Stuttered and fluent speech production: an ALE meta-analysis of functional neuroimaging studies

Abstract

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.

Figure 1

Axial slices demonstrating major ALE foci from the two meta‐analyses. a: Major ALE foci for the fluent controls. Principal sites of activation are labeled; bilateral cortical activations are labeled on only one side of the brain. b: Major ALE foci for the stuttering subjects. The labels highlight activations seen uniquely in the stuttering group. c: Group comparison of the ALE foci from the two groups. For this panel only, orange indicates stutterers > controls, and blue indicates controls > stutterers (the latter seen only for the superior temporal sulcus). Labels highlight the vocal‐motor areas shown by the meta‐analysis to have large cross‐laboratory concordance. The bilateral auditory areas, present in controls but absent in the stutterers, are below threshold in the group comparison. The Talairach coordinates for the slices are shown at the bottom of the figure. The same set of seven slices is shown in all three panels. The left side of a slice is the left side of the brain. The threshold for all analyses is P < 0.05. STS, superior temporal sulcus; RO, Rolandic operculum; M1, primary motor cortex; SMA, supplementary motor area; Vermis III, the medial portion of lobule III of the cerebellum; FO, frontal operculum/anterior insula; SMG, supramarginal gyrus; CMA, cingulate motor area.