The trajectory of gray matter development in Broca's area is abnormal in people who stutter

Abstract

The acquisition and mastery of speech-motor control requires years of practice spanning the course of development. People who stutter often perform poorly on speech-motor tasks thereby calling into question their ability to establish the stable neural motor programs required for masterful speech-motor control. There is evidence to support the assertion that these neural motor programs are represented in the posterior part of Broca's area, specifically the left pars opercularis. Consequently, various theories of stuttering causation posit that the disorder is related to a breakdown in the formation of the neural motor programs for speech early in development and that this breakdown is maintained throughout life. To date, no study has examined the potential neurodevelopmental signatures of the disorder across pediatric and adult populations. The current study aimed to fill this gap in our knowledge. We hypothesized that the developmental trajectory of cortical thickness in people who stutter would differ across the lifespan in the left pars opercularis relative to a group of control participants. We collected structural magnetic resonance images from 116 males (55 people who stutter) ranging in age from 6 to 48 years old. Differences in cortical thickness across ages and between patients and controls were investigated in 30 brain regions previously implicated in speech-motor control. An interaction between age and group was found for the left pars opercularis only. In people who stutter, the pars opercularis did not demonstrate the typical maturational pattern of gradual gray matter thinning with age across the lifespan that we observed in control participants. In contrast, the developmental trajectory of gray matter thickness in other regions of interest within the neural network for speech-motor control was similar for both groups. Our findings indicate that the developmental trajectory of gray matter in left pars opercularis is abnormal in people who stutter.

Keywords: Broca’s area; cortical thickness; developmental disorders; developmental stuttering; inferior frontal gyrus; motor control; neurodevelopment; speech production.

Figure 1

MRI preprocessing: the T1 images were (A) registered to the ICBM 152 template with a 12-parameter linear transformation, (B) RF inhomogeneity corrected and skull stripped, (C) tissue segmented and gray and white matter surfaces created and (D) tissue partial volumes estimated. Cortical thickness was measured as the distance between the white and gray surfaces in native space.

Figure 2

The regions of interest depicted on the gray matter surface of the left hemisphere: (A) the anterior (green) and posterior (red) angular gyrus, anterior (pink) and posterior (blue) superior temporal sulcus and anterior (dark pink) and posterior (blue) superior temporal gyrus; (B) ventral (green) and dorsal (brown) premotor cortex, ventral (red) and dorsal (blue) primary motor cortex and ventral (pink) and dorsal (purple) sensorimotor cortex; (C) pars orbitalis (BA47); (D) pars triangularis (BA45) and (E). pars opercularis (BA44).

Figure 3

Each graph depicts the association between age (6–49 years old) and cortical thickness (millimeters) for an exemplary region interest. Results for the people who stutter are shown in red and for the control group in blue. Regression lines are included and circles indicate individual measurements. The only significant interaction between age and group for cortical thickness was found in the left pars opercularis (p = 0.001, q = 0.04). By contrast, the developmental trajectory of thickness for all of the other ROIs was similar for both groups and no statistically significant differences were identified.