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Neural oscillatory correlates of speech auditory-motor integration in the cortex of healthy individuals and patients with schizophrenia

Abstract

The nature of the integration of auditory and motor processes in the brain has been a subject of long-standing interest in the cognitive sciences and neuroscience(Price, 2012). Dysfunction in auditory-motor integration underlies pathology in a wide range of disease processes including stroke, stuttering, dyslexia, and neuropsychiatric disorders such as schizophrenia. Understanding the functional integration of the neural circuits that subserve the different stages of auditory-motor transformation and coordination remains a major challenge in both basic and clinical human systems neuroscience.

Here, we report on the neural oscillatory correlates of speech auditory encoding, working memory and verbal reproduction (the "phonological loop") in healthy human subjects, and schizophrenic patients both before and after computerized cognitive training. We present a high-resolution spatiotemporal description of the brain network that supports the functions of the phonological loop in the healthy subjects, show the aberrant behavior of this network in schizophrenia, reveal novel compensatory mechanisms deployed in the cortex in schizophrenics, and show how some of the significant abnormalities are normalized through cognitive training.

In the healthy subjects, we demonstrate that Area Spt and Broca's Area act as dissociable input and output buffers in a reverberating bi-directional dorsal stream for phoneme perception and production. These buffers interact in time along a tightly controlled schedule as part of a speech-motor feedback loop that operates before speech onset. In the schizophrenic patients, we find that the normal dorsal stream pathway is disrupted, and that schizophrenics activate the ventral visual stream in compensation, and in particular the visual word form area (VWFA), in a manner mediated by an overall suppressed dorsal lateral prefrontal cortex, the activity level of which in turn correlated with overall patient functional status. Both the posterior dorsal stream deficits and the VWFA compensation are greater in patients with severe auditory hallucinations, reflecting the significant underlying lesion to the auditory-motor system in these patients. Finally, we demonstrate that computerized cognitive training acts to normalize the oscillatory deficits of the dorsal stream and that this normalization correlates with improvements in both task performance and long-term verbal learning and memory scores.

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