Abstract
The anterior temporal lobes (ATLs) play a key role in conceptual knowledge representation. The hub-and-spoke theory suggests that the contribution of the ATLs to semantic representation is (a) transmodal, i.e. integrating information from multiple sensorimotor and verbal modalities, and (b) pan-categorical, representing concepts from all categories. Another literature, however, suggests that this region's responses are modality- and category-selective; prominent examples include category selectivity for socially relevant concepts and face recognition. The predictions of each approach have never been directly compared. We used data from three studies to compare category-selective responses within the ATLs. Study 1 compared ATL responses to famous people versus another conceptual category (landmarks) from visual versus auditory inputs. Study 2 compared ATL responses to famous people from pictorial and written word inputs. Study 3 compared ATL responses to a different kind of socially relevant stimuli, namely abstract non-person-related words, in order to ascertain whether ATL subregions are engaged for social concepts more generally or only for person-related knowledge. Across all three studies a dominant bilateral ventral ATL cluster responded to all categories in all modalities. Anterior to this ‘pan-category’ transmodal region, a second cluster responded more weakly overall yet selectively for people, but did so equally for spoken names and faces (Study 1). A third region in the anterior superior temporal gyrus responded selectively to abstract socially relevant words (Study 3), but did not respond to concrete socially relevant words (i.e. written names; Study 2). These findings can be accommodated by the graded hub-and-spoke model of concept representation. On this view, the ventral ATL is the centre point of a bilateral ATL hub, which contributes to conceptual representation through transmodal distillation of information arising from multiple modality-specific association cortices. Partial specialization occurs across the graded ATL hub as a consequence of gradedly differential connectivity across the region.This article is part of the theme issue ‘Varieties of abstract concepts: development, use and representation in the brain’.
Highlights
The neural organization of conceptual knowledge has long been a fundamental issue in cognitive neuroscience, with much debate on the degree to which representations are segregated by modality and category.On the one hand, researchers have emphasized cortical specialization for& 2018 The Authors
This study explored the neural organization of conceptual knowledge in the anterior temporal lobes (ATLs)
Bilateral vATL cluster responded in a pan-category and transmodal manner, overlapped with peaks reported in previous semantic studies
Summary
The neural organization of conceptual knowledge (or semantic knowledge) has long been a fundamental issue in cognitive neuroscience, with much debate on the degree to which representations are segregated by modality and category. Related to the argument that the ATLs show a category effect for socially relevant concepts, a third literature proposes that the ATLs are selectively involved in face processing [56,63,64,65,66,67], perhaps in the function of linking familiar faces to stored semantic knowledge [68]. This study was designed to draw these three currently separate literatures together in order to understand the role of various ATL subregions in the representation of different kinds of social versus non-social concept. The hub-and-spoke theory holds that the ATLs form a pan-category transmodal ‘hub’ that develops coherent conceptual representations through interaction with distributed information sources [7,8,14,17,18] This theory stems from studies of semantic dementia (SD) patients who exhibit a selective yet progressive multimodal, pan-category impairment of semantic knowledge, following bilateral ATL atrophy [19 –21]. We compared activation within the ATL between abstract socially relevant words versus concrete socially relevant words (i.e. famous names from Study 2)
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