How right hemisphere damage after stroke can impair speech comprehension.

Andrea Gajardo-Vidal,Jennifer T Crinion,Susan Prejawa,Cathy J Price,Alex P Leff,Diego L Lorca-Puls,Oiwi Parker Jones,David W Green,Thomas M H Hope,Mohamed L Seghier

doi:10.1093/brain/awy270

Abstract

Acquired language disorders after stroke are strongly associated with left hemisphere damage. When language difficulties are observed in the context of right hemisphere strokes, patients are usually considered to have atypical functional anatomy. By systematically integrating behavioural and lesion data from brain damaged patients with functional MRI data from neurologically normal participants, we investigated when and why right hemisphere strokes cause language disorders. Experiment 1 studied right-handed patients with unilateral strokes that damaged the right (n = 109) or left (n = 369) hemispheres. The most frequently impaired language task was: auditory sentence-to-picture matching after right hemisphere strokes; and spoken picture description after left hemisphere strokes. For those with auditory sentence-to-picture matching impairments after right hemisphere strokes, the majority (n = 9) had normal performance on tests of perceptual (visual or auditory) and linguistic (semantic, phonological or syntactic) processing. Experiment 2 found that these nine patients had significantly more damage to dorsal parts of the superior longitudinal fasciculus and the right inferior frontal sulcus compared to 75 other patients who also had right hemisphere strokes but were not impaired on the auditory sentence-to-picture matching task. Damage to these right hemisphere regions caused long-term speech comprehension difficulties in 67% of patients. Experiments 3 and 4 used functional MRI in two groups of 25 neurologically normal individuals to show that within the regions identified by Experiment 2, the right inferior frontal sulcus was normally activated by (i) auditory sentence-to-picture matching; and (ii) one-back matching when the demands on linguistic and non-linguistic working memory were high. Together, these experiments demonstrate that the right inferior frontal cortex contributes to linguistic and non-linguistic working memory capacity (executive function) that is needed for normal speech comprehension. Our results link previously unrelated literatures on the role of the right inferior frontal cortex in executive processing and the role of executive processing in sentence comprehension; which in turn helps to explain why right inferior frontal activity has previously been reported to increase during recovery of language function after left hemisphere stroke. The clinical relevance of our findings is that the detrimental effect of right hemisphere strokes on language is (i) much greater than expected; (ii) frequently observed after damage to the right inferior frontal sulcus; (iii) task dependent; (iv) different to the type of impairments observed after left hemisphere strokes; and (v) can result in long-lasting deficits that are (vi) not the consequence of atypical language lateralization.

Highlights

To investigate the processing level that was affected in the 12 patients with right hemisphere damage and impaired scores on the auditory sentence-to-picture matching task, we considered how these patients performed on other language tasks
In Experiment 2, we found that the right hemisphere regions that were most frequently damaged in patients with impaired auditory sentence-to-picture matching included dorsal parts of the superior longitudinal fasciculus impinging on the right inferior frontal sulcus, and more ventral subcortical regions in the vicinity of the right putamen, thalamus and caudate
Our study shows that damage to the right inferior frontal cortex and right mediodorsal thalamus can impair sentence comprehension, and this is likely to be the consequence of disruption to a right hemisphere system that is involved in normal language processing

Summary

Introduction

Despite a long history of research favouring the view that the left hemisphere is dominant for language processing in most right-handed subjects, there is accumulating evidence that the right hemisphere contributes to (i) language function in neurologicallynormal individuals (Hartwigsen et al, 2010a; Hartwigsen et al, 2010b; Sollmann et al, 2014) and (ii) language recovery after (a) left-hemisphere brain damage (Crinion and Price, 2005; Thiel et al, 2006; Forkel et al, 2014; Xing et al, 2016; Nardo et al, 2017) or (b) disruption of left-hemisphere processing (Hartwigsen et al, 2013; Jung and Lambon Ralph, 2016). The hypothesis that right hemisphere executive processing is necessary for normal language function contrasts with the dominant view that when language impairments are observed in right-handed patients with unilateral right hemisphere damage, they necessarily imply atypical language lateralisation prior to the stroke (Marien et al, 2004). The executive processing hypothesis is consistent with other literature that has associated right hemisphere activation with selective attention (Corbetta et al, 2005; Hillis et al, 2005; Bartolomeo et al, 2012), imagery and domain general inhibitory control mechanisms (Aron et al, 2004, 2014; Neef et al, 2018) and working memory (Jonides et al, 1993; Ravizza et al, 2005)

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