Functional Lateralization of Speech Processing in Adults and Children Who Stutter

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.

This study reports an activation likelihood estimation (ALE) meta-analysis of imaging studies of chronic developmental stuttering in adults. Two parallel meta-analyses were carried out: (1) stuttered production in the stutterers; (2) fluent production in the control subjects. The control subjects' data replicated previous analyses of single-word reading, identifying activation in primary motor cortex, premotor cortex, supplementary motor area, Rolandic operculum, lateral cerebellum, and auditory areas, among others. The stuttering subjects' analysis showed that similar brain areas are involved in stuttered speech as in fluent speech, but with some important differences. Motor areas were over-activated in stuttering, including primary motor cortex, supplementary motor area, cingulate motor area, and cerebellar vermis. Frontal operculum, Rolandic operculum, and anterior insula showed anomalous right-laterality in stutterers. Auditory activations, due to hearing one's own speech, were essentially undetectable in stutterers. The phenomenon of efference copy is proposed as a unifying account of the pattern activation revealed within this ALE meta-analysis. This provides the basis for a stuttering system model that is testable and should help to advance the understanding and treatment of this disorder.

Language ability and handedness are likely to be associated with asymmetry of the cerebral cortex (grey matter) and connectivity (white matter). Grey matter asymmetry, most likely linked to language has been identified with voxel-based morphometry (VBM) using T(1)-weighted images. Differences in white matter obtained with this technique are less consistent, probably due to the relative insensitivity of the T(1) contrast to the ultrastructure of white matter. Furthermore, previous VBM studies failed to find differences related to handedness in either grey or white matter. We revisited these issues and investigated two independent groups of subjects with diffusion-tensor imaging (DTI) for asymmetries in white matter composition. Using voxel-based statistical analyses an asymmetry of the arcuate fascicle was observed, with higher fractional anisotropy in the left hemisphere. In addition, we show differences related to handedness in the white matter underneath the precentral gyrus contralateral to the dominant hand. Remarkably, these findings were very robust, even when investigating small groups of subjects. This highlights the sensitivity of DTI for white matter tissue differences, making it an ideal tool to study small patient populations.