Abstract

Studies of semantic dementia, imaging, and repetitive TMS have suggested that the bilateral anterior temporal lobes (ATLs) underpin a modality-invariant representational hub within the semantic system. Questions remain, however, regarding functional specialization across a variety of knowledge domains within the ATL region. We investigated direct evidence for the functional relevance of the superior ATL in processing social concepts. Using converging evidence from noninvasive brain stimulation and neuropsychology, we demonstrate graded differentiation of right and left superior anterior temporal areas in social cognition. Whereas the left superior ATL is necessary for processing both social and nonsocial abstract concepts, social conceptual processing predominates in the right superior ATL. This graded hemispheric specialization is mirrored in the patient results. Our data shed new light on the classic debate about hemispheric differences in semantic and social cognition. These results are considered in the context of models of semantic representation and the emerging data on connectivity for left and right ATL regions.

Highlights

  • Planned t tests on the RTs were used to compare performance in right ATL (rATL) and left ATL (lATL) for social and nonsocial concepts

  • We report one-tailed p values

  • Our results are in agreement with the central role of the anterior temporal lobes (ATLs) in representing conceptual knowledge (Lambon Ralph, 2013; Patterson et al, 2007; Spitsyna, Warren, Scott, Turkheimer, & Wise, 2006; Bozeat, Lambon Ralph, Patterson, Garrard, & Hodges, 2000) and the importance of the right temporal lobe for social cognitive impairments in rATL neurodegeneration (Chan et al, 2009; Liu et al, 2004)

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Summary

Introduction

Human neuroscience needs to understand which brain regions support social behavior and how they function. Multiple lines of evidence suggest that the anterior temporal lobes (ATLs) are part of the network supporting semantic (Lambon Ralph, 2013) and social cognition (Zahn et al, 2007; Amodio & Frith, 2006; Moll, Zahn, de Oliveira-Souza, Krueger, & Grafman, 2005). The role of the ATL in semantic cognition has been supported by patient investigations (Patterson, Nestor, & Rogers, 2007; Snowden, Goulding, & Neary, 1989), neuroimaging studies (Visser, Embleton, Jefferies, Parker, & Lambon Ralph, 2010; Vandenberghe, Price, Wise, Josephs, & Frackowiak, 1996), and neurostimulation studies (Pobric, Jefferies, & Lambon Ralph, 2007, 2010; Lambon Ralph, Pobric, & Jefferies, 2009). In addition to a generalized yet selective semantic impairment, right ATL (rATL) neurodegeneration has been associated with impairments of social behavior (Chan et al, 2009), such as lack of empathy (Rankin et al, 2006), socially inappropriate behavior (Zahn et al, 2009), and theory of mind tasks (Irish, Hodges, & Piguet, 2014), with careful assessment, similar neuropsychiatric features are observed in cases with predominantly left ATL (lATL) atrophy, only less frequently (Chan et al, 2009)

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