Dissociated development of speech and limb sensorimotor learning in stuttering: speech auditory-motor learning is impaired in both children and adults who stutter

Abstract

Stuttering is a neurodevelopmental disorder of speech fluency. Various experimental paradigms have demonstrated that affected individuals show limitations in sensorimotor control and learning. However, controversy exists regarding two core aspects of this perspective. First, it has been claimed that sensorimotor learning limitations are detectable only in adults who stutter (after years of coping with the disorder) but not during childhood close to the onset of stuttering. Second, it remains unclear whether stuttering individuals' sensorimotor learning limitations affect only speech movements or also unrelated effector systems involved in nonspeech movements. We report data from separate experiments investigating speech auditory-motor learning (N = 60) and limb visuomotor learning (N = 84) in both children and adults who stutter versus matched nonstuttering individuals. Both children and adults who stutter showed statistically significant limitations in speech auditory-motor adaptation with formant-shifted feedback. This limitation was more profound in children than in adults and in younger children versus older children. Between-group differences in the adaptation of reach movements performed with rotated visual feedback were subtle but statistically significant for adults. In children, even the nonstuttering groups showed limited visuomotor adaptation just like their stuttering peers. We conclude that sensorimotor learning is impaired in individuals who stutter, and that the ability for speech auditory-motor learning -- which was already adult-like in 3-6 year-old typically developing children -- is severely compromised in young children near the onset of stuttering. Thus, motor learning limitations may play an important role in the fundamental mechanisms contributing to the onset of this speech disorder.

Relevance of Auditory Errors Decreases When Errors Are Introduced Suddenly

“…However, our between-subject analysis showed that responses to gradual perturbations were like sudden perturbations (except in the change phase) for formant-shift and formant-clamp perturbations. The results for gradually vs. suddenly introduced formant-shift perturbations are consistent with the results of previous studies (Kearney et al, 2020; Kim et al, 2020; MacDonald et al, 2010). These results may be related to the fact that the within-subject analysis is more sensitive to detect potential effects (for a review, see Charness et al, 2012) of the sudden and gradual introduction of perturbations.…”

“…Our results may also have clinical implications. For example, we have previously shown that adaptive responses to auditory perturbations are significantly small (or nonexistent) for adults who stutter (Daliri et al, 2017; Daliri & Max, 2018; Kim et al, 2020; Max & Daliri, 2019). Previously, we interpreted the small adaptive responses of people who stutter as lower sensitivity to errors.…”

“…Prediction errors typically occur due to structural changes in speech articulators (e.g., rapid developmental changes during childhood or structural changes during the aging process) or sensory feedback (e.g., hearing impairment) (Daliri et al, 2013; Perkell, 2012; Perkell et al, 1992; Pittman et al, 2018; Vorperian et al, 2005, 2009). One could generate prediction errors in the laboratory setting by experimentally manipulating somatosensory feedback (Daliri et al, 2013; Lametti et al, 2012; Tremblay et al, 2003) or auditory feedback (Abur et al, 2018; Ballard et al, 2018; Daliri et al, 2017; Daliri & Max, 2018; Houde & Jordan, 1998; Kim et al, 2020; Kothare et al, 2020; Scott et al, 2020; Stepp et al, 2017). Due to practical reasons and the importance of auditory feedback for speech production, many studies have used auditory perturbations to induce auditory prediction errors during speaking (for a review, see Fuchs et al, 2019).…”

“…In that study, we applied the perturbations gradually; thus, the SMS was exposed to small errors that incrementally increased over several trials, allowing the SMS to develop adaptive responses to the experienced errors. Studies of limb motor learning suggest that different neural processes may prepare adaptive responses to gradually and suddenly introduced errors (Doya, 2000; Kim et al, 2020; Smith & Shadmehr, 2005; Venkatakrishnan et al, 2011; Werner et al, 2010). By examining adaptive responses to formant-shift perturbations, previous studies have shown that the SMS generates similar adaptive responses to gradually and suddenly introduced auditory errors (Kearney et al, 2020; Kim et al, 2020; MacDonald et al, 2010).…”

“…Studies of limb motor learning suggest that different neural processes may prepare adaptive responses to gradually and suddenly introduced errors (Doya, 2000; Kim et al, 2020; Smith & Shadmehr, 2005; Venkatakrishnan et al, 2011; Werner et al, 2010). By examining adaptive responses to formant-shift perturbations, previous studies have shown that the SMS generates similar adaptive responses to gradually and suddenly introduced auditory errors (Kearney et al, 2020; Kim et al, 2020; MacDonald et al, 2010). However, it remained unclear how the SMS would evaluate and respond to suddenly introduced formant-clamp perturbations.…”