Multidimensional assessment of empathic abilities: Neural correlates and gender differences

https://doi.org/10.1016/j.psyneuen.2009.10.006Get rights and content

Summary

Empathy is a multidimensional construct and comprises the ability to perceive, understand and feel the emotional states of others. Gender differences have been reported for various aspects of emotional and cognitive behaviors including theory of mind. However, although empathy is not a single ability but a complex behavioral competency including different components, most studies relied on single aspects of empathy, such as perspective taking or emotion perception. To extend those findings we developed three paradigms to assess all three core components of empathy (emotion recognition, perspective taking and affective responsiveness) and clarify to which extent gender affects the neural correlates of empathic abilities. A functional MRI study was performed with 12 females (6 during their follicular phase, 6 during their luteal phase) and 12 males, measuring these tasks as well as self-report empathy questionnaires.

Data analyses revealed no significant gender differences in behavioral performance, but females rated themselves as more empathic than males in the self-report questionnaires. Analyses of functional data revealed distinct neural networks in females and males, and females showed stronger neural activation across all three empathy tasks in emotion-related areas, including the amygdala. Exploratory analysis of possible hormonal effects indicated stronger amygdala activation in females during their follicular phase supporting previous data suggesting higher social sensitivity and thus facilitated socio-emotional behavior. Hence, our data support the assumption that females and males rely on divergent processing strategies when solving emotional tasks: while females seem to recruit more emotion and self-related regions, males activate more cortical, rather cognitive-related areas.

Introduction

Gender differences in different behavioral domains, among them several emotional competencies (Bradley et al., 2001, Grossman and Wood, 1993, Kring and Gordon, 1998) have been documented for a long time. Several studies demonstrated that females frequently report about more intense but also more negative emotions than males (e.g., Fischer et al., 2004, Tobin et al., 2000, Vrana and Rollock, 2002). Despite a general ability in both genders to correctly infer the emotional state of others, some studies suggest that female subjects show significantly better performance in emotion recognition and expression than male participants (e.g., Goos and Silverman, 2002, Hall and Matsumoto, 2004, Montagne et al., 2005). However, a growing body of research demonstrates no gender differences in behavioral parameters but in the underlying neural network, ranging from different activation in frontal regions to subcortical areas such as the amygdala (e.g., Kemp et al., 2004, Lee et al., 2002, Lee et al., 2005). Applying neuroimaging tools, a stronger lateralization of these neural networks in males during emotion processing has frequently been observed (e.g., Kesler-West et al., 2001, Killgore and Yurgelun-Todd, 2001; for meta-analysis see Wager et al., 2003). Some studies also report a significant interaction of emotional valence and gender of participants on neural activation, particularly affecting the amygdala (Schienle et al., 2005, Wrase et al., 2003). Moreover, divergent results regarding activation of the amygdala and orbitofrontal cortex have also been demonstrated in adolescent girls and boys (e.g., McClure et al., 2004). Recently, Li et al. (2008) reported significant attentional and evaluative biases for moderately negative pictures, showing that women might be particularly more sensitive to less salient stimuli. Gender differences have also been observed for the neural correlates of interaction of emotion and cognition (Koch et al., 2007, Seubert et al., 2009) and also for mood induction with happy and sad facial expressions (Schneider et al., 2000), emotional pictures (Hofer et al., 2006) and emotional words (Hofer et al., 2007). These studies indicated that females and males use different neural networks comprising various frontal and temporal regions as well as subcortical areas such as the amygdala for the processing and experiencing of positive and negative emotions.

Concerning empathy and empathic behavior, several studies have suggested that females might be more empathic than males, but mostly relied on self-report data (e.g., Baron-Cohen and Wheelwright, 2004, Eisenberg and Lennon, 1983, Hoffman, 1977, Rueckert and Naybar, 2008) possibly prompting gender stereotype responses. The influence of such stereotypes on behavior as well as cerebral responses has been demonstrated impressively (Krendl et al., 2008). Hence, assessments of empathic abilities should avoid stimulating such stereotypes.

Besides self-report, gender differences in empathy have also been shown using functional neuroimaging, for example Singer et al. (2006) studied brain activity while female and male subjects underwent mild electric shocks or witnessed a confederate receiving a similar shock. While females showed a response in pain-related areas even when an unfairly behaving confederate received a shock, males exhibited activation in brain regions associated with reward, i.e. nucleus accumbens and orbitofrontal cortex, under this condition. Using EEG, a similar effect has been reported by Fukushima and Hiraki (2006), who observed a medial-frontal negative component in women and men when they lost in a gambling task, but interestingly, women also showed this pattern when they only observed a negative outcome for their confederate. Additionally, Han et al. (2008) observed a stronger modulation of the long latency response associated with affective empathy in females than males in a pain judgment task. Recently, gender differences have also been reported for the neural correlates of emotional perspective taking (Schulte-Rüther et al., 2008) using an emotional attribution task. The results suggest that the better performance of females is related to an enhanced recruitment of inferior frontal and superior temporal regions, while males activate the left temporo-parietal junction instead when assessing emotional states of others and themselves.

