The neural correlates of speech motor sequence learning

Speech is perhaps the most sophisticated example of a species-wide movement capability in the animal kingdom, requiring split-second sequencing of approximately 100 muscles in the respiratory, laryngeal, and oral movement systems. Despite the unique role speech plays in human interaction and the debilitating impact of its disruption, little is known about the neural mechanisms underlying speech motor learning. Here, we studied the behavioral and neural correlates of learning new speech motor sequences. Participants repeatedly produced novel, meaningless syllables comprising illegal consonant clusters (e.g., GVAZF) over 2 days of practice. Following practice, participants produced the sequences with fewer errors and shorter durations, indicative of motor learning. Using fMRI, we compared brain activity during production of the learned illegal sequences and novel illegal sequences. Greater activity was noted during production of novel sequences in brain regions linked to non-speech motor sequence learning, including the BG and pre-SMA. Activity during novel sequence production was also greater in brain regions associated with learning and maintaining speech motor programs, including lateral premotor cortex, frontal operculum, and posterior superior temporal cortex. Measures of learning success correlated positively with activity in left frontal operculum and white matter integrity under left posterior superior temporal sulcus. These findings indicate speech motor sequence learning relies not only on brain areas involved generally in motor sequencing learning but also those associated with feedback-based speech motor learning. Furthermore, learning success is modulated by the integrity of structural connectivity between these motor and sensory brain regions.R01 DC007683 - NIDCD NIH HHS; R01DC007683 - NIDCD NIH HH

Accessory to dissipate heat from transcranial magnetic stimulation coils

Background: Transcranial magnetic stimulation (TMS) produces magnetic pulses by passing a strong electrical current through coils of wire. Repeated stimulation accumulates heat, which places practical constraints on experimental design. New Method: We designed a condensation-free pre-chilled heat sink to extend the operational duration of transcranial magnetic stimulation coils. Results: The application of a pre-chilled heat sink reduced the rate of heating across all tests and extended the duration of stimulation before coil overheating, particularly in conditions where heat management was problematic. Comparison with Existing Method: Applying an external heat sink had the practical effect of extending the operational time of TMS coils by 5.8 to 19.3 minutes compared to standard operating procedures. Conclusion: Applying an external heat sink increases the quantity of data that can be collected within a single experimental session

Paradoxical facilitation alongside interhemispheric inhibition

Neurophysiological experiments using transcranial magnetic stimulation (TMS) have sought to probe the function of the motor division of the corpus callosum. Primary motor cortex sends projections via the corpus callosum with a net inhibitory influence on the homologous region of the opposite hemisphere. Interhemispheric inhibition (IHI) experiments probe this inhibitory pathway. A test stimulus (TS) delivered to the motor cortex in one hemisphere elicits motor evoked potentials (MEPs) in a target muscle, while a conditioning stimulus (CS) applied to the homologous region of the opposite hemisphere modulates the effect of the TS. We predicted that large CS MEPs would be associated with increased IHI since they should be a reliable index of how effectively contralateral motor cortex was stimulated and therefore of the magnitude of interhemispheric inhibition. However, we observed a strong tendency for larger CS MEPs to be associated with reduced interhemispheric inhibition which in the extreme lead to a net effect of facilitation. This surprising effect was large, systematic, and observed in nearly all participants. We outline several hypotheses for mechanisms which may underlie this phenomenon to guide future research. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1007/s00221-021-06183-9

Pediatric Responses to Fundamental and Formant Frequency Altered Auditory Feedback: A Scoping Review

