Neural substrates of socioemotional self‐awareness in neurodegenerative disease

Abstract

BackgroundNeuroimaging studies examining neural substrates of impaired self-awareness in patients with neurodegenerative diseases have shown divergent results depending on the modality (cognitive, emotional, behavioral) of awareness. Evidence is accumulating to suggest that self-awareness arises from a combination of modality-specific and large-scale supramodal neural networks.MethodsWe investigated the structural substrates of patients' tendency to overestimate or underestimate their own capacity to demonstrate empathic concern for others. Subjects' level of empathic concern was measured using the Interpersonal Reactivity Index, and subject-informant discrepancy scores were used to predict regional atrophy pattern, using voxel-based morphometry analysis. Of the 102 subjects, 83 were patients with neurodegenerative diseases such as behavioral variant frontotemporal dementia (bvFTD) or semantic variant primary progressive aphasia (svPPA); the other 19 were healthy older adults.ResultsbvFTD and svPPA patients typically overestimated their level of empathic concern compared to controls, and overestimating one's empathic concern predicted damage to predominantly right-hemispheric anterior infero-lateral temporal regions, whereas underestimating one's empathic concern showed no neuroanatomical basis.ConclusionsThese findings suggest that overestimation and underestimation of one's capacity for empathic concern cannot be interpreted as varying degrees of the same phenomenon, but may arise from different pathophysiological processes. Damage to anterior infero-lateral temporal regions has been associated with semantic self-knowledge, emotion processing, and social perspective taking; neuropsychological functions partly associated with empathic concern itself. These findings support the hypothesis that—at least in the socioemotional domain—neural substrates of self-awareness are partly modality-specific.

Characterizing Sexual Behavior in Frontotemporal Dementia

“…Alterations in empathy were significantly associated with lack of affection and decreased frequency of sexual relations in patients. Accordingly, damage to frontoinsular and anterior infero-lateral temporal cortices, typically observed in FTD syndromes, likely disrupts a core capacity to empathize and respond to the affection of others [42,43]. From a neuroendocrine perspective, oxytocin is known to be an important mediator of social behavior and emotional recognition, and an improvement in behavior in bvFTD patients has been suggested with administration of oxytocin [44].…”

Self-awareness in neurodegenerative disease relies on neural structures mediating reward-driven attention

“…This group showed a selective impairment in awareness for interpersonal abilities, the functional domain where they show the most profound decline. Impaired awareness for behavioural deficits has been previously associated with right temporal atrophy (Zamboni and Wilcock, 2011;Sollberger et al, 2014). A proposed mechanism for this finding was that impaired empathy and understanding of others' minds, frequently associated with right temporal atrophy, affects the ability to understand others' reactions to one's inappropriate behaviour, and to update one's self-knowledge accordingly (Zamboni et al, 2010).…”

The behavioural variant frontotemporal dementia (bvFTD) syndrome in psychiatry

“…Such lack of empathy/sympathy in bvFTD is also predominately a right-sided manifestation of the disease including the right ATL, as well as the right medial orbitofrontal cortex (OFC) and anterior insula. [16][17][18][19] Disinhibition is perhaps the most striking feature of bvFTD. The OFC may be conceptualised as a 'relay station' between higher order frontal cortices that inhibit a more 'primitive' (ie, reward-driven) limbic cortex; therefore, the OFC plays a critical role in modifying behaviour according to perceived reward and punishment values.…”