Uncovering the functional anatomy of the human insula during speech.

Oscar Woolnough,Patrick Sarahan Rollo,Kiefer James Forseth,Nitin Tandon

doi:10.7554/elife.53086

Oscar Woolnough, Patrick Sarahan Rollo + Show 2 more

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https://doi.org/10.7554/elife.53086

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Abstract

The contribution of insular cortex to speech production remains unclear and controversial given diverse findings from functional neuroimaging and lesional data. To create a precise spatiotemporal map of insular activity, we performed a series of experiments: single-word articulations of varying complexity, non-speech orofacial movements and speech listening, in a cohort of 27 patients implanted with penetrating intracranial electrodes. The posterior insula was robustly active bilaterally, but after the onset of articulation, during listening to speech and during production of non-speech mouth movements. Preceding articulation there was very sparse activity, localized primarily to the frontal operculum rather than the insula. Posterior insular was active coincident with superior temporal gyrus but was more active for self-generated speech than external speech, the opposite of the superior temporal gyrus. These findings support the conclusion that the insula does not serve pre-articulatory preparatory roles.

Highlights

Multiple lesion studies have linked insular damage to speech and orofacial motor control disorders such as apraxia of speech (AOS) (Dronkers, 1996; Marien et al, 2001; Ogar et al, 2006; Itabashi et al, 2016), dysarthria (Baier et al, 2011) and dysphagia (Daniels et al, 1996)
Participants read visually presented words aloud (n = 27), performed an object naming task (n = 23) of common objects presented as line drawings, listened to speech stimuli as a part of a naming to description task (n = 21) and performed an orofacial praxis task (n = 8), where they silently performed non-speech mouth movements (Figure 1A)
The response time (RT) for the object naming task was 1192 ± 245 ms. 75.1 ± 10.6% of responses in the naming task had both correct articulation and the expected, most common word choice; only these were used for subsequent analysis

Summary

Introduction

Multiple lesion studies have linked insular damage to speech and orofacial motor control disorders such as apraxia of speech (AOS) (Dronkers, 1996; Marien et al, 2001; Ogar et al, 2006; Itabashi et al, 2016), dysarthria (Baier et al, 2011) and dysphagia (Daniels et al, 1996). Dronkers’ study was the first to quantitatively link anterior insular damage to a disruption in speech production, finding a 100% lesion overlap in the left superior precentral gyrus of the insula (SPG) in AOS patients. Lesion symptom mapping revealed that patients with SPG lesions produced a greater number of speech errors during complex, multisyllabic articulations (Ogar et al, 2006; Baldo et al, 2011). This implicated the insula in pre-articulatory motor plans specific to speech. In the dual-stream model of the speech articulation network, the anterior insula is included as part of the putative dorsal sensorimotor pathway (Hickok and Poeppel, 2007)

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