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

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.

Dynamics of functional networks for syllable and word-level processing

“…with previous research, lexical processing activated left supramarginal gyrus, fronto-central and middle temporal brain areas, which have been argued to support lexical-semantic processing of words (Fig 2A, 3A) (46,54,32,47,51). 'Mere' syllable transition processing, in contrast, activated fronto-centro-temporal brain areas in both hemispheres ( Fig 2B, 3B).…”

“…That being said, the posterior MTG (perhaps left lateralized (44)) has been suggested to provide a sound-to-meaning interface for the mapping of phonological representations in STS to lexical representations (45,46,44,47,48). Lexical-semantic compositional processing as well as sentence level processing additionally has been shown to activate the anterior temporal lobe (ATL) (49)(50)(51). Sublexical contingencies, such as syllable transitions, contribute to word processing, and have been shown to activate parts of the STS (52,53) and a dorsal-path network (54).…”

The neural bases of resilient cognitive systems: Evidence of variable neuro-displacement in the semantic system

“…In summary, we found that semantically-demanding conditions upregulated the left-lateralized semantic regions including the vATL, IFG and pMTG as well as other regions in domain general networks. More specifically, there was increased activation in the bilateral ATL supporting the notion that semantic representation is inherently bilateral in nature (1,31,42). Functional connectivity between these regions (interhemispheric vATL connectivity and the vATL-PFC) was also increased.…”

“…We manipulated task difficulty in two different ways: stimulus manipulation (SM) and response time manipulation (RM) (Fig.1). The RM data have been reported in a recent examination of the semantic network in patients with ATL resection (31).…”

“…The bilateral nature of ATL-reliant semantic representation could, itself be crucial for its resilient, well-engineered characteristics. Past studies of healthy participants after ATL rTMS, patients with resection for temporal lobe epilepsy, and comparative neurosurgical investigations have shown that bilateral lesions are required for substantial, chronic semantic impairments (i.e., breaking the resilience of the system) and that after unilateral stimulation or resection, there are compensatory upregulations of activation in contralateral regions, peri-damage areas and increased positive transcallosal functional connectivity (18,19,21,31,43). The resilience that follows from bilateral neural systems has also been formally demonstrated and explored through implemented neurocomputational models of bilateral semantic representation.…”