Regular articleAging is associated with changes in the neural circuits underlying empathy
Introduction
Empathetic responding, which implies a shared interpersonal experience, is implicated in many aspects of social cognition, notably prosocial behavior, morality, and the regulation of aggression (Decety, 2010, Eisenberg and Eggum, 2009). Many behavioral studies have investigated the development of empathy during childhood (e.g., Bandstra et al., 2011, Roth-Hanania et al., 2011, Vaish and Warneken, 2012, Zahn-Waxler et al., 1992), and a few have begun to examine neuro-developmental changes using functional neuroimaging methods (Decety and Michalska, 2010, Decety et al., 2008, Decety et al., 2012). Much less is known about the developmental changes in empathy over the life span. To the best of our knowledge, no study has yet examined the neuro-hemodynamic response underlying empathy in elderly adults in comparison with younger adults. Such studies are critical to advance our understanding of typical aging processes, and can provide insight into neurodegenerative conditions associated with socioemotional deficits (Gleichgerrcht et al., 2011, Lough et al., 2006).
Empathy is a construct that has been defined in multiple ways using various criteria (Batson, 2009). While empathy is often viewed as feelings of concern for another, it is important to note that empathy is a multidimensional construct composed of dissociable neurocognitive components that include sensorimotor resonance, emotional, and cognitive components. Emotional empathy involves the capacity to either share or becomes affectively aroused by others' emotions, commonly referred to as emotion contagion or empathic arousal. Cognitive empathy operates similarly to the construct of theory of mind and perspective-taking, that is the ability to explain, predict, and interpret behavior by attributing mental states such as desires, beliefs, intentions, and emotions to oneself and to others (Decety and Svetlova, 2012).
The neural mechanisms underlying the emotional component of empathy have been well studied in adults particularly with regards to the perception of pain and distress in others. Numerous neuroimaging studies have demonstrated the reliable activation of a neural network involved in pain processing, including the anterior mid-cingulate cortex (aMCC), anterior insular cortex (AIC), supplementary motor area (SMA), and periaqueductal gray area. Activation of this network has been reported in response to facial expressions of pain, body parts being injured, imagining the pain of others, or simply anticipating harm to someone (Botvinick et al., 2005, Chen et al., 2012, Cheng et al., 2007, Cheng et al., 2010, Decety and Porges, 2011, Decety et al., 2010, Jackson et al., 2005, Jackson et al., 2006, Lamm et al., 2007, Singer et al., 2004). Of particular importance, the involvement of the AIC is nearly ubiquitous in studies of pain empathy (Gu et al., 2010). The aMCC, a region that implements a domain-general process integral to negative affect, pain, and cognitive control, is activated by anticipation of pain and instrumental escape from pain (Shackman et al., 2011).
The cognitive component of empathy partially overlaps with the construct of affective theory of mind, which accounts for the intersubjective awareness that other individuals', internal subjective states may be similar or different from our own (Shamay-Tsoory, 2009). The ability to conceptualize and reflect on our own and other's emotions, to appreciate that these can differ, is central to socioemotional competence. Functional neuroimaging studies have identified a circumscribed neural network reliably underpinning the understanding of mental states, linking the medial prefrontal cortex (mPFC), posterior superior temporal sulcus and/or temporoparietal junction (pSTS/TPJ), and temporal poles and/or amygdala (Brunet et al., 2000, Choudhury et al., 2009, Vollm et al., 2006). Particularly, the mPFC has been reported to preserve the cortical thickness in the elderly individuals (Salat et al., 2004). When engaging in the self-referencing and mentalizing tasks, older adults and younger counterparts could elicit comparable activations in the mPFC and pSTS and/or TPJ (Castelli et al., 2010, Gutchess et al., 2007).
Evidence about age-related changes in empathy from self-reported questionnaires and performance-based tasks is mixed. Driven by large samples consisting of individuals in their teens or early 20s through later adulthood (i.e., the 70s or 80s), some studies suggest age-related stability in empathy (Diehl et al., 1996, Eysenck et al., 1985), whereas other studies point to a pattern of negative age differences in empathy (Grühn et al., 2008, Helson et al., 2002, Phillips et al., 2002, Schieman and van Gundy, 2000). When dichotomizing the cognitive and emotional components of empathy, the findings are also inconclusive. One study found that older adults regulate their emotions more effectively than younger counterparts (Gross et al., 1997), whereas another reported reduced cognitive empathy in late adulthood (Bailey and Henry, 2008, Bailey et al., 2008). Furthermore, based exclusively on emotion recognition tasks, a growing body of evidence reports an age-related decline (Ruffman et al., 2008 for a meta-analysis). Importantly, contextual factors, such as the age-relevance of the emotion-elicitor (Charles and Piazza, 2007), seem to moderate age differences in empathic accuracy and emotional congruence (Richter and Kunzmann, 2011).
