Structural anatomy of empathy in neurodegenerative disease

Abstract

Empathy is a complex social behaviour mediated by a network of brain structures. Recently, several functional imaging studies have investigated the neural basis of empathy, but few corroborative human lesion studies exist. Severe empathy loss is a common feature of frontotemporal lobar degeneration (FTLD), and is also seen in other neurodegenerative diseases. In this study, the neuroanatomic basis of empathy was investigated in 123 patients with FTLD, Alzheimer's disease, corticobasal degeneration and progressive supranuclear palsy using the Interpersonal Reactivity Index (IRI). IRI Empathic Concern and Perspective taking scores were correlated with structural MRI brain volume using voxel-based morphometry. Voxels in the right temporal pole, the right fusiform gyrus, the right caudate and right subcallosal gyrus correlated significantly with total empathy score (P < 0.05 after whole-brain correction for multiple comparisons). Empathy score correlated positively with the volume of right temporal structures in semantic dementia, and with subcallosal gyrus volume in frontotemporal dementia. These findings are consistent with previous research suggesting that a primarily right frontotemporal network of brain regions is involved in emotion processing, and highlights the roles of the right temporal pole and inferior frontal/striatal regions in regulating complex social interactions. This is the first large-scale lesion study to investigate the neural basis of empathy using correlational analytic methods. The results suggest that the right anterior temporal and medial frontal regions are essential for real-life empathic behaviour.

Social Cognition, Executive Functioning, and Neuroimaging Correlates of Empathic Deficits in Frontotemporal Dementia

“…In the only other study to date examining anatomical correlates of empathy changes in bvFTD, a combined empathy score was related to structural integrity of the right subcallosal gyrus, with scores from a larger, mixed neurodegenerative disease group associating empathy with atrophy in right frontal-temporal regions, particularly the temporal pole, subcallosal gyrus, and caudate and fusiform gyrus. 26 Our results suggested distinct differences between anatomical correlates for empathic perspective-taking and empathic emotional concern, although both showed strong frontal-lobe correlations. These cognitive and emotional empathic changes in our bvFTD sample are consistent with extensive literature based on clinical lesion analysis, functional brain imaging, and connectional anatomy in nonhuman primates, indicating that the prefrontal regions are involved in cognitive and emotional processing, and, quite likely, complex integration of cognition and emotion.…”

“…14 Such changes were not evident in the caregiver ratings for the PNFA and SD samples, supporting the specificity of the results for the consensus diagnosis of bvFTD disorders and presumed frontal-limbic involvement. The lack of observed empathic changes in SD patients, as seen by Rankin et al, 26 may be related in part to an ascertainment bias. That is, patients referred to our center may have comparatively less prominent social features than patients referred to the center where Rankin et al completed their study.…”

“…These results parallel the findings of previous work. 9,26 The lack of empathy in bvFTD is extraordinarily disturbing to caregivers. 14 Such changes were not evident in the caregiver ratings for the PNFA and SD samples, supporting the specificity of the results for the consensus diagnosis of bvFTD disorders and presumed frontal-limbic involvement.…”

“…A second, larger sampling of caregivers reported both cognitive and emotional empathic changes in FTD patients with frontal-related behavioral changes and with features of semantic dementia (SD), although changes were not detected in patients with progressive nonfluent aphasia (PNFA). 26 When caregivers rated empathic behaviors pre- versus post-disease onset in a sample of frontal-variant FTD patients, significant decline was detected in both cognitive and emotional empathy. 9 Hence, we hypothesized that analysis of a standardized behavioral inventory would confirm significant cognitive and emotional empathic deficits in a bvFTD sample, although we were uncertain about empathic changes in an FTD aphasic sample (SD and PNFA), since we have not observed such changes in previous research or in clinical care.…”

“…27,28 Rankin et al 26 directly related empathy and cortical atrophy in a large group of patients with various neurodegenerative conditions. They reported an association of overall empathy score with atrophy in the right temporal pole, right fusiform gyrus, and the right medial frontal region.…”