Activation in Right Dorsolateral Prefrontal Cortex Underlies Stuttering Anticipation

Abstract

People who stutter learn to anticipate many of their overt stuttering events. Despite the critical role of anticipation, particularly how responses to anticipation shape stuttering behaviors, the neural bases associated with anticipation are unknown. We used a novel approach to identify anticipated and unanticipated words in 22 adult stutterers, which were produced in a delayed-response task while hemodynamic activity was measured using functional near infrared spectroscopy (fNIRS). Twenty-two control participants were included such that each individualized set of anticipated/unanticipated words was produced by one stutterer and one control. We conducted an analysis on the right dorsolateral prefrontal cortex (R-DLPFC) based on converging lines of evidence from the stuttering and cognitive control literatures. We also assessed connectivity between the R-DLPFC and right supramarginal gyrus (R-SMG), two key nodes of the frontoparietal network (FPN), to assess the role of cognitive control, particularly error-likelihood monitoring, in stuttering anticipation. All analyses focused on the five-second anticipation phase preceding the go signal to produce speech. Results indicate that anticipated words are associated with elevated activation in the R-DLPFC, and that compared to non-stutterers, stutterers exhibit greater activity in the R-DLPFC, irrespective of anticipation. Further, anticipated words are associated with reduced connectivity between the R-DLPFC and R-SMG. These findings highlight the potential roles of the R-DLPFC and the greater FPN as a neural substrate of stuttering anticipation. The results also support previous accounts of error-likelihood monitoring and action-stopping in stuttering anticipation. Overall, this work offers numerous directions for future research with clinical implications for targeted neuromodulation.

Reactive Inhibitory Control Precedes Overt Stuttering Events

“…35 Mean reaction time was 675.84 ms (SD = 272.99). Reaction time was calculated as the time between the go signal (i.e., the green asterisk) and speech onset as defined by the first articulatory movement or accessory behavior (as in Jackson et al 22 ) Accessory behaviors refer to non-speech behaviors that often co-occur with stuttering events (e.g., eye blinking, facial tension). Articulatory onset was defined as the first articulatory movement, which was determined based on visual inspection using Davinci Resolve (Black Magic Design, Australia).…”

“…Global inhibition and anticipation are separable but related processes that occur in similar time frames (i.e., prior to speech initiation). Elevated activation in the right dorsolateral prefrontal cortex for anticipated versus unanticipated words has been interpreted as a substrate for error-likelihood monitoring 22 , which could facilitate the speaker's responses to the anticipation of stuttering, for example, by substituting planned words, applying a learned strategy, or avoiding speech altogether. 19 Neef et al 26 suggested that global inhibition is reactive, whereas anticipation is proactive.…”

“…The interview was adapted from Jackson et al 1,22 In that study, both anticipated and unanticipated words were elicited from participants, which yielded a near equal distribution of stuttered and fluent speech during fNIRS recording. However, Jackson et al 1,22 included interactive speech whereas the current study did not; the likelihood of stuttering during testing with face-to-face communication is higher.…”

“…The interview was adapted from Jackson et al 1,22 In that study, both anticipated and unanticipated words were elicited from participants, which yielded a near equal distribution of stuttered and fluent speech during fNIRS recording. However, Jackson et al 1,22 included interactive speech whereas the current study did not; the likelihood of stuttering during testing with face-to-face communication is higher. Therefore, we only elicited anticipated words in the current study to increase the probability of a near-balanced distribution of stuttered and fluent speech in the absence of face-to-face communication (i.e., in the shielded room while MEG data were recorded).…”

“…Time-locking to stimulus presentation is useful when the focus is on the neural dynamics elicited by the stimuli themselves. For example, Jackson et al 22 found elevated activation in the right dorsolateral prefrontal cortex (R-DLPFC) in response to anticipated words (i.e., words that are associated with more stuttering for the individual, such as one's own name). Other considerations with studies that have looked at activity prior to speech initiation include relatively small sample sizes (less than ten participants), limited numbers of stuttered trials (less than 20%) 16,18 , and not comparing stuttered and fluent speech in stutterers.…”