Redistribution of neural phase coherence reflects establishment of feedforward map in speech motor adaptation

Abstract

Sengupta R, Nasir SM. Redistribution of neural phase coherence reflects establishment of feedforward map in speech motor adaptation. J Neurophysiol 113: 2471-2479, 2015. First published January 28, 2015 doi:10.1152/jn.00731.2014.-Despite recent progress in our understanding of sensorimotor integration in speech learning, a comprehensive framework to investigate its neural basis is lacking at behaviorally relevant timescales. Structural and functional imaging studies in humans have helped us identify brain networks that support speech but fail to capture the precise spatiotemporal coordination within the networks that takes place during speech learning. Here we use neuronal oscillations to investigate interactions within speech motor networks in a paradigm of speech motor adaptation under altered feedback with continuous recording of EEG in which subjects adapted to the real-time auditory perturbation of a target vowel sound. As subjects adapted to the task, concurrent changes were observed in the theta-gamma phase coherence during speech planning at several distinct scalp regions that is consistent with the establishment of a feedforward map. In particular, there was an increase in coherence over the central region and a decrease over the fronto-temporal regions, revealing a redistribution of coherence over an interacting network of brain regions that could be a general feature of error-based motor learning in general. Our findings have implications for understanding the neural basis of speech motor learning and could elucidate how transient breakdown of neuronal communication within speech networks relates to speech disorders. speech motor learning; neural oscillations; feedforward map AS WE LEARN TO SPEAK, THE auditory, somatosensory and motor areas of our brain operate in parallel to perceive speech stimuli, detect feedback errors and generate the motor commands necessary to achieve speech goals (Guenther 2006;Perkell 2012;Tourville et al. 2008). While this process is believed to involve coordinated activity over several distributed brain areas (Guenther 2006;Hickok et al. 2011;Scott and Wise 2004), the neural mechanisms underlying their precise spatiotemporal coordination remain elusive. The oscillatory dynamics inherent in the brain's electrical activity provide a suitable means to study the neural communication within brain networks (Golfinopoulos et al. 2010;Varela et al. 2011) at timescales relevant for speech. In this study, we provide evidence that brain oscillation patterns change as a result of speech motor adaptation, enabling us to probe into the neural basis of learning at finer temporal resolutions.In recent years, the role of neuronal oscillations and crossfrequency phase coupling, particularly in the theta (3-8 Hz) and gamma (30 -55 Hz) bands, has been demonstrated in a variety of cognitive and sensorimotor tasks in humans involv- (Schack et al. 2002). Based on these results, it has been proposed that communication within brain networks during behavior is facilitated by synchronous neuronal o...

A neurophysiological model of speech production deficits in fragile X syndrome

“…Gamma oscillations originating in frontal cortex occurring prior to speech onset are thought to help drive fronto-temporal coherence in TDC ( Brown et al , 2005 ; Chen et al , 2011 ; Budde et al , 2014 ; Sengupta and Nasir, 2015 ). Frontal pre-speech gamma power was observed in both FXS and TDC groups but was increased in the patient group.…”

“…Our electrophysiological findings in FXS have similarities with those in other disorders with prominent speech production deficits. For example, individuals who stutter demonstrate a profile of aberrant fronto-temporal connectivity prior to speech production and under-activation of auditory language regions following speech production ( Brown et al , 2005 ; Budde et al , 2014 ; Sengupta and Nasir, 2015 ). In autism spectrum disorder, reduced correlations between frontal and temporal cortex at rest have been documented and related to more severe expressive language impairments and autism spectrum disorder symptomatology ( Dinstein et al , 2012 ).…”

Cortical dynamics of disfluency in adults who stutter

“…The EEG signals were extracted using Matlab‐based EEGLAB toolbox (Delorme and Makeig ) and band‐pass filtered offline between 0.75 and 55 Hz using a second‐order Butterworth filter. All trial ERP epochs were then time aligned at the first TTL pulse of the production prompt and re‐referenced at electrode Afz (Sengupta and Nasir ). A time window of 2500 msec preceding the appearance of the production prompt was used for the analysis reported in this article.…”

“…Indeed, distinct theta‐gamma coherence patterns have been shown to accompany motor adaptation and speech motor training in fluent adults (Perfetti et al. ; Sengupta and Nasir , ). The functional roles of neural oscillations in different stages of speech planning and production are not, however, well‐understood even in fluent speakers.…”

Beta rhythm modulation by speech sounds: somatotopic mapping in somatosensory cortex

“…Compensatory changes occurring in feedback-altered speech are underpinned by the recruitment of a sensorimotor network 11 . Low-frequency brain oscillations might be responsible for signaling and orchestrating such compensatory mechanisms after prediction errors 12 , while a complex cross-frequency interplay subtends motor adaptation effects 13 , likely resembling adjustments in feedforward models 14 .…”