Purpose: The ability to hear ourselves speak has been shown to play an important role in the development and maintenance of fluent and coherent speech. Despite this, little is known about the developing speech motor control system throughout childhood, in particular if and how vocal and articulatory control may differ throughout development. A scoping review was undertaken to identify and describe the full range of studies investigating responses to frequency altered auditory feedback in pediatric populations and their contributions to our understanding of the development of auditory feedback control and sensorimotor learning in childhood and adolescence. Method: Relevant studies were identified through a comprehensive search strategy of six academic databases for studies that included (a) real-time perturbation of frequency in auditory input, (b) an analysis of immediate effects on speech, and (c) participants aged 18 years or younger. Results: Twenty-three articles met inclusion criteria. Across studies, there was a wide variety of designs, outcomes and measures used. Manipulations included fundamental frequency (9 studies), formant frequency (12), frequency centroid of fricatives (1), and both fundamental and formant frequencies (1). Study designs included contrasts across childhood, between children and adults, and between typical, pediatric clinical and adult populations. Measures primarily explored acoustic properties of speech responses (latency, magnitude, and variability). Some studies additionally examined the association of these acoustic responses with clinical measures (e.g., stuttering severity and reading ability), and neural measures using electrophysiology and magnetic resonance imaging. Conclusion: Findings indicated that children above 4 years generally compensated in the opposite direction of the manipulation, however, in several cases not as effectively as adults. Overall, results varied greatly due to the broad range of manipulations and designs used, making generalization challenging. Differences found between age groups in the features of the compensatory vocal responses, latency of responses, vocal variability and perceptual abilities, suggest that maturational changes may be occurring in the speech motor control system, affecting the extent to which auditory feedback is used to modify internal sensorimotor representations. Varied findings suggest vocal control develops prior to articulatory control. Future studies with multiple outcome measures, manipulations, and more expansive age ranges are needed to elucidate findings

Human larynx motor cortices coordinate respiration for vocal-motor control

Vocal flexibility is a hallmark of the human species, most particularly the capacity to speak and sing. This ability is supported in part by the evolution of a direct neural pathway linking the motor cortex to the brainstem nucleus that controls the larynx the primary sound source for communication. Early brain imaging studies demonstrated that larynx motor cortex at the dorsal end of the orofacial division of motor cortex (dLMC) integrated laryngeal and respiratory control, thereby coordinating two major muscular systems that are necessary for vocalization. Neurosurgical studies have since demonstrated the existence of a second larynx motor area at the ventral extent of the orofacial motor division (vLMC) of motor cortex. The vLMC has been presumed to be less relevant to speech motor control, but its functional role remains unknown. We employed a novel ultra-high field (7T) magnetic resonance imaging paradigm that combined singing and whistling simple melodies to localise the larynx motor cortices and test their involvement in respiratory motor control. Surprisingly, whistling activated both ‘larynx areas’ more strongly than singing despite the reduced involvement of the larynx during whistling. We provide further evidence for the existence of two larynx motor areas in the human brain, and the first evidence that laryngeal-respiratory integration is a shared property of both larynx motor areas. We outline explicit predictions about the descending motor pathways that give these cortical areas access to both the laryngeal and respiratory systems and discuss the implications for the evolution of speech

A fNIRS investigation of speech planning and execution in adults who stutter

Our study aimed to determine the neural correlates of speech planning and execution in adults who stutter (AWS). Fifteen AWS and 15 controls (CON) completed two tasks that either manipulated speech planning or execution processing loads. Functional near-infrared spectroscopy (fNIRS) was used to measure changes in blood flow concentrations during each task, thus providing an indirect measure of neural activity. An image-based reconstruction technique was used to analyze the results and facilitate their interpretation in the context of previous functional neuroimaging studies of AWS that used positron emission tomography (PET) or functional magnetic resonance imaging (fMRI). For planning, we compared neural activity associated with high versus low planning load in AWS and CON. For execution, we compared the neural activity associated with overt versus covert naming in AWS and CON. Broadly, group level effects corroborate previous PET/fMRI findings including under-activation in lefthemisphere perisylvian speech-language networks and over-activation in righthemisphere homologues. Increased planning load revealed atypical left-hemisphere activation in AWS, whereas increased execution load yielded atypical right frontotemporo-parietal and bilateral motor activation in AWS. Our results add to the limited literature differentiating speech planning versus execution processes in AWS

Weak Responses to Auditory Feedback Perturbation during Articulation in Persons Who Stutter: Evidence for Abnormal Auditory-Motor Transformation

