their right hand and observed pictures of other people's right and left hands in pain. We found neither behavioral nor neural evidence for somatosensory-specific modulation of pain empathy. However, exploratory analyses revealed a general effect of the placebo on empathy, and higher brain activity in bilateral anterior insula when viewing others' right hands in pain (i.e., corresponding to one's own placebo hand). These results refine our knowledge regarding the neural mechanisms of pain empathy, and imply that the sharing of somatosensory representations seems to play less of a causal role than the one of affective representations.
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Affiliation(s)
- Helena Hartmann
- Social, Cognitive and Affective Neuroscience Unit, Department of Cognition, Emotion, and Methods in Psychology, Faculty of Psychology, University of Vienna, 1010 Vienna, Austria
| | - Federica Riva
- Social, Cognitive and Affective Neuroscience Unit, Department of Cognition, Emotion, and Methods in Psychology, Faculty of Psychology, University of Vienna, 1010 Vienna, Austria
| | - Markus Rütgen
- Social, Cognitive and Affective Neuroscience Unit, Department of Cognition, Emotion, and Methods in Psychology, Faculty of Psychology, University of Vienna, 1010 Vienna, Austria
| | - Claus Lamm
- Social, Cognitive and Affective Neuroscience Unit, Department of Cognition, Emotion, and Methods in Psychology, Faculty of Psychology, University of Vienna, 1010 Vienna, Austria
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45
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Lincoln SH, Germine LT, Mair P, Hooker CI. Simulation and social behavior: an fMRI study of neural processing during simulation in individuals with and without risk for psychosis. Soc Cogn Affect Neurosci 2021; 15:165-174. [PMID: 32248225 PMCID: PMC7304514 DOI: 10.1093/scan/nsaa047] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/25/2019] [Revised: 11/17/2019] [Accepted: 02/28/2020] [Indexed: 12/26/2022] Open
Abstract
Social dysfunction is a risk indicator for schizophrenia spectrum disorders, with at-risk individuals demonstrating a range of social behavior impairments. Variability in social ability may be explained by individual differences in the psychological processes of social behavior. In particular, mental simulation, the process by which an individual generates an internal representation of the thoughts or feelings of another, may explain variation in social behavior. This study investigates the neural process of simulation in healthy individuals and individuals at risk for psychosis. Using a novel fMRI pain paradigm, individuals watch videos of another person’s hand or foot experiencing pain. After each video, individuals are asked to simulate the observed painful situation on their own hand or foot. Neural activity during simulation in the somatosensory cortex was associated with real-world self-reported social behavior, such that a stronger neural response in the somatosensory cortex was associated with greater rates of positive social experiences and affective empathy across all participants. These findings suggest that the neural mechanisms that underlie simulation are important for social behavior, and may explain individual variability in social functioning in healthy and at-risk populations.
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Affiliation(s)
| | - Laura T Germine
- Department of Psychiatry, Harvard Medical School, Boston, MA 02115, USA.,McLean Hospital, Belmont, MA 02478, USA
| | - Patrick Mair
- Department of Psychology, Harvard University, Cambridge, MA 02138, USA
| | - Christine I Hooker
- Department of Psychiatry and Behavioral Sciences, Rush University Medical Center, Chicago, IL 60612, USA
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46
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Malinowska JK. Can I Feel Your Pain? The Biological and Socio-Cognitive Factors Shaping People’s Empathy with Social Robots. Int J Soc Robot 2021. [DOI: 10.1007/s12369-021-00787-5] [Citation(s) in RCA: 4] [Impact Index Per Article: 1.0] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 01/10/2023]
Abstract
AbstractThis paper discuss the phenomenon of empathy in social robotics and is divided into three main parts. Initially, I analyse whether it is correct to use this concept to study and describe people’s reactions to robots. I present arguments in favour of the position that people actually do empathise with robots. I also consider what circumstances shape human empathy with these entities. I propose that two basic classes of such factors be distinguished: biological and socio-cognitive. In my opinion, one of the most important among them is a sense of group membership with robots, as it modulates the empathic responses to representatives of our- and other- groups. The sense of group membership with robots may be co-shaped by socio-cognitive factors such as one’s experience, familiarity with the robot and its history, motivation, accepted ontology, stereotypes or language. Finally, I argue in favour of the formulation of a pragmatic and normative framework for manipulations in the level of empathy in human–robot interactions.
