Review
Is there a core neural network in empathy? An fMRI based quantitative meta-analysis

https://doi.org/10.1016/j.neubiorev.2010.10.009Get rights and content

Abstract

Whilst recent neuroimaging studies have identified a series of different brain regions as being involved in empathy, it remains unclear concerning the activation consistence of these brain regions and their specific functional roles. Using MKDA, a whole-brain based quantitative meta-analysis of recent fMRI studies of empathy was performed. This analysis identified the dACC-aMCC-SMA and bilateral anterior insula as being consistently activated in empathy. Hypothesizing that what are here termed affective–perceptual and cognitive–evaluative forms of empathy might be characterized by different activity patterns, the neural activations in these forms of empathy were compared. The dorsal aMCC was demonstrated to be recruited more frequently in the cognitive–evaluative form of empathy, whilst the right anterior insula was found to be involved in the affective–perceptual form of empathy only. The left anterior insula was active in both forms of empathy. It was concluded that the dACC-aMCC-SMA and bilateral insula can be considered as forming a core network in empathy, and that cognitive–evaluative and affective–perceptual empathy can be distinguished at the level of regional activation.

Research highlights

▶ A core network of brain regions underlies empathy across all stimuli and tasks. ▶ This network consists of the dACC-aMCC-SMA and bilateral anterior insula. ▶ Cognitive–evaluative and affective–perceptual empathy differ neurally. ▶ C–E empathy involves dorsal aMCC specifically; A–P empathy the right AI.

Introduction

Empathy, a phenomenon characterizing our understanding and sharing of others’ feelings, is vital to our everyday communication and survival in a social environment (Eisenberg and Strayer, 1987). Although the definition of empathy differs somewhat from study to study (see a detailed review in Batson, 2009), it can be broadly defined as the experiencing of an affective or sensory state similar to that shown by a perceived individual, where one is aware as to whether the source of the state is oneself or another. This operational definition allows empathy to be distinguished from related concepts such as sympathy and theory-of-mind (both of which involve an understanding but no sharing of another's state), as well as emotional contagion (where there is no awareness as to whether the source of the experienced state is the self or another). Whilst an increasing number of neuroimaging studies of empathy have been carried out, these have not so far provided consistent answers to several fundamental empathy-related questions. More specifically, it remains unclear as to whether differing forms of empathy tasks and stimuli elicit common patterns of neural activation, or whether instead these produce disparate, task- or stimulus-specific, neural responses.

Studies have utilised tasks and stimuli that range across a number of domains. A variety of feelings – such as pain (Morrison et al., 2004, Singer et al., 2004), disgust (Jabbi et al., 2007, Wicker et al., 2003), and happiness (Chakrabarti et al., 2006, Hennenlotter et al., 2005, Jabbi et al., 2007) – have been used as targets for empathy, with, in addition, empathy being induced through either simple observation (Blakemore et al., 2005, Grosbras and Paus, 2006, Keysers et al., 2004, Singer et al., 2004, Singer et al., 2006, Wicker et al., 2003), imagination (Jackson et al., 2006a, Lamm et al., 2007), or evaluation (Gu and Han, 2007, Jackson et al., 2005, Moriguchi et al., 2007). This variation, and the concurrent variation in reported regions of activity, has meant that it remains unclear as to which brain regions are consistently activated in empathy, and thus whether or not there is a core network within the brain that underlies empathy across all stimulus domains.

Some empathy studies have reported that an empathic response can be evoked automatically in participants through observation, without them being aware of the goal of the experiments (Blakemore et al., 2005, Keysers et al., 2004, Singer et al., 2004, Singer et al., 2006, Wicker et al., 2003). This can be termed an ‘affective–perceptual’ form of empathy. In contrast, other studies have suggested that empathic responses are substantially influenced by whether or not one attends to the feelings of the target through the explicit imagination or evaluation of feelings (Fan and Han, 2008, Gu and Han, 2007, Preston et al., 2007; see more detailed review in Singer and Lamm, 2009). This ‘cognitive–evaluative’ form of empathy may thus potentially be differentiated from the ‘affective–perceptual’ form. Whether this is case or not remains unclear, however.