Taken together, these findings suggest that, although males and females may not differ in terms of behavioral and peripheral physiological measures of emotional responsiveness, the two genders may well differ in the recruitment of cerebral networks (e.g., Kemp et al., 2004, Schulte-Rüther et al., 2008). However, due to the heterogeneity of task demands, neuroimaging tools and data analysis, the nature of these differences remains unclear. While most studies explored empathic abilities using pain-related paradigms (e.g., Singer et al., 2006), only Schulte-Rüther et al. (2008) explored differences regarding empathic abilities for some basic emotions.

To evaluate these previous findings, it is important to mention, that empathy is a multidimensional construct and requires the ability to perceive, understand and feel the emotional states of others. Due to the complexity of the construct empathy has various definitions, but according to most models one can derive at least three core components (Decety and Jackson, 2004): (a) recognition of emotions in oneself and others via facial expressions, speech or behavior, (b) the sharing of emotional states with others, i.e. the ability to experience similar emotions as others while being conscious that this is the simulation of the emotional feeling and it is not one's own emotion (affective responsiveness), and (c) to take the perspective of another person, though the distinction between self and other remains intact (emotional perspective taking). In light of the heterogeneity of previous studies on gender differences in emotional competencies and their neural correlates, this is the first study to assess the neural network underlying all three defining components of empathy in females and males. This approach enabled a more encompassing and detailed analysis of these emotional competencies, their interactions and possible general and task-specific gender differences.

Based on prior results (e.g., Rueckert and Naybar, 2008), we hypothesized higher empathy scores of females in self-report measures. Moreover, considering previous neuroimaging studies on emotional competencies and separate empathy components, we hypothesized a significant difference between females and males in the cerebral networks underlying the empathy components due to diverging processing strategies and sensitivity to emotional stimuli (e.g., Li et al., 2008, Schulte-Rüther et al., 2008). Since the amygdala has been known to be essential for the evaluation and relevance detection of emotional stimuli (cf. Sander et al., 2003) and gender differences in amygdala activation during emotion processing have been reported frequently, we aimed to determine its exact role in the different components of empathy.

Regarding previous results (e.g, Schulte-Rüther et al., 2008), we assume that during emotional perspective taking and emotion recognition females will recruit more emotion-related regions such as the inferior frontal and superior temporal gyrus, while males will exhibit stronger activation in the temporo-parietal junction. Finally, for affective responsiveness we hypothesize overall stronger neural activation in female subjects, and particularly in the superior temporal and medial-frontal regions as well as the amygdala (cf. Hofer et al., 2006, Hofer et al., 2007).

Due to our preceding results (Derntl et al., 2008a, Derntl et al., 2008b) we also conducted exploratory analyses concerning the influence of cycle phase on the activation pattern and suggested more pronounced responses in emotional networks during the follicular phase.

Section snippets

Sample

Twelve right handed healthy Caucasian females aged 23–40 years (mean age 28.3 years, SD = 6.6) and twelve right handed healthy Caucasian males aged 21–34 years (mean age 26.3 years, SD = 4.1) participated in the study. They were recruited via advertisements posted at the RWTH Aachen University, Germany. All subjects were paid for their participation and written informed consent was obtained. The study was approved by the local Institutional Review Board and subjects were treated according to the

Behavioral performance

Due to an error of the response device, behavioral data of one male subject were not included in the final analysis.

Discussion

In this fMRI study we investigated the neural networks underlying empathic behavior in healthy females and males. We assessed empathic abilities with three tasks separately tapping the core components of this human competency: (1) emotion recognition, (2) emotional perspective taking, and (3) affective responsiveness. Additionally, we gathered self-report data from empathy questionnaires. Despite similar behavioral performance, functional data analyses revealed that females and males showed

Conclusion

We observed significant gender differences in the neurobiological substrates underlying the processing of three separate tasks tapping the core components of empathy resulting in a similar behavioral outcome. Our results strongly support the assumption that females recruit more emotion-related regions, whereas males engage a different neural network, rather associated with cognitive evaluation, mentalizing, and behavior anticipation.

Role of funding source

Funding for this study was provided by the Interdisciplinary Centre for Clinical Research (ICCR) of the Medical Faculty RWTH Aachen University (IZKF, TVN70 to U.H.); the ICCR had no further role in study design; in the collection, analysis and interpretation of data; in the writing of the report; and in the decision to submit the paper for publication.

Conflict of interest

None declared.

Acknowledgements

B.D. and A.F. were supported by the Interdisciplinary Centre for Clinical Research of the Medical Faculty RWTH Aachen University (IZKF, TVN70 to U.H.) and the International Research Training Group (IRTG 1328) of the German Research Foundation (DFG). UH was further supported by the DFG (KFO 112).

References (93)

  • U. Habel et al.

    Amygdala activation and facial expressions: explicit emotion discrimination versus implicit emotion processing

    Neuropsychologia

    (2007)
  • S. Han et al.

    Gender difference in empathy for pain: an electrophysiological investigation

    Brain Res.