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47
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Wang P, Zhu M, Mo S, Li X, Wang J. The effect of somatosensory alpha transcranial alternating current stimulation on pain empathy is trait empathy and gender dependent. CNS Neurosci Ther 2021; 27:687-693. [PMID: 33739605 PMCID: PMC8111491 DOI: 10.1111/cns.13631] [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: 08/17/2020] [Revised: 02/02/2021] [Accepted: 02/03/2021] [Indexed: 12/30/2022] Open
Abstract
Background Pain empathy enables a person to experience and understand other's pain state by observing others in pain condition. Such prosocial ability is deficient in many psychopathological disorders. Somatosensory alpha suppression is considered as neural correlates of pain empathy and is hypothesized as a target for enhancement of pain empathy. Researches demonstrated that alpha suppression could be enhanced by transcranial alternating current stimulation (tACS) at alpha frequency non‐invasively. Aims We applied alpha tACS over the primary somatosensory cortex of healthy subjects to investigate whether alpha tACS is able to enhance the pain empathy performance. Results The results showed that there was no difference of pain empathy performance between alpha tACS and sham tACS either when tACS was applied during the task or before task. While in the alpha tACS group, the pain empathy performance was positively correlated with empathic concern of male subjects, the sub‐component of personal trait empathy. Conclusions Alpha tACS cannot alter the empathy performance overall, but the modulation effect of alpha tACS on pain empathy is dependent on the gender and trait empathy of subjects.
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Affiliation(s)
- Peipei Wang
- Department of Neurobiology, School of Basic Medical Sciences, Capital Medical University, Beijing, China
| | - Minjia Zhu
- Department of Orthodontics, School of Stomatology, Capital Medical University, Beijing, China
| | - Shaohua Mo
- Department of Neurosurgery, Beijing Tiantan Hospital, Capital Medical University, Beijing, China
| | - Xiaoli Li
- State Key Laboratory of Cognitive Neuroscience and Learning, Beijing Normal University, Beijing, China
| | - Jing Wang
- Department of Neurobiology, School of Basic Medical Sciences, Capital Medical University, Beijing, China
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48
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Tinnermann A, Büchel C, Haaker J. Observation of others' painful heat stimulation involves responses in the spinal cord. SCIENCE ADVANCES 2021; 7:7/14/eabe8444. [PMID: 33789899 PMCID: PMC8011973 DOI: 10.1126/sciadv.abe8444] [Citation(s) in RCA: 7] [Impact Index Per Article: 1.8] [Reference Citation Analysis] [Abstract] [Grants] [Track Full Text] [Subscribe] [Scholar Register] [Received: 09/22/2020] [Accepted: 02/11/2021] [Indexed: 05/03/2023]
Abstract
Observing others' aversive experiences is central to know what is dangerous for ourselves. Hence, observation often elicits behavioral and physiological responses comparable to first-hand aversive experiences and engages overlapping brain activation. While brain activation to first-hand aversive experiences relies on connections to the spinal cord, it is unresolved whether merely observing aversive stimulation also involves responses in the spinal cord. Here, we show that observation of others receiving painful heat stimulation involves neural responses in the spinal cord, located in the same cervical segment as first-hand heat pain. However, while first-hand painful experiences are coded within dorsolateral regions of the spinal cord, observation of others' painful heat stimulation involves medial regions. Dorsolateral areas that process first-hand pain exhibit negative responses when observing pain in others. Our results suggest a distinct processing between self and others' pain in the spinal cord when integrating social information.
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Affiliation(s)
- Alexandra Tinnermann
- Department of Systems Neuroscience, University Medical Center Hamburg-Eppendorf, Martinistr. 52, 20246 Hamburg, Germany
- Max Planck School of Cognition, Leipzig, Germany
| | - Christian Büchel
- Department of Systems Neuroscience, University Medical Center Hamburg-Eppendorf, Martinistr. 52, 20246 Hamburg, Germany
- Max Planck School of Cognition, Leipzig, Germany
| | - Jan Haaker
- Department of Systems Neuroscience, University Medical Center Hamburg-Eppendorf, Martinistr. 52, 20246 Hamburg, Germany.
