Mapping the Multiple Graded Contributions of the Anterior Temporal Lobe Representational Hub to Abstract and Social Concepts: Evidence from Distortion-corrected fMRI.

Richard J Binney,Matthew A Lambon Ralph,Paul Hoffman

doi:10.1093/cercor/bhw260

Richard J Binney, Matthew A Lambon Ralph + Show 1 more

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https://doi.org/10.1093/cercor/bhw260

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Abstract

A growing body of recent convergent evidence indicates that the anterior temporal lobe (ATL) has connectivity-derived graded differences in semantic function: the ventrolateral region appears to be the transmodal, omni-category center-point of the hub whilst secondary contributions come from the peripheries of the hub in a manner that reflects their differential connectivity to different input/output modalities. One of the key challenges for this neurocognitive theory is how different types of concept, especially those with less reliance upon external sensory experience (such as abstract and social concepts), are coded across the graded ATL hub. We were able to answer this key question by using distortion-corrected fMRI to detect functional activations across the entire ATL region and thus to map the neural basis of social and psycholinguistically-matched abstract concepts. Both types of concept engaged a core left-hemisphere semantic network, including the ventrolateral ATL, prefrontal regions and posterior MTG. Additionally, we replicated previous findings of weaker differential activation of the superior and polar ATL for the processing of social stimuli, in addition to the stronger, omni-category activation observed in the vATL. These results are compatible with the view of the ATL as a graded transmodal substrate for the representation of coherent concepts.

Highlights

Through a process of transmodal distillation of verbal and nonverbal experience, conceptual knowledge brings meaning to objects, people and words, and is the foundation for sophisticated and flexible interaction with our environment and other agents within it
A growing body of recent convergent evidence indicates that the anterior temporal lobe (ATL) has connectivity-derived graded differences in semantic function: the ventrolateral region appears to be the transmodal, omni-category center-point of the hub whilst secondary contributions come from the peripheries of the hub in a manner that reflects their differential connectivity to different input/output modalities
A key question for our study was the following: what contribution do these ATL subregions make to the representation of different categories of knowledge? The logic of the graded ATL hub hypothesis would lead to the expectation that the “core” ventrolateral area underpins all types of concept with the additional contribution of other ATL subregions reflecting the connectivity of each area to any critical modalities of information (Hoffman et al 2015a)

Summary

Introduction

Through a process of transmodal distillation of verbal and nonverbal experience, conceptual knowledge brings meaning to objects, people and words, and is the foundation for sophisticated and flexible interaction with our environment and other agents within it. The genesis of this hypothesis was neuropsychological investigation of patients with semantic dementia (SD; a variant of frontotemporal dementia) whose ATL-centered atrophy leads to selective and gradual dissolution of conceptual knowledge, encompassing both verbal and non-verbal domains (Bozeat et al 2000; Hodges and Patterson 2007) It has been bolstered and extended by a recent accumulation of convergent evidence from functional imaging (including PET, fMRI and MEG), intracranial recording studies and transcranial magnetic stimulation studies of healthy subjects (Vandenberghe et al 1996; Marinkovic et al 2003; Pobric et al 2007; Lambon Ralph et al 2009; Binney et al 2010; Mion et al 2010; Chan et al 2011; Visser and Lambon Ralph 2011; Guo et al 2013; Abel et al 2014, 2016; Shimotake et al 2014). A key question for our study was the following: what contribution do these ATL subregions make to the representation of different categories of knowledge? The logic of the graded ATL hub hypothesis would lead to the expectation that the “core” ventrolateral area underpins all types of concept with the additional contribution of other ATL subregions reflecting the connectivity of each area to any critical modalities of information (Hoffman et al 2015a)

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