Involvement of the Cortico-Basal Ganglia-Thalamocortical Loop in Developmental Stuttering.

Soo-Eun Chang,Frank H Guenther

doi:10.3389/fpsyg.2019.03088

Abstract

Stuttering is a complex neurodevelopmental disorder that has to date eluded a clear explication of its pathophysiological bases. In this review, we utilize the Directions Into Velocities of Articulators (DIVA) neurocomputational modeling framework to mechanistically interpret relevant findings from the behavioral and neurological literatures on stuttering. Within this theoretical framework, we propose that the primary impairment underlying stuttering behavior is malfunction in the cortico-basal ganglia-thalamocortical (hereafter, cortico-BG) loop that is responsible for initiating speech motor programs. This theoretical perspective predicts three possible loci of impaired neural processing within the cortico-BG loop that could lead to stuttering behaviors: impairment within the basal ganglia proper; impairment of axonal projections between cerebral cortex, basal ganglia, and thalamus; and impairment in cortical processing. These theoretical perspectives are presented in detail, followed by a review of empirical data that make reference to these three possibilities. We also highlight any differences that are present in the literature based on examining adults versus children, which give important insights into potential core deficits associated with stuttering versus compensatory changes that occur in the brain as a result of having stuttered for many years in the case of adults who stutter. We conclude with outstanding questions in the field and promising areas for future studies that have the potential to further advance mechanistic understanding of neural deficits underlying persistent developmental stuttering.

Highlights

INTRODUCTIONDevelopmental stuttering (for brevity, “stuttering” hereafter) is a childhood onset speech disorder that affects approximately 5–8% of children and 1% of adults (Månsson, 2000; Reilly et al, 2009)
Developmental stuttering is a childhood onset speech disorder that affects approximately 5–8% of children and 1% of adults (Månsson, 2000; Reilly et al, 2009)
Differences between adults and children who stutter have been identified, including auditory cortex deactivation relative to controls during speech and decreased compensation to auditory perturbations in adults who stutter but not Children who stutter (CWS). This assertion has only been supported in a small number of studies involving CWS, but if this pattern holds up in additional studies, it suggests that decreased auditory feedback processing during speech in adults who stutter is a secondary effect that may develop over years of stuttering; perhaps, as a compensatory mechanism that decreases the probability that a stutter will be induced by the detection of minor inaccuracies in speech output through auditory feedback

Summary

INTRODUCTION

Developmental stuttering (for brevity, “stuttering” hereafter) is a childhood onset speech disorder that affects approximately 5–8% of children and 1% of adults (Månsson, 2000; Reilly et al, 2009). The anomalies in the connections between prefrontal areas and the basal ganglia may affect higher-order cognitive functions (e.g., attention), which help establish and later develop speech control automaticity via the cortico-BG loop This interpretation is relevant to the Chow and Chang (2017) findings that show a negative relationship between stuttering severity and FA along the anterior and superior thalamic radiations in PDS. If auditory feedback of one’s own speech does not match the expected pattern for the current sound (due, for example, to subtle errors in articulation), the striatum may detect a mismatch between the current sensorimotor context and the context needed for initiating the motor program, reducing its competitive advantage over competing motor programs, which in turn may lead to impaired generation of initiation signals by the basal ganglia and a concomitant stutter There were no significant group differences found in the auditory areas, providing some support for the idea that deactivation of auditory cortex is a compensatory mechanism developed after years of stuttering rather than a root cause of the disorder

Findings

DISCUSSION

CONCLUSIONS