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Brain Advance Access published online on October 10, 2007

Brain, doi:10.1093/brain/awm241
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© The Author (2007). Published by Oxford University Press on behalf of the Guarantors of Brain. All rights reserved. For Permissions, please email: journals.permissions@oxfordjournals.org

Structural and functional abnormalities of the motor system in developmental stuttering

Kate E. Watkins1,2, Stephen M. Smith2, Steve Davis3 and Peter Howell3

1Department of Experimental Psychology, University of Oxford, 2FMRIB Centre, Department of Clinical Neurology, University of Oxford and 3Department of Psychology, University College London, UK

Correspondence to: Kate Watkins, Department of Experimental Psychology, University of Oxford, South Parks Road, Oxford OX1 3UD, UK E-mail: kate.watkins{at}psy.ox.ac.uk

Though stuttering is manifest in its motor characteristics, the cause of stuttering may not relate purely to impairments in the motor system as stuttering frequency is increased by linguistic factors, such as syntactic complexity and length of utterance, and decreased by changes in perception, such as masking or altering auditory feedback. Using functional and diffusion imaging, we examined brain structure and function in the motor and language areas in a group of young people who stutter. During speech production, irrespective of fluency or auditory feedback, the people who stuttered showed overactivity relative to controls in the anterior insula, cerebellum and midbrain bilaterally and underactivity in the ventral premotor, Rolandic opercular and sensorimotor cortex bilaterally and Heschl's gyrus on the left. These results are consistent with a recent meta-analysis of functional imaging studies in developmental stuttering. Two additional findings emerged from our study. First, we found overactivity in the midbrain, which was at the level of the substantia nigra and extended to the pedunculopontine nucleus, red nucleus and subthalamic nucleus. This overactivity is consistent with suggestions in previous studies of abnormal function of the basal ganglia or excessive dopamine in people who stutter. Second, we found underactivity of the cortical motor and premotor areas associated with articulation and speech production. Analysis of the diffusion data revealed that the integrity of the white matter underlying the underactive areas in ventral premotor cortex was reduced in people who stutter. The white matter tracts in this area via connections with posterior superior temporal and inferior parietal cortex provide a substrate for the integration of articulatory planning and sensory feedback, and via connections with primary motor cortex, a substrate for execution of articulatory movements. Our data support the conclusion that stuttering is a disorder related primarily to disruption in the cortical and subcortical neural systems supporting the selection, initiation and execution of motor sequences necessary for fluent speech production.

Key Words: speech dysfluency; functional imaging; diffusion tensor imaging; basal ganglia; ventral premotor cortex

Abbreviations: BOLD, blood oxygenation-level dependant; FA, fractional anisotropy; FSL, FMRIB software library; IFG, inferior frontal gyrus; PPN, pedunculopontine nucleus; PWS, people who stutter; STN, subthalamic nucleus; TBSS, tract-based spatial statistics

Received March 30, 2007. Revised August 29, 2007. Accepted September 10, 2007.


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