Mammalian empathy: behavioural manifestations and neural basis
Abstract
Recent research on empathy in humans and other mammals seeks to dissociate emotional and cognitive empathy. These forms, however, remain interconnected in evolution, across species and at the level of neural mechanisms. New data have facilitated the development of empathy models such as the perception-action model (PAM) and mirror-neuron theories. According to the PAM, the emotional states of others are understood through personal, embodied representations that allow empathy and accuracy to increase based on the observer's past experiences. In this Review, we discuss the latest evidence from studies carried out across a wide range of species, including studies on yawn contagion, consolation, aid-giving and contagious physiological affect, and we summarize neuroscientific data on representations related to another's state.
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Translational rodent models that capture aspects of social affect include emotion contagion and social buffering.
“Translational rodent models that capture aspects of social affect include emotion contagion and social buffering24.”
From Insular cortex mediates approach and avoidance responses to social affective stimuli (2018) · cites this paper as [24]
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BackgroundMethodSocial Media and Well-Being: Pitfalls, Progress, and Next Steps
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Insular cortex mediates approach and avoidance responses to social affective stimuli
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“Similar responses in humans 99 and other primates 100,101 suggest that a demonstrator’s emotional expression of, for example, pain might itself serve as a vicarious reinforcer, a US, imbuing neutral stimuli with value and motivating actions.”
BackgroundIntegrating Empathy and Interpersonal Emotion Regulation
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“Clinicians who do use it are prone to cautious delivery of exposure—for instance, refraining from using highly anxiety-provoking stimuli, terminating exposure tasks early, or interweaving anxiety-reduction exercises into those tasks (Deacon et al. 2013).”
BackgroundToward a consensus on the nature of empathy: A review of reviews
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The Role of Empathy and Compassion in Conflict Resolution
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“Furthermore, empathy promotes helping behavior toward members of one’s own group (de Waal & Preston, 2017; Preston & de Waal, 2002).”
BackgroundNeurocognitive Basis of Racial Ingroup Bias in Empathy
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“Fortunately, brain imaging research has contributed greatly to our understanding of the neural underpinnings of empathy and their associations with social behavior [11,12].”
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Are we really measuring empathy? Proposal for a new measurement framework
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“…in humans and we have not 449 addressed the implications of this new framework for non-human animal studies, which can 450 provide an important contribution to the understanding of the cognitive and affective processes 451 underlying empathy (de Waal & Preston, 2017; Panksepp & Panksepp, 2013).”
BackgroundNeural control of affiliative touch in prosocial interaction
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Empathy and emotion regulation: An integrative account
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“These diverse facets of empathy have been tentatively integrated by de Waal and Preston (2017) in their perception- action model or PAM.”
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Social circuits and their dysfunction in autism spectrum disorder
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Emotional contagion and prosocial behavior in rodents
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Human attachments shape interbrain synchrony toward efficient performance of social goals
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“Spontaneous facial expressions, as opposed to fake or manipulative expressions (Calvo et al. 2013), are considered as honest signals informing the observers about the internal emotional state of the performer (de Waal 2003; Gallese 2003; Gallese et al. 2004; de Waal and Preston 2017).”
BackgroundUnderstanding others: Emotion recognition in humans and other animals
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Neural basis of prosocial behavior
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The neural development of empathy is sensitive to caregiving and early trauma
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Facial mimicry, empathy, and emotion recognition: a meta-analysis of correlations
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“Next, the perception action model (PAM) claims that imitation responses, such as facial mimicry, can motivate altruism by enhancing personal investment in the emotions of others (de Waal & Preston, 2017; Preston & de Waal, 2002).”
BackgroundConduct Disorders and Empathy Development
Frick, P. J., & Kemp, E. C. (2020) · Annual Review of Clinical Psychology · doi:10.1146/annurev-clinpsy-081219-105809 · Cited by 114 · see citing works
Comparing the value of perceived human versus AI-generated empathy
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“It enhances resilience 16 and serves as a catalyst for prosocial and altruistic behaviour in humans 17–20 as well as other mammals 21,22 .”
