Dissecting structural connectivity of the left and right inferior frontal cortex in children who stutter

Abstract

Inferior frontal cortex pars opercularis (IFCop) features a distinct cerebral dominance and vast functional heterogeneity. Left and right IFCop are implicated in developmental stuttering. Weak left IFCop connections and divergent connectivity of hyperactive right IFCop regions have been related to impeded speech. Here, we reanalyzed diffusion magnetic resonance imaging data from 83 children (41 stuttering). We generated connection probability maps of functionally segregated area 44 parcels and calculated hemisphere-wise analyses of variance. Children who stutter showed reduced connectivity of executive, rostral-motor, and caudal-motor corticostriatal projections from the left IFCop. We discuss this finding in the context of tracing studies from the macaque area 44, which leads to the need to reconsider current models of speech motor control. Unlike the left, the right IFCop revealed increased connectivity of the inferior posterior ventral parcel and decreased connectivity of the posterior dorsal parcel with the anterior insula, particularly in stuttering boys. This divergent connectivity pattern in young children adds to the debate on potential core deficits in stuttering and challenges the theory that right hemisphere differences might exclusively indicate compensatory changes that evolve from lifelong exposure. Instead, early right prefrontal connectivity differences may reflect additional brain signatures of aberrant cognition–emotion–action influencing speech motor control.

Brain developmental trajectories associated with childhood stuttering persistence and recovery

“…Previous studies have reported results from datasets collected from subsets of participants in the current study (shown in Table S3 ). DTI datasets from a subset of participants have been reported in three previous papers ( Chang et al, 2015 , Chang and Zhu, 2013 , Johnson et al, 2022 , Neef et al, 2022 ). Resting state fMRI datasets from a subset of participants were also reported in previous studies ( Chang and Zhu, 2013 , Chang et al, 2016 , Chang et al, 2018 ).…”

Cortical tracking of speech is reduced in adults who stutter when listening for speaking

“…C. Etchell et al, 2014, 2018; Ingham et al, 2012; Neef et al, 2015), suggesting that they may have a role in compensatory (as well as in pathological) speech-motor programming and execution processes in AWS (Busan et al, 2019; A. C. Etchell et al, 2014; Neef et al, 2015, 2016, 2018b, 2023).…”

Knowns and unknowns about the neurobiology of stuttering

“…Furthermore, in children with persistent stuttering, MRI techniques have shown morphological differences in cortical and subcortical motor structures, including decreases in cortical thickness in the left premotor and motor regions [76], and decreases in gray matter volume in the left ventral premotor cortex and subcortical areas, including the basal ganglia [77]. White matter structure differences have also been observed, affecting areas involved in auditorymotor integration, motor initiation, monitoring, and interhemispheric coordination [77][78][79][80]. These structural differences are correlated with stuttering severity [77], suggesting their relevance to speech fluency.…”

“…The absence of a similar rightward shift in children [ 81 ] supports this proposed compensatory hypothesis. However, task-related MRI data in children are scarce, and recent studies present a more diverse perspective, suggesting that the alterations observed in the right hemisphere may represent a combination of both compensatory efforts and direct manifestations of stuttering [ 51 , 80 , 85 ].…”