To effectively approach these unanswered empathy-related questions, a quantitative meta-analysis of recent fMRI studies of empathy was carried out using the MKDA approach (Kober et al., 2008a). This method allows the identification of those areas that are consistently activated in empathy across all task and stimulus domains, and thus allows the question as to whether there is a core network in empathy to be answered. The meta-analytical method also allows those regions that are active during cognitive–evaluative empathy tasks to be compared with those activated by affective–perceptual empathy tasks, revealing to what extent the brain response to these task types overlaps or differs. The approach adopted here has the advantage over the small number of prior empathy-related meta-analyses of studying activations across the whole brain, rather than any one specific region (specifically the temperoparietal junction in Decety and Lamm, 2007; and the medial prefrontal cortex in Seitz et al., 2006).

It was hypothesised, firstly, that a set of core regions would be found to be active across all empathy task domains; and, secondly, that a differentiation would be seen between the non-core regions active in cognitive–evaluative and affective–perceptual empathy tasks. Based upon the literature, it was further hypothesised that cognitive–evaluative empathy would specifically recruit cortical midline structures such as the anterior mid-cingulate cortex (aMCC) and dorso-medial pre-frontal cortex (DMPFC) (Lamm et al., 2007), whilst regions such as the insula and midbrain would be preferentially recruited in affective–perceptual empathy (Craig, 2009, Phan et al., 2002).

Section snippets

Study selection

A step-wise procedure was used to identify the relevant experimental articles. First, studies were selected through a standard search in PubMed (http://www.pubmed.gov) and ISI Web of Science (http://apps.isiknowledge.com), with keywords [‘empathy’ OR ‘empathic’ OR ‘emotion contagion’ OR ‘affective theory of mind’ OR ‘affective mentalizing’] AND [‘fMRI’ OR ‘magnetic resonance imaging’]. Search terms other than empathy were included in order to identify any relevant studies that may have been

Description of the selected studies and the balances between its categorizations

Forty studies – with 50 contrasts and 664 peak coordinates – were considered to be relevant for empathy, and thus included in our analysis (see Supplementary Table 1). Among these 50 contrasts, 32 contrasts investigating the affective–perceptual forms of empathy were compared with 18 contrasts investigating the cognitive–evaluative forms of empathy. The stimulus modality investigated in these contrasts is described in Supplementary Table 2. Chi-square test showed no significant difference

Discussion

A quantitative meta-analysis on fMRI studies of empathy was conducted in order to, firstly, determine the existence of a shared network of brain regions across all task and stimulus domains; and, secondly, to identify any differences in brain activation between two putative empathy types, affective–perceptual and cognitive evaluative. As hypothesised, a collection of brain regions consistently activated during empathy, independent of task and stimulus type, was identified, consisting of the

Acknowledgments

The study was supported by a Heisenberg grant from the Salus Foundation, German Research Foundation (DFG, 304/4-1 to G.N.), the SFB/DFG (SFB (779-A6 to G.N.), and the Hope of Depression Research Foundation (HDRF) (to G.N).

References (85)

  • C.A. Hynes et al.

    Differential role of the orbital frontal lobe in emotional versus cognitive perspective-taking

    Neuropsychologia

    (2006)
  • M. Jabbi et al.

    Empathy for positive and negative emotions in the gustatory cortex

    Neuroimage

    (2007)
  • P.L. Jackson et al.

    Empathy examined through the neural mechanisms involved in imagining how I feel versus how you feel pain

    Neuropsychologia

    (2006)
  • P.L. Jackson et al.

    How do we perceive the pain of others? A window into the neural processes involved in empathy

    Neuroimage

    (2005)
  • P.L. Jackson et al.

