Exploring the role of the posterior middle temporal gyrus in semantic cognition: Integration of anterior temporal lobe with executive processes

James Davey,Hannah E Thompson,Glyn Hallam,Theodoros Karapanagiotidis,Charlotte Murphy,Irene De Caso,Katya Krieger-Redwood,Boris C Bernhardt,Jonathan Smallwood,Elizabeth Jefferies

doi:10.1016/j.neuroimage.2016.05.051

James Davey, Hannah E Thompson + Show 8 more

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https://doi.org/10.1016/j.neuroimage.2016.05.051

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Abstract

Making sense of the world around us depends upon selectively retrieving information relevant to our current goal or context. However, it is unclear whether selective semantic retrieval relies exclusively on general control mechanisms recruited in demanding non-semantic tasks, or instead on systems specialised for the control of meaning. One hypothesis is that the left posterior middle temporal gyrus (pMTG) is important in the controlled retrieval of semantic (not non-semantic) information; however this view remains controversial since a parallel literature links this site to event and relational semantics. In a functional neuroimaging study, we demonstrated that an area of pMTG implicated in semantic control by a recent meta-analysis was activated in a conjunction of (i) semantic association over size judgements and (ii) action over colour feature matching. Under these circumstances the same region showed functional coupling with the inferior frontal gyrus — another crucial site for semantic control. Structural and functional connectivity analyses demonstrated that this site is at the nexus of networks recruited in automatic semantic processing (the default mode network) and executively demanding tasks (the multiple-demand network). Moreover, in both task and task-free contexts, pMTG exhibited functional properties that were more similar to ventral parts of inferior frontal cortex, implicated in controlled semantic retrieval, than more dorsal inferior frontal sulcus, implicated in domain-general control. Finally, the pMTG region was functionally correlated at rest with other regions implicated in control-demanding semantic tasks, including inferior frontal gyrus and intraparietal sulcus. We suggest that pMTG may play a crucial role within a large-scale network that allows the integration of automatic retrieval in the default mode network with executively-demanding goal-oriented cognition, and that this could support our ability to understand actions and non-dominant semantic associations, allowing semantic retrieval to be ‘shaped’ to suit a task or context.

Highlights

Across our lifetime we acquire a large body of conceptual knowledge, only a subset of which is relevant for any given task or context; automatic spreading activation within semantic representations is often insufficient for efficient semantic cognition (Thompson-Schill et al, 1997; Badre et al, 2005; Jefferies, 2013)
The field of semantic cognition is converging on a component process account, involving conceptual representations plus control mechanisms which can shape the pattern of retrieval to suit the task or context, the brain mechanisms that underpin this capacity remain poorly understood
Our analysis suggests that posterior middle temporal gyrus (pMTG) is a functional nexus drawing together two well-documented large-scale networks implicated in automatic semantic processing and executive control, and allowing more controlled patterns of retrieval

Summary

Introduction

Across our lifetime we acquire a large body of conceptual knowledge, only a subset of which is relevant for any given task or context; automatic spreading activation within semantic representations is often insufficient for efficient semantic cognition (Thompson-Schill et al, 1997; Badre et al, 2005; Jefferies, 2013). To recover weak associations (carrot-horse) and to match words on the basis of specific sensory-motor features, such as actions or colour (e.g., carrot with traffic cone), since the functional characteristics of these concepts are more central to their meaning (Thompson-Schill et al, 1997; Badre et al, 2005; Whitney et al, 2011; Noonan et al, 2013; Davey et al, 2015a). Analyses of interregional signal correlations during task free (i.e. resting-state) functional scans have shown that ATL is part of a large scale assembly that includes medial prefrontal and posterior cingulate cortices, commonly referred to as the default mode network (DMN, Raichle et al, 2001; Buckner et al, 2008; Yeo et al, 2011; Jackson et al, 2016)

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