Neural Basis of Observational Fear Learning: A Potential Model of Affective Empathy
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Why contagious yawning does not (yet) equate to empathy
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A meta‐analysis of the relationship between empathy and executive function
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The contagion of social defeat stress: Insights from rodent studies
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Physiological synchrony is associated with cooperative success in real-life interactions
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Embodied stress: The physiological resonance of psychosocial stress
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Modeling empathy: building a link between affective and cognitive processes
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“A definition of empathy as an umbrella term for any type of process triggered by observing the others’ emotional states and activating one’s own (de Waal and Preston 2017), has been used as an attempt to cover this broad range of behaviors.”
BackgroundMethodInfluentialEmotional contagion in nonhuman animals: A review
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Harm to Others Acts as a Negative Reinforcer in Rats
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The causal role of the somatosensory cortex in prosocial behaviour
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Challenges in the comparative study of empathy and related phenomena in animals
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Synchronous caregiving from birth to adulthood tunes humans’ social brain
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Whale and dolphin behavioural responses to dead conspecifics
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A Missense Variant at the Nrxn3 Locus Enhances Empathy Fear in the Mouse
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Neural mechanisms necessary for empathy-related phenomena across species
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The neurodevelopmental precursors of altruistic behavior in infancy
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The Role of Sensorimotor Processes in Pain Empathy
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The social dilemma: prefrontal control of mammalian sociability
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“These findings are consistent with an evolutionary theory of cooperation that expects helping behavior to occur disproportionately between genetically related or reciprocating individuals (de Waal & Preston, 2017; Axelrod & Hamilton, 1981; Vázquez, Gómez, Ordoñana, Swann, & Whitehouse, 2017).”
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Modern theories of human evolution foreshadowed by Darwin’s <i>Descent of Man</i>
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Why we heal: The evolution of psychological healing and implications for global mental health
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Laughter, play faces and mimicry in animals: evolution and social functions
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Cortical regulation of helping behaviour towards others in pain
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Therapeutic Alliance as Active Inference: The Role of Therapeutic Touch and Synchrony
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Dysfunction of Empathy and Related Processes in Borderline Personality Disorder: A Systematic Review
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Technologically-assisted communication attenuates inter-brain synchrony
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Empathy framework for embodied conversational agents
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“…processes discovered and defined in the domain of actions “result from the fact that the subject’s representations of the emotional state are automatically activated when the subject pays attention to the emotional state of the object” (Preston and de Waal, 2002, p. 1; de Waal and Preston, 2017).”
BackgroundPhysiological synchrony is associated with attraction in a blind date setting
Prochazkova, E., Sjak-Shie, E., Behrens, F., Lindh, D., & Kret, M. E. (2021) · Nature Human Behaviour · doi:10.1038/s41562-021-01197-3 · Cited by 80 · see citing works
“The function of physiological synchrony is not well understood, but similar to motor mimicry (for example, facial expression mimicry), it may help people to align emotionally 15,16 .”
A computational model of empathy for interactive agents
Yalcin, O. N., & DiPaola, S. (2018) · Biologically Inspired Cognitive Architectures · doi:10.1016/j.bica.2018.07.010 · Cited by 71 · see citing works
“Empathy, as the capacity to relate another’s emotional state [3], is found to evoke altruistic and prosocial behavior, have a positive effect on the length of relationship, provide competence in communication and have a negative effect on aggressive behavior [4].”
BackgroundInfluentialShalev, I., Warrier, V., Greenberg, D. M., Smith, P. L., Allison, C. L., Baron‐Cohen, S., Eran, A., & Uzefovsky, F. (2022) · Autism Research · doi:10.1002/aur.2794 · Cited by 62 · see citing works
“Further support is provided by neuroimaging studies showing that CE and EE differ in brain activation and structure (de Waal & Preston, 2017; Shamay-Tsoory et al., 2008; Uribe et al., 2019).”
