Network Modeling for Functional Magnetic Resonance Imaging (fMRI) Signals during Ultra-Fast Speech Comprehension in Late-Blind Listeners.

Susanne Dietrich,Hermann Ackermann,Ingo Hertrich,Virginie Van Wassenhove

doi:10.1371/journal.pone.0132196

Susanne Dietrich, Hermann Ackermann + Show 2 more

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https://doi.org/10.1371/journal.pone.0132196

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Abstract

In many functional magnetic resonance imaging (fMRI) studies blind humans were found to show cross-modal reorganization engaging the visual system in non-visual tasks. For example, blind people can manage to understand (synthetic) spoken language at very high speaking rates up to ca. 20 syllables/s (syl/s). FMRI data showed that hemodynamic activation within right-hemispheric primary visual cortex (V1), bilateral pulvinar (Pv), and left-hemispheric supplementary motor area (pre-SMA) covaried with their capability of ultra-fast speech (16 syllables/s) comprehension. It has been suggested that right V1 plays an important role with respect to the perception of ultra-fast speech features, particularly the detection of syllable onsets. Furthermore, left pre-SMA seems to be an interface between these syllabic representations and the frontal speech processing and working memory network. So far, little is known about the networks linking V1 to Pv, auditory cortex (A1), and (mesio-) frontal areas. Dynamic causal modeling (DCM) was applied to investigate (i) the input structure from A1 and Pv toward right V1 and (ii) output from right V1 and A1 to left pre-SMA. As concerns the input Pv was significantly connected to V1, in addition to A1, in blind participants, but not in sighted controls. Regarding the output V1 was significantly connected to pre-SMA in blind individuals, and the strength of V1-SMA connectivity correlated with the performance of ultra-fast speech comprehension. By contrast, in sighted controls, not understanding ultra-fast speech, pre-SMA did neither receive input from A1 nor V1. Taken together, right V1 might facilitate the “parsing” of the ultra-fast speech stream in blind subjects by receiving subcortical auditory input via the Pv (= secondary visual pathway) and transmitting this information toward contralateral pre-SMA.

Highlights

Vision loss may allow for cross-modal reorganization processes within the visual system in association with distinct perceptual exigencies
A previous functional magnetic resonance imaging investigation [10] found in a late-blind subject group that hemodynamic activity in right-hemispheric primary visual cortex (V1), bilateral pulvinar (Pv), and the anterior part of the left-hemispheric supplementary motor area–in addition to the “classical” perisylvian language zones–covaried with the capabilities of ultra-fast speech (16 syl/s) comprehension
Based upon functional magnetic resonance imaging (fMRI) studies [10,11,12,13] as well as investigations using magnetencephalography (MEG) [14], it has been suggested that righthemispheric V1 plays an important role with respect to the (i) perception of ultra-fast speech features, i.e. syllable onsets, and (ii) forwarding of syllabic information via left-hemispheric part of the left-hemispheric supplementary motor area (pre-SMA) to the speech processing structures, i.e. inferior frontal gyrus

Summary

Introduction

Vision loss may allow for cross-modal reorganization processes within the visual system in association with distinct perceptual exigencies. A previous functional magnetic resonance imaging (fMRI) investigation [10] found in a late-blind subject group that hemodynamic activity in right-hemispheric primary visual cortex (V1), bilateral pulvinar (Pv), and the anterior part of the left-hemispheric supplementary motor area (pre-SMA)–in addition to the “classical” perisylvian language zones (left-hemispheric inferior frontal gyrus, bilateral superior/middle temporal gyrus/sulcus)–covaried with the capabilities of ultra-fast speech (16 syl/s) comprehension. Pv has been assumed to synchronize–driven by acoustic input–striate cortex with the central-auditory system during ultra-fast speech perception [10, 12], based upon cross-modal subcortical pathways that in sighted individuals subserve audiovisual coincidence detection [15] and the control of visual attention [16]

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