Elsevier

Neurobiology of Aging

Volume 35, Issue 4, April 2014, Pages 827-836
Neurobiology of Aging

Regular article
Aging is associated with changes in the neural circuits underlying empathy

https://doi.org/10.1016/j.neurobiolaging.2013.10.080Get rights and content

Abstract

Although the neurodevelopment of empathy from childhood to adolescence has been documented, no study has yet examined it across a life span aging perspective. Sixty-five healthy participants from 3 age groups (young, middle-aged, old) underwent functional magnetic resonance imaging while presented with visual stimuli depicting body parts being injured, either accidentally by oneself or intentionally by another, thus isolating pain and agency as 2 variables of interest. Older adults reported less dispositional emotional empathy as assessed by the interpersonal reactivity index, and their unpleasantness ratings were more sensitive to intentional harm. The response in anterior insula and anterior mid-cingulate cortex to others' pain, indicative of emotional empathy, showed an age-related decline, whereas the response in medial prefrontal cortex and posterior superior temporal sulcus to perceived agency did not change with age. Dynamic causal modeling demonstrated that their effective connectivity remained stable. The pattern of hemodynamic response was not related to regional gray matter volume loss. These findings suggest that the neural response associated with emotional empathy lessened with age, whereas the response to perceived agency is preserved.

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.

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    Yao-Chu Chen and Cheng-Chiang Chen equally contributed to the study.

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