    To what extent do we share the pain of others? Insight from the neural bases of pain empathy

    Pain

    (2006)
  • C. Keysers et al.

    A touching sight: SII/PV activation during the observation and experience of touch

    Neuron

    (2004)
  • H. Kober et al.

    Functional grouping and cortical-subcortical interactions in emotion: a meta-analysis of neuroimaging studies

    NeuroImage

    (2008)
  • H. Kober et al.

    Functional grouping and cortical-subcortical interactions in emotion: a meta-analysis of neuroimaigng studies

    Neuroimage

    (2008)
  • E.J. Lawrence et al.

    The role of ‘shared representations’ in social perception and empathy: an fMRI study

    Neuroimage

    (2006)
  • K.R. Leslie et al.

    Functional imaging of face and hand imitation: towards a motor theory of empathy

    Neuroimage

    (2004)
  • J.S. Morris et al.

    Saying it with feeling: neural responses to emotional vocalizations

    Neuropsychologia

    (1999)
  • K.L. Phan et al.

    Functional neuroanatomy of emotion: a meta-analysis of emotion activation studies in PET and fMRI

    NeuroImage

    (2002)
  • G. Salimi-Khorshidi et al.

    Meta-analysis of neuroimaging data: a comparison of image-based and coordinate-based pooling of studies

    NeuroImage

    (2009)
  • M. Schulte-Ruther et al.

    Gender differences in brain networks supporting empathy

    NeuroImage

    (2008)
  • T. Singer

    The neuronal basis and ontogeny of empathy and mind reading: review of literature and implications for future research

    Neurosci. Biobehav. Rev.

    (2006)
  • T. Singer et al.

    A common role of insula in feelings, empathy and uncertainty

    Trends Cogn. Sci.

    (2009)
  • B.A. Vogt et al.

    Cytology of human dorsal midcingulate and supplementary motor cortices

    J. Chem. Neuroanat.

    (2003)
  • B. Wicker et al.

    Both of us disgusted in My insula: the common neural basis of seeing and feeling disgust

    Neuron

    (2003)
  • C.D. Batson

    These things called empathy

  • F. Benuzzi et al.

    Does it look painful or disgusting? Ask your parietal and cingulate cortex

    J. Neurosci.

    (2008)
  • S.J. Blakemore et al.

    Somatosensory activations during the observation of touch and a case of vision-touch synaesthesia

    Brain

    (2005)
  • M. Brett

    The MNI Brain and the Talairach Atlas

    (1999)
  • L. Carr et al.

    Neural mechanisms of empathy in humans: a relay from neural systems for imitation to limbic areas

  • B. Chakrabarti et al.

    Empathizing with basic emotions: common and discrete neural substrates

    Soc. Neurosci.

    (2006)
  • Q. Chen et al.

    Empathy is moderated by genetic background in mice

    PLoS ONE

    (2009)
  • A.D. Craig

    How do you feel? Interoception: the sense of the physiological condition of the body

    Nat. Rev. Neurosci.

    (2002)
  • A.D. Craig

    Interoception: the sense of the physiological condition of the body

    Curr. Opin. Neurobiol.

    (2003)
  • A.D. Craig

    How do you feel--now? The anterior insula and human awareness

    Nat. Rev. Neurosci.

    (2009)
  • H.D. Critchley et al.

    Neural systems supporting interoceptive awareness

    Nat. Neurosci.

    (2004)
  • B. de Gelder et al.

    Fear fosters flight: a mechanism for fear contagion when perceiving emotion expressed by a whole body

    Proc. Natl. Acad. Sci. U.S.A.

    (2004)
  • J. Decety

    To what extent in the experience of empathy mediated by shared neural circuits?

    Emotion Rev.

    (2010)
  • J. Decety et al.

    The functional architecture of human empathy

    Behav. Cogn. Neurosci. Rev.

    (2004)
  • Cited by (708)

    View all citing articles on Scopus
    View full text