The ability to perceive others in pain is an empathetic capacity with great evolutionary significance. When individuals perceive others in physical pain, agency plays an important role in whether the action resulting in the pain is perceived as intentional or accidental (Akitsuki and Decety, 2009, Decety et al., 2008). Specifically, whether harm was caused intentionally or not, influences self-reported pain (Gray and Wegner, 2008) and neural responses (Decety et al., 2012). The perception of agency is a critical aspect in social understanding (Decety and Grèzes, 2006; Decety and Sommerville, 2003). Accordingly, we chose to use 2 categories of empathy-eliciting stimuli, depicting an individual in pain caused either accidentally by oneself or intentionally by another, with a well-validated functional magnetic resonance imaging (fMRI) paradigm in participants aged between 20 and 80 years to examine the aging trajectories underpinning emotional empathy and perceived agency. According to previous fMRI studies (Akitsuki and Decety, 2009, Decety et al., 2009), the AIC and aMCC involvement in response to perceiving others' pain primarily reflects emotional empathy, whereas the mPFC and pSTS and/or TPJ activation represents the neural computation involved in the perception of agency. It was hypothesized that, if aging affects emotional empathy, the hemodynamic response and effective connectivity between AIC and aMCC elicited by the perception of pain in others would change with age. On the other hand, if decline in understanding agency were associated with aging, then elderly individuals would demonstrate different hemodynamic activity and effective connectivity to perceived agency as compared with younger counterparts. Furthermore, given the fact that gray matter volume loss appears to be a linear function of age throughout adult life (Good et al., 2001), we conducted voxel-based morphometry (VBM) and examined the extent to which changes in BOLD responses for emotional empathy and agency perception would be driven by regional gray matter volume loss.
Section snippets
Participants
The study enrolled 3 groups of right-handed, ethnic Chinese participants from the community: (1) 22 young participants (11 males, aged from 20 to 35 years); (2) 22 middle-aged participants (11 males, 40–55 years); and (3) 21 older participants (11 males, 65–80 years). All participants were screened to ensure they had no history of neurologic damage or color-blindness. The older participants were further screened for medication use, recent surgical procedures, and psychiatric illness. Subjects
Behavior performance
Table 1 lists the demographic data and clinical variables. The older adults were not suffering from dementia, as indicated by higher CASI C-2.0 scores (96.5 ± 3.1) on the diagnosis of dementia (Lin et al., 2002). A 1-way analysis of variance revealed that older adults reported the lowest dispositional empathy (IRI) (p < 0.05) except on the perspective-taking subscale (p > 0.05). For the subjective ratings of unpleasantness and pain intensity, a 2-way mixed analysis of variance indicated an
Discussion
The present study examined whether aging has an impact on the neural mechanisms involved in empathy. We tackled this issue with self-reported dispositional empathy (IRI) and subjective pain ratings, and functional and structural neuroimaging data across 3 age groups. Results showed that older participants reported less dispositional empathy (except on the perspective-taking subscale), but rated unpleasantness higher for the scenarios that depicted the pain intentionally caused by another person
Conclusion
Recruiting younger, middle-aged, and older adults, this multimodal study combined subjective evaluation and structural and functional imaging to elucidate the relationship between gray matter, brain activity, and empathy associated with healthy aging. Notably, the present study adds to previous developmental findings (Decety and Michalska, 2010) in demonstrating the neurocognitive trajectories of empathy over the life span (7–80 years). The comprehensive life span approach can identify the
Disclosure statement
The authors certify that they have no actual or potential conflicts of interest regarding the research reported in this article.
Acknowledgements
This study was sponsored by National Science Council (NSC 99-2314-B-010-037-MY3; NSC 100-2628-H-010-001-MY3), National Yang-Ming University Hospital (RD2011-005; RD2012-005), and a grant from the Ministry of Education (Aim for the Top University Plan). Dr Jean Decety was supported by a grant (BCS-0718480) from the National Science Foundation.
