Altered effective connectivity and anomalous anatomy in the basal ganglia-thalamocortical circuit of stuttering speakers

Chunming Lu,Danling Peng,Chuansheng Chen,Ning Ning,Guosheng Ding,Kuncheng Li,Yanhui Yang,Chunlan Lin

doi:10.1016/j.cortex.2009.02.017

Abstract

Combining structural equation modeling (SEM) and voxel-based morphometry (VBM), this study investigated the interactions among neural structures in the basal ganglia-thalamocortical circuit (BGTC) in the left hemisphere of stuttering and non-stuttering speakers. Stuttering speakers ( n = 12) and non-stuttering controls ( n = 12) were scanned while performing a picture-naming task and a passive-viewing (baseline) task. Results showed significant differences between stuttering and non-stuttering speakers in both effective connectivity and anatomical structures in the BGTC in the left brain. Specifically, compared to non-stuttering speakers, stuttering speakers showed weaker negative connectivity from the left posterior middle temporal gyrus (PMTG) to the putamen, but stronger positive connectivity from the putamen to the thalamus, from the thalamus to the PMTG and anterior supplementary motor area (preSMA), and from the anterior superior temporal gyrus (ASTG) to the preSMA. Accompanying such altered connectivity were anatomical differences: compared to non-stuttering controls, stuttering speakers showed more grey matter (GM) volume concentration in the left putamen, less GM volume concentration in the left medial frontal gyrus and ASTG, and less white matter volume concentration underlying the left posterior superior temporal gyrus inside the BGTC. These results shed significant light on the neural mechanisms (in terms of both functional connectivity and neural anatomy) of stuttering.

Highlights

Stuttered speech is characterized by frequent repetition or prolongation of sounds or syllables or words, or frequent hesitations or pauses
Of greater relevance to our structural equation modeling (SEM) model, the present study revealed that the anterior superior temporal gyrus (ASTG) (BA21) showed a significant decrease of grey matter (GM) volume concentration whereas the left posterior superior temporal gyrus (BA41) showed a decrease of white matter (WM) volume concentration among the stuttering speakers
By employing the multivariate technique of SEM, the present study revealed significant differences in effective connectivity among the nodes of the basal ganglia-thalamocortical circuit (BGTC) between stuttering speakers and non-stuttering controls

Summary

Introduction

Stuttered speech is characterized by frequent repetition or prolongation of sounds or syllables or words, or frequent hesitations or pauses. More recent positron emission tomography (PET) and functional magnetic resonance imaging (fMRI) studies have further confirmed these results (e.g., De Nil et al, 2003; Fox et al, 1996, 2000; Neumann et al, 2003; Preibisch et al, 2003; Wu et al, 1995) These results may lead one to believe that the right hemisphere is related to stuttering, a now-classic study by Braun et al (1997) revealed that activation in the right hemisphere was related to fluent speech among stuttering speakers, whereas activation in the left hemisphere was related to the production of stuttered speech. In their 1914 book, Everbusch et al discussed the brain and aphasia and wrote ‘‘the right hemisphere vicariates for the left in childhood’’ (Everbusch et al, 1914, p. 461)

Results

Discussion

Conclusion