    (2008)
  • A. Hofer et al.

    Gender differences in regional cerebral activity during the perception of emotion: a functional MRI study

    NeuroImage

    (2006)
  • A.H. Kemp et al.

    Gender differences in the cortical electrophysiological processing of visual emotional stimuli

    NeuroImage

    (2004)
  • M.L. Kesler-West et al.

    Neural substrates of facial emotion processing using fMRI

    Cogn. Brain. Res.

    (2001)
  • T.T. Kircher et al.

    The neural correlates of intentional and incidental self processing

    Neuropsychologia

    (2002)
  • R. Knickmeyer et al.

    Fetal testosterone and empathy

    Horm. Behav.

    (2006)
  • K. Koch et al.

    Gender differences in the cognitive control of emotion: an fMRI study

    Neuropsychologia

    (2007)
  • T.M. Lee et al.

    Gender differences in neural correlates of recognition of happy and sad faces in humans assessed by functional magnetic resonance imaging

    Neurosci. Lett.

    (2002)
  • H. Li et al.

    The neural mechanism underlying the female advantage in identifying negative emotions: an event-related potential study

    NeuroImage

    (2008)
  • E.A. Maguire et al.

    The brain network associated with acquiring semantic knowledge

    NeuroImage

    (2004)
  • E.B. McClure et al.

    A developmental examination of gender differences in brain engagement during evaluation of threat

    Biol. Psychiatry

    (2004)
  • E. Moser et al.

    Amygdala activation at 3 T in response to human and avatar facial expressions of emotions

    J. Neurosci. Methods

    (2007)
  • J. Narumoto et al.

    Attention to emotion modulates fMRI activity in human right superior temporal sulcus

    Brain. Res. Cogn. Brain Res.

    (2001)
  • R. Pearson et al.

    Fear recognition across the menstrual cycle

    Horm. Behav.

    (2005)
  • L. Pessoa et al.

    Fate of unattended fearful faces in the amygdala is determined by both attentional resources and cognitive modulation

    NeuroImage

    (2005)
  • K.L. Phan et al.

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

    NeuroImage

    (2002)
  • S. Phillips et al.

    Separating relational from item load effects in paired recognition: temporoparietal and middle frontal gyral activity with increased associates, but not items during encoding and retention

    NeuroImage

    (2002)
  • L. Rueckert et al.

    Gender differences in empathy: the role of the right hemisphere

    Brain Cogn.

    (2008)
  • A. Schienle et al.

    Brain activation of spider phobics towards disorder-relevant, generally disgust- and fear-inducing pictures

    Neurosci. Lett.

    (2005)
  • J.D. Schmahmann

    The role of the cerebellum in affect and psychosis

    J. Neurolinguistics

    (2000)
  • F. Schneider et al.

    Differential amygdala activation in schizophrenia during sadness

    Schizophr. Res.

    (1998)
  • M. Schulte-Rüther et al.

    Gender differences in brain networks supporting empathy

    NeuroImage

    (2008)
  • R.J. Seitz et al.

    Valuating other people's emotional face expression: a combined functional magnetic resonance imaging and electroencephalography study

    Neuroscience

    (2008)
  • B.A. Völlm et al.

    Neuronal correlates of theory of mind and empathy: a functional magnetic resonance imaging study in a nonverbal task

    NeuroImage

    (2006)
  • K. Vogeley et al.

    Mind reading: neural mechanisms of theory of mind and self-perspective

    NeuroImage

    (2001)
  • T.D. Wager et al.

    Valence, gender, and lateralization of functional brain anatomy in emotion: a meta-analysis of findings from neuroimaging

    NeuroImage

    (2003)
  • J. Wrase et al.

    Gender differences in the processing of standardized emotional visual stimuli in humans: a functional magnetic resonance imaging study

    Neurosci. Lett.

    (2003)
  • H. Ackermann et al.

    The contribution of the cerebellum to speech production and speech perception: clinical and functional imaging data

    Cerebellum

    (2007)
  • K. Amunts et al.

    Cytoarchitectonic mapping of the human amygdala, hippocampal region and entorhinal cortex: intersubject variability and probability maps

    Anat. Embryol. (Berl)

    (2005)
  • S. Aschenbrenner et al.

    Regensburger Word Fluency Test [Regensburger Wortflüssigkeits-Test, RWT]

    (2000)
  • A. Assmus et al.

    Functional interactions during the retrieval of conceptual action knowledge: a fMRI study

    J. Cogn. Neurosci.

    (2007)
  • S. Baron-Cohen et al.

    The empathy quotient: an investigation of adults with Asperger syndrome or high functioning autism, and normal sex difference

    J. Autism. Dev. Disord.

    (2004)
  • R.J. Blair

    Neurobiological basis of psychopathy

    Br. J. Psychiatry

    (2003)
  • M.M. Bradley et al.

    Emotion and motivation II: sex differences in picture processing

    Emotion

    (2001)
  • L. Carr et al.

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

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

    (2003)
  • Cited by (298)

    View all citing articles on Scopus
    View full text