Revealing the Dynamic Modulations That Underpin a Resilient Neural Network for Semantic Cognition: An fMRI Investigation in Patients With Anterior Temporal Lobe Resection.

Grace E Rice,Paul Hoffman,Matthew A Lambon Ralph,Perry Moore,Helen Caswell

doi:10.1093/cercor/bhy116

Abstract

One critical feature of any well-engineered system is its resilience to perturbation and minor damage. The purpose of the current study was to investigate how resilience is achieved in higher cognitive systems, which we explored through the domain of semantic cognition. Convergent evidence implicates the bilateral anterior temporal lobes (ATLs) as a conceptual knowledge hub. While bilateral damage to this region produces profound semantic impairment, unilateral atrophy/resection or transient perturbation has a limited effect. Two neural mechanisms might underpin this resilience to unilateral ATL damage: 1) the undamaged ATL upregulates its activation in order to compensate; and/or 2) prefrontal regions involved in control of semantic retrieval upregulate to compensate for the impoverished semantic representations that follow from ATL damage. To test these possibilities, 34 postsurgical temporal lobe epilepsy patients and 20 age-matched controls were scanned whilst completing semantic tasks. Pictorial tasks, which produced bilateral frontal and temporal activation, showed few activation differences between patients and control participants. Written word tasks, however, produced a left-lateralized activation pattern and greater differences between the groups. Patients with right ATL resection increased activation in left inferior frontal gyrus (IFG). Patients with left ATL resection upregulated both the right ATL and right IFG. Consistent with recent computational models, these results indicate that 1) written word semantic processing in patients with ATL resection is supported by upregulation of semantic knowledge and control regions, principally in the undamaged hemisphere, and 2) pictorial semantic processing is less affected, presumably because it draws on a more bilateral network.

Highlights

One critical feature of any well-engineered system is its resilience to perturbation and minor damage
Two neural mechanisms might underpin this resilience to unilateral ATL damage: 1) the undamaged ATL upregulates its activation in order to compensate; and/or 2) prefrontal regions involved in control of semantic retrieval upregulate to compensate for the impoverished semantic representations that follow from ATL damage
Patients with unilateral anterior temporal lobe (ATL) resection exhibit short-term memory problems and relatively mild semantic memory impairments (Wilkins and Moscovitch 1978; Alpherts et al 2006; Lambon Ralph et al 2012; Willment and Golby 2013; Sidhu et al 2015). This mild semantic impairment is shown through slower response times on semantic tasks, rather than marked decreases in accuracy (Wilkins and Moscovitch 1978; Lambon Ralph et al 2012; Rice et al 2018), on more challenging/specific level semantic concepts decreases in accuracy performance are found

Summary

Introduction

One critical feature of any well-engineered system is its resilience to perturbation and minor damage. Patients with unilateral anterior temporal lobe (ATL) resection exhibit short-term memory problems and relatively mild semantic memory impairments (Wilkins and Moscovitch 1978; Alpherts et al 2006; Lambon Ralph et al 2012; Willment and Golby 2013; Sidhu et al 2015) This mild semantic impairment is shown through slower response times on semantic tasks (e.g., picture naming, word-picture matching, synonym judgment), rather than marked decreases in accuracy (Wilkins and Moscovitch 1978; Lambon Ralph et al 2012; Rice et al 2018), on more challenging/specific level semantic concepts decreases in accuracy performance are found. Two nonexclusive and potentially related explanations for the robustness of the semantic system are: 1) after unilateral resection the remaining contralateral ATL changes its activation in order to compensate; and/or 2) performance on semantic tasks is maintained through changes in the activation in other regions of the semantic network

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