Abstract

In the healthy human brain, the processing of language is strongly lateralised, usually to the left hemisphere, while the processing of complex non-linguistic sounds recruits brain regions bilaterally. Here we asked whether the anterior temporal lobes, strongly implicated in semantic processing, are critical to this special treatment of spoken words. Nine patients with semantic dementia (SD) and fourteen age-matched controls underwent magnetoencephalography and structural MRI. Voxel based morphometry demonstrated the stereotypical pattern of SD: severe grey matter loss restricted to the anterior temporal lobes, with the left side more affected. During magnetoencephalography, participants listened to word sets in which identity and meaning were ambiguous until word completion, for example PLAYED versus PLATE. Whereas left-hemispheric responses were similar across groups, patients demonstrated increased right hemisphere activity 174–294 msec after stimulus disambiguation. Source reconstructions confirmed recruitment of right-sided analogues of language regions in SD: atrophy of anterior temporal lobes was associated with increased activity in right temporal pole, middle temporal gyrus, inferior frontal gyrus and supramarginal gyrus. Overall, the results indicate that anterior temporal lobes are necessary for normal and efficient lateralised processing of word identity by the language network.

Highlights

  • The neural processing of spoken words is strongly lateralised to the dominant cerebral hemisphere, usually the left, while the processing of complex non-linguistic sounds recruits brain regions bilaterally (Shtyrov, Kujala, Palva, Ilmoniemi, & Na€a€ta€nen, 2000; Tervaniemi & Hugdahl, 2003; Zatorre et al, 1992, 2002)

  • Across a range of primate species, acoustic information entering primary auditory cortex is rapidly transferred along reciprocal connections to the anterior temporal lobe (ATL) (Friederici, 2012; Hackett, 2011), a region that is strongly implicated in the representation and processing of semantic information in the human brain (Binder et al, 2011; Binney, Embleton, Jefferies, Parker, & Lambon Ralph, 2010; Guo et al, 2013; Lambon Ralph, Jefferies, Patterson, & Rogers, 2017; Mion et al, 2010; Mummery et al, 2000; Pobric, Jefferies, & Lambon Ralph, 2007; Visser, Jefferies, & Lambon Ralph, 2010)

  • Frequentist, inference from statistical parametric mapping, voxel based morphometry (Fig. 2) demonstrated the expected pattern of semantic dementia (SD), with predominant grey matter loss compared to the control group in the left ATL [peak (e29 1e40) t(18) 1⁄4 13.34 FWE p < .001], with more posterior temporal regions affected to a lesser degree

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Summary

Introduction

The neural processing of spoken words is strongly lateralised to the dominant cerebral hemisphere, usually the left, while the processing of complex non-linguistic sounds recruits brain regions bilaterally (Shtyrov, Kujala, Palva, Ilmoniemi, & Na€a€ta€nen, 2000; Tervaniemi & Hugdahl, 2003; Zatorre et al, 1992, 2002). We employed a spoken-word version of the auditory mismatch paradigm (for a review see Na€a€ta€nen, Paavilainen, Rinne, & Alho, 2007), in which repeated ‘standard’ words (for example PLAY) were changed in either grammatical category (tense) or semantic meaning by the spliced addition of the additional endings d/t (to become, in this case, PLAYED or PLATE) This paradigm is a sensitive tool for measuring automatic lexico-semantic processing of spoken words in the brain (Pulvermuller, Shtyrov, Ilmoniemi, & Marslen-Wilson, 2006; Shtyrov, Kujala, & Pulvermuller, 2010) and has a special benefit for patient studies as it does not require any active stimulus processing, or even attention on the auditory stream (Gansonre, Højlund, Leminen, Bailey, & Shtyrov, 2018). This allowed us to examine the processing, not just of words in general, but of those aspects of word processing that are to do with semantic identity and meaning

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