References (85)
- et al.
Social context and perceived agency affects empathy for pain: an event-related fMRI investigation
Neuroimage
(2009) - et al.
The behavioural expression of empathy to others' pain versus others' sadness in young children
Pain
(2011) - et al.
The Faces Pain Scale for the self-assessment of the severity of pain experienced by children: development, initial validation, and preliminary investigation for ratio scale properties
Pain
(1990) - et al.
Viewing facial expressions of pain engages cortical areas involved in the direct experience of pain
Neuroimage
(2005) - et al.
A PET investigation of the attribution of intentions with a nonverbal task
Neuroimage
(2000) - et al.
Effects of aging on mindreading ability through the eyes: an fMRI study
Neuropsychologia
(2010) - et al.
Love hurts: an fRMI study
Neuroimage
(2010) - et al.
Expertise modulates the perception of pain in others
Curr. Biol.
(2007) - et al.
The power of simulation: Imagining one's own and other's behavior
Brain Research
(2006) - et al.
Who caused the pain? an fMRI investigation of empathy and intentionality in children
Neuropsychologia
(2008)
Atypical empathic responses in adolescents with aggressive conduct disorder: a functional MRI investigation
Biol. Psychol.
Imagining being the agent of actions that carry different moral consequences: an fMRI study
Neuropsychologia
Shared representations between self and others: a social cognitive neuroscience view
Trends Cogn. Sci.
Putting together phylogenetic and ontogenetic perspectives on empathy
Dev. Cogn. Neurosci.
Age norms for impulsiveness, venturesomeness and empathy in adults
Pers. Indiv. Differ
A voxel-based morphometric study of ageing in 465 normal adult human brains
Neuroimage
Age-related differences in brain activation during emotional face processing
Neurobiol. Aging
Morphometry of the human cortex cerebri and corpus striatum during aging
Neurobiol. Aging
Age-related shift in brain region activity during successful memory performance
Neurobiol. Aging
An fMRI study of the functional neuroanatomy of picture encoding in younger and older adults
Brain Res. Cogn. Brain Res.
Empathy examined through the neural mechanisms involved in imagining how I feel versus how you feel pain
Neuropsychologia
How do we perceive the pain of others? A window into the neural processes involved in empathy
Neuroimage
Cortical sites of sustained and divided attention in normal elderly humans
Neuroimage
Emotional curiosity: modulation of visuospatial attention by arousal is preserved in aging and early-stage Alzheimer's disease
Neuropsychologia
Meta-analytic evidence for common and distinct neural networks associated with directly experienced pain and empathy for pain
Neuroimage
Social reasoning, emotion and empathy in frontotemporal dementia
Neuropsychologia
Brain aging: reorganizing discoveries about the aging mind
Curr. Opin. Neurobiol.
Empathy development from 8 to 16 months: early signs of concern for others
Infant Behav. Dev.
A meta-analytic review of emotion recognition and aging: implications for neuropsychological models of aging
Neurosci. Biobehav. Rev.
Effects of aging on functional connectivity of the amygdala during negative evaluation: a network analysis of fMRI data
Neurobiol. Aging
Regional frontal cortical volumes decrease differentially in aging: an MRI study to compare volumetric approaches and voxel-based morphometry
Neuroimage
Neuronal correlates of theory of mind and empathy: a functional magnetic resonance imaging study in a nonverbal task
Neuroimage
Effects of age on volumes of cortex, white matter and subcortical structures
Neurobiol. Aging
The effects of divided attention on encoding- and retrieval-related brain activity: a PET study of younger and older adults
J. Cogn. Neurosci.
Growing less empathic with age: disinhibition of the self-perspective
J. Gerontol. B Psychol. Sci. Soc. Sci.
Empathy and social functioning in late adulthood
Aging Ment. Health
These things called empathy: eight related but distinct phenomena
Hemispheric asymmetry reduction in older adults: the HAROLD model
Psychol. Aging
Emotional experience improves with age: evidence based on over 10 years of experience sampling
Psychol. Aging
Memories of social interactions: age differences in emotional intensity
Psychol. Aging
Sensorimotor resonance is an outcome but not a platform to anticipating harm to others
Soc. Neurosci.
Mentalizing and Development during Adolescence
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Yao-Chu Chen and Cheng-Chiang Chen equally contributed to the study.