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49
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Sandri A, Cecchini MP, Riello M, Zanini A, Nocini R, Fiorio M, Tinazzi M. Pain, Smell, and Taste in Adults: A Narrative Review of Multisensory Perception and Interaction. Pain Ther 2021; 10:245-268. [PMID: 33635507 PMCID: PMC8119564 DOI: 10.1007/s40122-021-00247-y] [Citation(s) in RCA: 5] [Impact Index Per Article: 1.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/15/2021] [Accepted: 02/13/2021] [Indexed: 12/31/2022] Open
Abstract
Every day our sensory systems perceive and integrate a variety of stimuli containing information vital for our survival. Pain acts as a protective warning system, eliciting a response to remove harmful stimuli; it may also be a symptom of an illness or present as a disease itself. There is a growing need for additional pain-relieving therapies involving the multisensory integration of smell and taste in pain modulation, an approach that may provide new strategies for the treatment and management of pain. While pain, smell, and taste share common features and are strongly linked to emotion and cognition, their interaction has been poorly explored. In this review, we provide an overview of the literature on pain modulation by olfactory and gustatory substances. It includes adult human studies investigating measures of pain threshold, tolerance, intensity, and/or unpleasantness. Due to the limited number of studies currently available, we have structured this review as a narrative in which we comment on experimentally induced and clinical pain separately on pain–smell and pain–taste interaction. Inconsistent study findings notwithstanding, pain, smell, and taste seem to interact at both the behavioral and the neural levels. Pain intensity and unpleasantness seem to be affected more by olfactory substances, whereas pain threshold and tolerance are influenced by gustatory substances. Few pilot studies to date have investigated these effects in clinical populations. While the current results are promising for the future, more evidence is needed to elucidate the link between the chemical senses and pain. Doing so has the potential to improve and develop novel options for pain treatment.
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Affiliation(s)
- Angela Sandri
- Department of Neurosciences, Biomedicine and Movement Sciences, University of Verona, Verona, Italy.
| | - Maria Paola Cecchini
- Anatomy and Histology Section, Department of Neuroscience, Biomedicine and Movement Sciences, University of Verona, Verona, Italy
| | - Marianna Riello
- Neurology Unit, Department of Neuroscience, Biomedicine and Movement Sciences, University of Verona, Verona, Italy
| | - Alice Zanini
- Anatomy and Histology Section, Department of Neuroscience, Biomedicine and Movement Sciences, University of Verona, Verona, Italy
| | - Riccardo Nocini
- Otolaryngology Section, Department of Surgery, Dentistry, Paediatrics and Gynaecology , University of Verona, Verona, Italy
| | - Mirta Fiorio
- Department of Neurosciences, Biomedicine and Movement Sciences, University of Verona, Verona, Italy
| | - Michele Tinazzi
- Neurology Unit, Department of Neuroscience, Biomedicine and Movement Sciences, University of Verona, Verona, Italy.
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Investigating the effects of pain observation on approach and withdrawal actions. Exp Brain Res 2021; 239:847-856. [PMID: 33399898 DOI: 10.1007/s00221-020-05990-w] [Citation(s) in RCA: 2] [Impact Index Per Article: 0.5] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/06/2020] [Accepted: 11/18/2020] [Indexed: 12/18/2022]
Abstract
Previous research has shown that observing another individual receiving a painful stimulus leads to motor facilitation as indexed by faster reaction times. The current study explores whether the type of action that is executed modulates this facilitation effect. Specifically, we examined whether approach-like and withdraw-like movements are differentially influenced by pain observation. In experiment 1, participants performed key presses (approach) and releases (withdraw) after observing another person in pain (vs. no pain). In experiment 2, participants used a joystick to make forward (approach) and backward (withdraw) movements after observing another person in pain (vs. no pain). Across both experiments, we did not find evidence for differential effects of pain observation on approach-like and withdraw-like movements. We do, however, report a robust response-general effect of pain observation on motor behaviour (i.e., faster reaction times after pain observation vs. no pain, regardless of movement type). We discuss these results in relation to the wider emotion, attention, and social neuroscience of empathy literatures.
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