Neural systems mediating processing of sound units of language distinguish recovery versus persistence in stuttering

Abstract

BackgroundDevelopmental stuttering is a multi-factorial disorder. Measures of neural activity while children processed the phonological (language sound unit) properties of words have revealed neurodevelopmental differences between fluent children and those who stutter. However, there is limited evidence to show whether the neural bases of phonological processing can be used to identify stuttering recovery status. As an initial step, we aimed to determine if differences in neural activity during phonological processing could aid in distinguishing children who had recovered from stuttering and those whose stuttering persisted.MethodsWe examined neural activity mediating phonological processing in forty-three 7-8 year old children. Groups included children who had recovered from stuttering (CWS-Rec), those whose stuttering persisted (CWS-Per), and children who did not stutter (CWNS). All children demonstrated normal non-verbal intelligence and language skills. Electroencephalograms were recorded as the children listened to pairs of pseudo-words (primes-targets) that either rhymed or did not. Behavioral rhyme judgments along with peak latency and mean amplitude of the N400s elicited by prime and target stimuli were examined.ResultsAll the groups were very accurate in their rhyme judgments and displayed a typical ERP rhyme effect, characterized by increased N400 amplitudes over central parietal sites for nonrhyming targets compared to rhyming targets. However, over anterior electrode sites, an earlier onset of the N400 for rhyming compared to non-rhyming targets, indexing phonological segmentation and rehearsal, was observed in the CWNS and CWS-Rec groups. This effect occurred bilaterally for the CWNS, was greater over the right hemisphere in the CWS-Rec, and was absent in the CWS-Per.ConclusionsThese results are the first to show that differences in ERPs reflecting phonological processing are marked by atypical lateralization in childhood even after stuttering recovery and more pronounced atypical neural patterns for the children whose stuttering persisted. Despite comparable language and phonological skills as revealed by standardized tests, the neural activity mediating phonological segmentation and rehearsal differentiated 7-8 year old children whose stuttering persisted from those who had recovered from stuttering and typically developing peers.

How Stuttering Develops: The Multifactorial Dynamic Pathways Theory

“…However, the more anterior ERP, in which the onset of the waveform elicited by the rhyming targets is earlier (presumably facilitated by the prime word), was bilateral for the CWNS but right-lateralized for the CWS-Rec. CWS-Per did not show the anterior ERP facilitation effect (Mohan & Weber, 2015). These results indicate that the development of some neural circuits mediating linguistic processes is related to the child's developmental course to recovery or persistence of stuttering.…”

“…The CWS who persisted (CWS-Per) at this age, however, displayed an N400 ERP instead-in this case, a less mature pattern similar to responses of typically developing younger children (ages 3-5 years) in the same task (Usler & Weber-Fox, 2015). In the phonological domain, 7-to 8-year-old CWNS, CWS-Rec, and CWS-Per all showed a robust central-parietal N400 effect elicited by nonrhyming targets (Mohan & Weber, 2015). However, the more anterior ERP, in which the onset of the waveform elicited by the rhyming targets is earlier (presumably facilitated by the prime word), was bilateral for the CWNS but right-lateralized for the CWS-Rec.…”

“…ERPs are sensitive indicators of language proficiency in children and adults even when the range of participants' proficiencies is within normal limits Pakulak & Neville, 2010). In a series of studies from our laboratory, we have used paradigms that elicit well-known languagerelated ERP components (e.g., N400, P600) to determine if and how neural activity patterns mediating semantic, syntactic, and phonological processing differ for AWS and CWS compared with their fluent peers (e.g., Cuadrado & WeberFox, 2003;Mohan & Weber, 2015;Usler & Weber-Fox, 2015;Weber-Fox, 2001;Weber-Fox & Hampton, 2008;Weber-Fox, Hampton Wray, & Arnold, 2013;Weber-Fox, Spencer, Spruill, & Smith, 2004;Weber-Fox, Spruill, Spencer, & Smith, 2008). The N400 component reflects the identification, retrieval, and integration of semantic meaning (Kutas & Federmeier, 2011), and the P600 is thought to index reanalysis and repair processes, often for violations of syntax or grammar or garden path sentences (Gouvea et al, 2010).…”

A Lag in Speech Motor Coordination During Sentence Production Is Associated With Stuttering Persistence in Young Children

“…Bidirectional interactions between language formulation and speech motor coordination ability have been observed (Dromey & Bates, 2005;Goffman, 2010;Smith & Goffman, 2004). Recent studies from the Purdue Stuttering Project have reported maturational lags in various aspects of language processing related to stuttering persistence versus recovery (Kreidler, Hampton Wray, Usler, & Weber, 2016;Mohan & Weber, 2015;Usler & Weber-Fox, 2015). Under a dynamic view of development, the unstable speech motor control of some CWS-Per may be an adaptive effect of a maturational lag in neurodevelopment underlying language acquisition.…”

Preliminary Evidence That Growth in Productive Language Differentiates Childhood Stuttering Persistence and Recovery

“…Because 70%-80% of children are likely to experience spontaneous recovery from stuttering, it is of both practical and scientific value to determine whether or not there are features of early stuttering that can inform recovery. These studies have used a variety of metrics, including language proficiency scores close to onset and phonological encoding skill, including nonword repetition ability (Spencer & Weber-Fox, 2014) and phonological skills measured by standardized assessments Paden, Yairi, & Ambrose, 1999), dissociations among scores on standardized test measures (Clark, Conture, Walden, & Lambert, 2015), expressive language measures (Watkins & Yairi, 1997;Watkins, Yairi, & Ambrose, 1999), standardized language assessment scores over time (Ambrose et al, 2015), cortical processing indices of speech and language (such as event-related potentials; Mohan & Weber, 2015;Usler & Weber-Fox, 2015;Weber-Fox, Wray, & Arnold, 2013), and temperamental factors (Ambrose et al, 2015).…”