Previous empirical observations have led researchers to propose that auditory feedback (the auditory perception of self-produced sounds when speaking) functions abnormally in the speech motor systems of persons who stutter (PWS). Researchers have theorized that an important neural basis of stuttering is the aberrant integration of auditory information into incipient speech motor commands. Because of the circumstantial support for these hypotheses and the differences and contradictions between them, there is a need for carefully designed experiments that directly examine auditory-motor integration during speech production in PWS. In the current study, we used real-time manipulation of auditory feedback to directly investigate whether the speech motor system of PWS utilizes auditory feedback abnormally during articulation and to characterize potential deficits of this auditory-motor integration. Twenty-one PWS and 18 fluent control participants were recruited. Using a short-latency formant-perturbation system, we examined participants’ compensatory responses to unanticipated perturbation of auditory feedback of the first formant frequency during the production of the monophthong [ε]. The PWS showed compensatory responses that were qualitatively similar to the controls’ and had close-to-normal latencies (~150 ms), but the magnitudes of their responses were substantially and significantly smaller than those of the control participants (by 47% on average, p<0.05). Measurements of auditory acuity indicate that the weaker-than-normal compensatory responses in PWS were not attributable to a deficit in low-level auditory processing. These findings are consistent with the hypothesis that stuttering is associated with functional defects in the inverse models responsible for the transformation from the domain of auditory targets and auditory error information into the domain of speech motor commands

Decreased cerebellar-orbitofrontal connectivity correlates with stuttering severity: Whole-brain functional and structural connectivity associations with persistent developmental stuttering

Persistent developmental stuttering is characterized by speech production disfluency and affects 1% of adults. The degree of impairment varies widely across individuals and the neural mechanisms underlying the disorder and this variability remain poorly understood. Here, we elucidate compensatory mechanisms related to this variability in impairment using whole-brain functional and white matter connectivity analyses in persistent developmental stuttering. We found that people who stutter had stronger functional connectivity between cerebellum and thalamus than people with fluent speech, while stutterers with the least severe symptoms had greater functional connectivity between left cerebellum and left orbitofrontal cortex. Additionally, people who stutter had decreased functional and white matter connectivity among the perisylvian auditory, motor, and speech planning regions compared to typical speakers, but greater functional connectivity between the right basal ganglia and bilateral temporal auditory regions. Structurally, disfluency ratings were negatively correlated with white matter connections to left perisylvian regions and to the brain stem. Overall, we found increased connectivity among subcortical and reward network structures in people who stutter compared to controls. These connections were negatively correlated with stuttering severity, suggesting the involvement of cerebellum and orbitofrontal cortex may underlie successful compensatory mechanisms by more fluent stutterers

Motor sequence learning in children with recovered and persistent developmental stuttering: Preliminary findings

PURPOSE: Previous studies have associated developmental stuttering with difficulty learning new motor skills. We investigated non-speech motor sequence learning in children with persistent developmental stuttering (CWS), children who have recovered from developmental stuttering (CRS) and typically developing controls (CON). METHODS: Over the course of two days, participants completed the Multi-Finger Sequencing Task, consisting of repeated trials of a10-element sequence, interspersed with trials of random sequences of the same length. We evaluated motor sequence learning using accuracy and response synchrony, a timing measure for evaluation of sequencing timing. We examined error types as well as recognition and recall of the repeated sequences. RESULTS: CWS demonstrated lower performance accuracy than CON and CRS on the first day of the finger tapping experiment but improved to the performance level of CON and CRS on the second day. Response synchrony showed no overall difference among CWS, CRS and CON. Learning scores of repeated sequences did not differ from learning scores of random sequences in CWS, CRS and CON. CON and CRS demonstrated an adaptive strategy to response errors, whereas CWS maintained a high percentage of corrected errors for both days. CONCLUSIONS: Our study examined non-speech sequence learning across CWS, CRS and CON. Our preliminary findings support the idea that developmental stuttering is not associated with sequence learning per se but rather with general fine motor performance difficulties