Mammalian empathy: behavioural manifestations and neural basis

Journal name:
Nature Reviews Neuroscience
Volume:
18,
Pages:
498–509
Year published:
DOI:
doi:10.1038/nrn.2017.72
Published online

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.

At a glance

Figures

  1. The Russian-doll model of the evolution of empathy.
    Figure 1: The Russian-doll model of the evolution of empathy.

    Various components of the empathic response, which have been added layer upon layer during evolution, remain functionally integrated. At its core is the perception–action mechanism, which induces a similar emotional state in the observer as in the target. Its most basic expressions are motor mimicry and emotional contagion. The doll's outer layers, such as empathic concern and perspective-taking, build upon this core socio-affective basis while increasingly requiring emotion regulation, self–other distinction and cognition. Even though the doll's outer layers depend on prefrontal functioning, they remain fundamentally linked to the core perception–action mechanism. Adapted with permission from: de Waal, F. B. M. in Feelings & Emotions: The Amsterdam Symposium (eds Manstead T., Frijda, N. & Fischer A.) 379–399 (Cambridge Univ. Press, 2003).

  2. Behavioural manifestations of animal empathy.
    Figure 2: Behavioural manifestations of animal empathy.

    The table summarizes behavioural patterns that are considered to be expressions of empathy in non-human vertebrates, ranging from motor mirroring and yawn contagion to targeted helping. Most of these behaviours have been characterized by experimental research, whereas others have been documented observationally (see the references cited in the main text). The mechanisms and the non-human species in which these behaviours have been observed are shown. From top to bottom, the images show the following: two gelada baboon juveniles with playfaces (that is, they are showing rapid facial mimicry) (part a); a yawning wolf (part b); prairie vole mates matching each other's physiological stress level (part c); a juvenile bonobo wrapping her arms around another who has just lost a fight to provide consolation (part d); a rat that has learned to liberate another rat that was trapped in a container (part e); and an adult chimpanzee showing targeted helping by assisting a juvenile's descent from a tree (part f). The images in parts a–f are courtesy of Pier Francesco Ferrari, University of Parma, Italy; Teresa Romero, University of Lincoln, UK; Zack Johnson, Georgia Institute of Technology, USA; Zanna Clay, Durham University, UK; and Inbal Ben-Ami Bartal, University of California, Berkeley, USA.

  3. From affect transfer to altruism.
    Figure 3: From affect transfer to altruism.

    As shown in multiple animal studies, empathy may promote aid-giving behaviour between conspecifics6, 57, 58. First, the target's distress induces stress or distress in the observer through emotional transfer (step 1). The observer needs to downregulate its own distress in order to effectively attend to the target, such as through helping or consolation (step 2). The resulting reduction of the target's distress as a result of being helped is then transferred back to the observer, ameliorating the observer's caught distress (step 3); this reduction constitutes an intrinsic reward for performed altruism (step 4).

  4. Both cognitive and affective empathy access distributed, person-specific affective representations.
    Figure 4: Both cognitive and affective empathy access distributed, person-specific affective representations.

    Bottom-up, affective empathy (red box) occurs when an observer directly perceives the emotional state (such as a sad facial expression) of the target. This naturally activates distributed, personal representations of the target's state in the observer (purple box). These representations have developed over time with experience in the observer's life and include associated memories, semantic concepts, and bodily states and expressions. When empathy proceeds in a top-down, cognitive manner (blue box), the neural regions that support working memory, executive function, emotion regulation and visuospatial processes instead access the affective empathy representations from the top-down (indicated by the arrows). Thus, although the stimulation emerges from inside the mind rather than from the outside world, the affective regions and the associated representations are shared between cognitive and affective processes. Thus, subtractions of affective from cognitive forms of empathy reveal greater brain activity in the blue regions than in the red regions. However, the cognitive process must still access the affective regions and their shared associated representations (purple) to provide the imagination or simulation with content and meaning.

  5. Neural regions that participate in human empathy.
    Figure 5: Neural regions that participate in human empathy.

    The figure shows a medial sagittal view (far left), a left lateral side view (centre) and a coronal view (far right) of the human brain, and indicates the relative locations and roles of brain areas that are involved in human empathy. Affective representations are required to imagine how another person feels. Depending on the task, however, the observed neural activity will emphasize bottom-up, affective brain areas or top-down, cognitive ones. Regions that are more associated with affective empathy tasks — such as direct perception of the emotion or pain of another person — are shown in red: the anterior cingulate cortex (ACC) including perigenual and subgenual regions of the ACC, amygdala, thalamus, hypothalamus, primary motor cortex (M1), premotor cortex, the primary and secondary somatosensory cortices (S1 and S2), and the temporal pole (TP). Brain regions that are more associated with higher-level, top-down forms of empathy — such as imagining how you would feel in the place of another or taking their perspective — are shown in blue: the dorsolateral prefrontal cortex (DLPFC), inferior parietal lobule (IPL), temporoparietal junction (TPJ), superior temporal gyrus (STG) and fusiform gyrus (FG). Two regions that are commonly activated in both affective and cognitive tasks are shown in green: the anterior insula (AI) and the anterior middle cingulate cortex (aMCC), which extends dorsally into the supplementary motor area (SMA) and cingulate motor area (CMA). Neural locations are approximated so that the regions can be viewed in just three images (for example, the FG is normally too medial to be seen in the lateral image, the amygdala is shown in the medial view as emerging from behind the visible midline slice in right temporal cortex, and differences in laterality by region and task are not represented). IFG, inferior frontal gyrus; PI, posterior insula; VMPFC, ventromedial PFC.

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Author information

  1. Both authors contributed equally to this work.

    • Frans B. M. de Waal &
    • Stephanie D. Preston

Affiliations

  1. Psychology Department and Living Links, Yerkes National Primate Research Center, Emory University, 36 Eagle Row, Atlanta, Georgia 30322, USA.

    • Frans B. M. de Waal
  2. Department of Psychology, University of Michigan, 530 Church Street, Ann Arbor, Michigan 48109, USA.

    • Stephanie D. Preston

Competing interests statement

The authors declare no competing interests.

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Author details

  • Frans B. M. de Waal

    Frans B. M. de Waal is a Dutch-American ethologist and biologist who has published widely about primate behaviour and social cognition. He received his Ph.D. in 1977 from the University of Utrecht, The Netherlands, and is presently C. H. Candler Professor at Emory University and the Director of Living Links at the Yerkes National Primate Research Center, Georgia, USA. He is also a distinguished professor at the University of Utrecht and is a member of the National Academy of Sciences.

  • Stephanie D. Preston

    Stephanie D. Preston is an interdisciplinary psychologist with a B.A. in cognitive science from the University of Virginia, USA, an M.A. and a Ph.D. in behavioural neuroscience from the University of California, Berkeley, USA, and a postdoctoral fellowship in neurology from the University of Iowa, USA. She is a professor at the University of Michigan, USA, where she studies the impact of implicit emotional processes on prosocial behaviour, hoarding, consumer behaviour and pro-environmentalism.

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