Hemodynamics of speech production: An fNIRS investigation of children who stutter

Abstract

Stuttering affects nearly 1% of the population worldwide and often has life-altering negative consequences, including poorer mental health and emotional well-being, and reduced educational and employment achievements. Over two decades of neuroimaging research reveals clear anatomical and physiological differences in the speech neural networks of adults who stutter. However, there have been few neurophysiological investigations of speech production in children who stutter. Using functional near-infrared spectroscopy (fNIRS), we examined hemodynamic responses over neural regions integral to fluent speech production including inferior frontal gyrus, premotor cortex, and superior temporal gyrus during a picture description task. Thirty-two children (16 stuttering and 16 controls) aged 7-11 years participated in the study. We found distinctly different speech-related hemodynamic responses in the group of children who stutter compared to the control group. Whereas controls showed significant activation over left dorsal inferior frontal gyrus and left premotor cortex, children who stutter exhibited deactivation over these left hemisphere regions. This investigation of neural activation during natural, connected speech production in children who stutter demonstrates that in childhood stuttering, atypical functional organization for speech production is present and suggests promise for the use of fNIRS during natural speech production in future research with typical and atypical child populations.

Figure 1

Grand averaged Oxy-Hb (red) and Deoxy-Hb (blue) hemodynamic responses with standard error curves for IFG channels. Channels for the controls (n = 16) are shown on the left hand side of this figure and channels for the children who stutter (n = 16) are plotted on the right. Within each participant group, left hemisphere channels are plotted side-by-side with homologous right channels for comparison. Channels showing a significant group difference are bold-framed. Time = 0 indicates trial onset. Gray shading indicates the 3–8 s. window of analysis.

Figure 2

Grand averaged Oxy-Hb (red) and Deoxy-Hb (blue) hemodynamic responses with standard error curves for STG (top plots) and PMC (bottom plots) channels. Channels for the controls (n = 16) are shown on the left hand side of this figure and channels for the children who stutter (n = 16) are plotted on the right. Within each participant group, left hemisphere channels are plotted side-by-side with homologous right channels for comparison. Channels showing a significant group difference are bold-framed. Time = 0 indicates trial onset. Gray shading indicates the 3–8 s. window of analysis.

Figure 3

Topographic images of cortical activation within the boundaries of the probe derived from Oxy-Hb (left pairs) and Deoxy-Hb (right pairs) response amplitudes within the 3–8 s post-stimulus analysis window of analysis. First rows: left and right hemisphere average hemoglobin responses for the control participants. Second rows: left and right hemisphere average hemoglobin responses for group of children who stutter. Third row: t-maps outlining regions of significant difference between the control and stuttering groups (independent sample t-tests, p < 0.05, FDR-corrected). The brain templates, courtesy of John Richards’s Lab, represent average whole-head MRI images from 72 10-year-old children.

Figure 4

Experiment overview. Example of a talk trial (left slides) and a null trial (right slides). For the 30 talk trials, children viewed each picture for 2 s. A green “go” circle appeared in the corner of the picture cueing the children to begin speaking. After 4 s of speech, a stop sign appeared cueing the children to stop speaking. Finally, a patterned slide, devoid of overt semantic content, remained on the screen for 10–12 s to allow the hemodynamic response to recover. For the 15 null trials, the children watched a fixation point for 6 s (the amount of time they would have seen and described a picture) followed by the a stop sign and patterned recovery slide. The talk and null trials were randomized for presentation. Zoo illustration used with permission from Super Duper® Publications.

Figure 5

fNIRS probe arrays. Approximate positions of emitting (red circles) and detecting (blue circles) optodes are shown on a standard brain atlas (ICBM 152). The probes were placed symmetrically over both hemispheres, with channels 1–5 spanning inferior frontal gyrus, channels 6–7 over superior temporal gyrus, and channels 8–9 over precentral gyrus/premotor cortex.