Brain correlates of stuttering and syllable production: A PET performance-correlation analysis

Abstract

To distinguish the neural systems of normal speech from those of stuttering, PET images of brain blood flow were probed (correlated voxel-wise) with per-trial speech-behaviour scores obtained during PET imaging. Two cohorts were studied: 10 right-handed men who stuttered and 10 right-handed, age- and sex-matched non-stuttering controls. Ninety PET blood flow images were obtained in each cohort (nine per subject as three trials of each of three conditions) from which r-value statistical parametric images (SPI¿r¿) were computed. Brain correlates of stutter rate and syllable rate showed striking differences in both laterality and sign (i.e. positive or negative correlations). Stutter-rate correlates, both positive and negative, were strongly lateralized to the right cerebral and left cerebellar hemispheres. Syllable correlates in both cohorts were bilateral, with a bias towards the left cerebral and right cerebellar hemispheres, in keeping with the left-cerebral dominance for language and motor skills typical of right-handed subjects. For both stutters and syllables, the brain regions that were correlated positively were those of speech production: the mouth representation in the primary motor cortex; the supplementary motor area; the inferior lateral premotor cortex (Broca's area); the anterior insula; and the cerebellum. The principal difference between syllable-rate and stutter-rate positive correlates was hemispheric laterality. A notable exception to this rule was that cerebellar positive correlates for syllable rate were far more extensive in the stuttering cohort than in the control cohort, which suggests a specific role for the cerebellum in enabling fluent utterances in persons who stutter. Stutters were negatively correlated with right-cerebral regions (superior and middle temporal gyrus) associated with auditory perception and processing, regions which were positively correlated with syllables in both the stuttering and control cohorts. These findings support long-held theories that the brain correlates of stuttering are the speech-motor regions of the non-dominant (right) cerebral hemisphere, and extend this theory to include the non-dominant (left) cerebellar hemisphere. The present findings also indicate a specific role of the cerebellum in the fluent utterances of persons who stutter. Support is also offered for theories that implicate auditory processing problems in stuttering.

The neural substrates for atypical planning and execution of word production in stuttering

“…In previous research, researchers tried to use correlation analysis to separate stutteringrelated neural system from that for normal speech (e.g., Braun et al, 1997;Fox et al, 2000). Their results have been inconsistent (Braun et al, 1997;Fox et al, 2000;Giraud et al, 2008;Ingham et al, 2004). By separating the planning and execution processes, our results can help to shed light on the possible reasons for the inconsistenies.…”

“…We interpret these results to mean that the neural activity of these brain regions is the common neural feature for all stuttering speakers regardless of their severity levels. In previous research, researchers tried to use correlation analysis to separate stutteringrelated neural system from that for normal speech (e.g., Braun et al, 1997;Fox et al, 2000). Their results have been inconsistent (Braun et al, 1997;Fox et al, 2000;Giraud et al, 2008;Ingham et al, 2004).…”

“…The contribution from the left IFG to the discrimination of stuttering is consistent with the altered anatomical structure (i.e., reduced grey matter volume and fractional anisotropy) in this region among stuttering children . However, among previous functional imaging studies, some reported the involvement of the left IFG in stuttering (e.g., Braun et al, 1997;De Nil et al, 2008;Lu et al, 2009;Neumann et al, 2003;Watkins et al, 2008;Wu et al, 1995), whereas others did not (Chang et al, 2009;Fox et al, 2000;Ingham et al, 2000). This discrepency may have resulted from the fact that previous studies did not separately examine planning and execution processes in which the left IFG may play different roles.…”

“…Previous research has reported the involvement of the PMA in stuttering (e.g., Braun et al, 1997;Fox et al, 2000;Watkins et al, 2008), but has not specified its association with atypical motor execution. Interestingly, a study using intraoperative functional mapping in awake patients showed that there may be a well-ordered functional organization in the PMA: The ventral part might be involved in planification of articulation, and the dorsal part might be involved in the naming network (Duffau et al, 2003).…”

“…However, it is still unclear what the neural substrates for atypical planning or execution are and how the neural substrates for the two atypical processes interact with each other. Previous brain imaging studies have revealed widely distributed neural differences between stuttering and non-stuttering speakers, such as the the over-activation in the right frontal operculum/anterior insula and the right cerebellum, absent activation in the bilateral auditory areas, and increased or decreased activation in the motor areas and the basal ganglia (Brown et al, 2005;De Nil et al, 2008Fox et al, 2000;Ingham et al, 2000Ingham et al, , 2004Neumann et al, 2003;Wu et al, 1995). However, it is not clear which of the above neural differences are associated with atypical planning, execution, or interface between them.…”