MethodLü, Y.-F., Ren, B., Ling, B.-F., Zhang, J., Chen, X., & Li, Z. (2017) · Neuroscience Letters · doi:10.1016/j.neulet.2017.10.063 · Cited by 62 · see citing works
The question of animal emotions
de Waal, F. Β. Μ., & Andrews, K. (2022) · Science · doi:10.1126/science.abo2378 · Cited by 62 · see citing works
Li, L., Zhang, L., He, Z., Ma, H., Zhang, Y., Xun, Y., Yuan, W., Hou, W., Li, Y.-T., Lv, Z., et al. (2021) · eLife · doi:10.7554/elife.67638 · Cited by 61 · see citing works
Facial mimicry and play: A comparative study in chimpanzees and gorillas.
Palagi, E., Norscia, I., Pressi, S., & Cordoni, G. (2018) · Emotion · doi:10.1037/emo0000476 · Cited by 61 · see citing works
“In both human and nonhuman animals, spontaneous facial expressions can unveil the internal states of individuals (Gallese, 2003; Gallese, Keysers, & Rizzolatti, 2004; de Waal & Preston, 2017).”
BackgroundValidating Rat Model of Empathy for Pain: Effects of Pain Expressions in Social Partners
Li, C.-L., Yang, Y., He, T., Wang, R.-R., Geng, K.-W., Du, R., Luo, W.-J., Wei, N., Wang, X., Wang, Y., et al. (2018) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2018.00242 · Cited by 60 · see citing works
“Debate and controversy still exists between the PAM (de Waal and Preston, 2017; Preston and de Waal, 2017) and the mirror system (Rizzolatti and Caruana, 2017) in terms of theoretical considerations about representations of empathy.”
BackgroundSommerlad, A., Huntley, J. D., Livingston, G., Rankin, K. P., & Fancourt, D. E. (2021) · PLoS ONE · doi:10.1371/journal.pone.0257557 · Cited by 62 · see citing works
Observational fear behavior in rodents as a model for empathy
Kim, A., Keum, S., & Shin, H. (2018) · Genes Brain & Behavior · doi:10.1111/gbb.12521 · Cited by 60 · see citing works
Empathy regulation, prosociality, and moral judgment
Cameron, C. D., Conway, P. J., & Scheffer, J. A. (2021) · Current Opinion in Psychology · doi:10.1016/j.copsyc.2021.09.011 · Cited by 59 · see citing works
Bidirectional cingulate-dependent danger information transfer across rats
Han, Y., Bruls, R., Soyman, E., Thomas, R. M., Pentaraki, V., Jelinek, N., Heinemans, M., Bassez, I., Verschooren, S., Pruis, I., et al. (2019) · PLoS Biology · doi:10.1371/journal.pbio.3000524 · Cited by 59 · see citing works
“Second, what is being transferred? One important distinction relates to the distinction between behavioral mimicry and emotional contagion [30,31].”
BackgroundLévy, J., Goldstein, A., Pratt, M., & Feldman, R. (2018) · Scientific Reports · doi:10.1038/s41598-018-19810-3 · Cited by 55 · see citing works
Sharing playful mood: rapid facial mimicry in Suricata suricatta
Palagi, E., Marchi, E., Cavicchio, P., & Bandoli, F. (2019) · Animal Cognition · doi:10.1007/s10071-019-01269-y · Cited by 56 · see citing works
Anterior Cingulate Cortex Signals Attention in a Social Paradigm that Manipulates Reward and Shock
Schneider, K. N., Sciarillo, X. A., Nudelman, J. L., Cheer, J. F., & Roesch, M. R. (2020) · Current Biology · doi:10.1016/j.cub.2020.07.039 · Cited by 55 · see citing works
Help or flight? Increased threat imminence promotes defensive helping in humans
Vieira, J. B., Schellhaas, S., Enström, E., & Olsson, A. (2020) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2020.1473 · Cited by 58 · see citing works
Morawetz, C., Berboth, S., & Bode, S. (2021) · NeuroImage · doi:10.1016/j.neuroimage.2021.117817 · Cited by 55 · see citing works
The association between acute stress & empathy: A systematic literature review
Nitschke, J. P., & Bartz, J. A. (2022) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2022.105003 · Cited by 57 · see citing works
Psychopathy to Altruism: Neurobiology of the Selfish–Selfless Spectrum
Sonne, J., & Gash, D. M. (2018) · Frontiers in Psychology · doi:10.3389/fpsyg.2018.00575 · Cited by 61 · see citing works
“As defined by de Waal and Preston (2017), empathy is a “term for all processes that emerge from the fact that observers understand others’ states by activating their own personal, neural, and mental representations of that state.””
