Distinct neural substrates of receptive and responsive aspects of empathy in patients with neurodegenerative disease

Abstract

AbstractBackgroundThe way we interact with each other is influenced by how we perceive and evaluate socioemotional signals and adapt our interpersonal behavior to them (Lieberman, 2007). In this study, we investigated the neurostructural substrates of two key aspects of interpersonal behavior: socioemotional sensitivity and behavioral self‐management, using a neurodegenerative disease lesion model.MethodSocioemotional sensitivity and behavioral self‐management were measured by obtaining informant reports from two subscales of the Revised Self‐Monitoring Scale (RSMS)(Lennox & Wolfe, 1984). Scores were correlated with structural volume using voxel‐based morphometry. The study enrolled 360 participants, including 251 patients diagnosed with one of five neurodegenerative disease syndromes causing diverse structural brain changes (77 behavioral variant frontotemporal dementia, 30 semantic variant primary progressive aphasia, 33 non‐fluent variant primary progressive aphasia, 57 progressive supranuclear palsy, and 54 Alzheimer’s disease) and 109 neurologically healthy older controls.ResultSensitivity to others’ social cues was significantly predicted by volume in predominantly right‐hemispheric paralimbic ventro‐anterior‐ and mesio‐temporal regions, some of which are known to support auditory and visual social signal reading, while the remaining regions were part of the frontotemporal semantic appraisal network (Yeo, et al., 2011), involved in making social evaluations. In contrast, capacity to make behavioral adjustments in response to social cues was uniquely predicted by volume in predominantly right‐hemispheric neocortical frontal regions that comprise the cingulo‐opercular stable task control network (Dosenbach, et al., 2007), involved in maintaining attention during socioemotional tasks.ConclusionOur results clarify how receptive and responsive aspects of empathy rely on distinct, predominantly right‐hemispheric anterior fronto‐temporal brain regions, largely comprising two intrinsically connected networks including the semantic appraisal and cingulo‐opercular task control networks, along with right temporal structures mediating person perception. The fidelity with which this questionnaire method revealed these specific brain networks shows that standardized informant reports are valuable tools in assessing the complex socioemotional constructs involved in empathy. Lastly, the specificity of these brain‐behavior correlations provides further evidence that observable, measurable patterns of decreased empathy in patients with brain disorders can be a direct result of differently localized brain lesions.