BackgroundLi, L., Yuan, W., He, Z., Wang, L., Jing, X.-Y., Zhang, J., Yang, Y., Guo, Q., Zhang, X., Cai, W., et al. (2018) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2018.12.238 · Cited by 55 · see citing works
Towards a unified theory of emotional contagion in rodents—A meta-analysis
Hernandez-Lallement, J., Gómez-Sotres, P., & Carrillo, M. (2022) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2020.09.010 · Cited by 53 · see citing works
“Published literature on social behavior in rodents is quite extensive and ranges from the late 1940’s [14–25] to recent influential pieces unifying the building blocks of empathy across species [26,27].”
Bukowski, H., Tik, M., Silani, G., Ruff, C. C., Windischberger, C., & Lamm, C. (2020) · Cortex · doi:10.1016/j.cortex.2020.03.009 · Cited by 51 · see citing works
Sustainable Compassion Training: Integrating Meditation Theory With Psychological Science
Condon, P., & Makransky, J. (2020) · Frontiers in Psychology · doi:10.3389/fpsyg.2020.02249 · Cited by 53 · see citing works
Determinants of Social Cognitive Aging: Predicting Resilience and Risk
Henry, J. D., Grainger, S. A., & von Hippel, W. (2022) · Annual Review of Psychology · doi:10.1146/annurev-psych-033020-121832 · Cited by 53 · see citing works
Rats display empathic behavior independent of the opportunity for social interaction
Cox, S. S., & Reichel, C. M. (2019) · Neuropsychopharmacology · doi:10.1038/s41386-019-0572-8 · Cited by 51 · see citing works
Lévy, J., Yirmiya, K., Goldstein, A., & Feldman, R. (2019) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2019.100658 · Cited by 51 · see citing works
Upregulating positive affect through compassion: Psychological and physiological evidence
Förster, K., & Kanske, P. (2022) · International Journal of Psychophysiology · doi:10.1016/j.ijpsycho.2022.03.009 · Cited by 56 · see citing works
Measures of empathy and compassion: A scoping review
Vieten, C., Rubanovich, C. K., Khatib, L. A., Sprengel, M. L., Tanega, C., Polizzi, C. P., Vahidi, P., Malaktaris, A. L., Chu, G. M., Lang, A. J., et al. (2024) · PLoS ONE · doi:10.1371/journal.pone.0297099 · Cited by 50 · see citing works
- Authors
- de Waal, F. B. M., & Preston, S. D.
- Affiliations
- University of Michigan (US)
- Venue
- Nature Reviews Neuroscience
- Published
- 2017-06-29
- Volume
- 18
- Issue
- 8
- Pages
- 498-509
- ISSN
- 1471-003X (ISSN-L)
- 1471-0048
- OpenAlex
- W2732246028
- Cited by
- 957
- References
- 142
- Citations by year
- 2026: 97 · 2025: 111 · 2024: 149 · 2023: 119 · 2022: 132 · 2021: 120 · 2020: 92 · 2019: 74 · 2018: 50 · 2017: 13
- FWCI
- 9.86
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature reviews. Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- Funders
- University of Michigan
- Topics
- Social Sciences › Psychology › Social Psychology › Primate Behavior and Ecology
- Social Sciences › Psychology › Social Psychology › Action Observation and Synchronization
- Social Sciences › Psychology › Developmental and Educational Psychology › Child and Animal Learning Development
- Keywords
- empathy, affective empathy, cognitive empathy, perception-action model, mirror neurons, mirror neuron theory, consolation, neural basis of empathy, interspecies empathy, embodied representations, evolution of empathy
- MeSH terms
- Animals, Behavior, Animal, Brain, Emotions, Empathy, Biological Evolution, Humans, Mammals, Models, Neurological, Mirror Neurons
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