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      Neural Oscillations Carry Speech Rhythm through to Comprehension

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          Abstract

          A key feature of speech is the quasi-regular rhythmic information contained in its slow amplitude modulations. In this article we review the information conveyed by speech rhythm, and the role of ongoing brain oscillations in listeners’ processing of this content. Our starting point is the fact that speech is inherently temporal, and that rhythmic information conveyed by the amplitude envelope contains important markers for place and manner of articulation, segmental information, and speech rate. Behavioral studies demonstrate that amplitude envelope information is relied upon by listeners and plays a key role in speech intelligibility. Extending behavioral findings, data from neuroimaging – particularly electroencephalography (EEG) and magnetoencephalography (MEG) – point to phase locking by ongoing cortical oscillations to low-frequency information (~4–8 Hz) in the speech envelope. This phase modulation effectively encodes a prediction of when important events (such as stressed syllables) are likely to occur, and acts to increase sensitivity to these relevant acoustic cues. We suggest a framework through which such neural entrainment to speech rhythm can explain effects of speech rate on word and segment perception (i.e., that the perception of phonemes and words in connected speech is influenced by preceding speech rate). Neuroanatomically, acoustic amplitude modulations are processed largely bilaterally in auditory cortex, with intelligible speech resulting in differential recruitment of left-hemisphere regions. Notable among these is lateral anterior temporal cortex, which we propose functions in a domain-general fashion to support ongoing memory and integration of meaningful input. Together, the reviewed evidence suggests that low-frequency oscillations in the acoustic speech signal form the foundation of a rhythmic hierarchy supporting spoken language, mirrored by phase-locked oscillations in the human brain.

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          Most cited references81

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          Dynamic predictions: oscillations and synchrony in top-down processing.

          Classical theories of sensory processing view the brain as a passive, stimulus-driven device. By contrast, more recent approaches emphasize the constructive nature of perception, viewing it as an active and highly selective process. Indeed, there is ample evidence that the processing of stimuli is controlled by top-down influences that strongly shape the intrinsic dynamics of thalamocortical networks and constantly create predictions about forthcoming sensory events. We discuss recent experiments indicating that such predictions might be embodied in the temporal structure of both stimulus-evoked and ongoing activity, and that synchronous oscillations are particularly important in this process. Coherence among subthreshold membrane potential fluctuations could be exploited to express selective functional relationships during states of expectancy or attention, and these dynamic patterns could allow the grouping and selection of distributed neuronal responses for further processing.
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            The phase of ongoing EEG oscillations predicts visual perception.

            Oscillations are ubiquitous in electrical recordings of brain activity. While the amplitude of ongoing oscillatory activity is known to correlate with various aspects of perception, the influence of oscillatory phase on perception remains unknown. In particular, since phase varies on a much faster timescale than the more sluggish amplitude fluctuations, phase effects could reveal the fine-grained neural mechanisms underlying perception. We presented brief flashes of light at the individual luminance threshold while EEG was recorded. Although the stimulus on each trial was identical, subjects detected approximately half of the flashes (hits) and entirely missed the other half (misses). Phase distributions across trials were compared between hits and misses. We found that shortly before stimulus onset, each of the two distributions exhibited significant phase concentration, but at different phase angles. This effect was strongest in the theta and alpha frequency bands. In this time-frequency range, oscillatory phase accounted for at least 16% of variability in detection performance and allowed the prediction of performance on the single-trial level. This finding indicates that the visual detection threshold fluctuates over time along with the phase of ongoing EEG activity. The results support the notion that ongoing oscillations shape our perception, possibly by providing a temporal reference frame for neural codes that rely on precise spike timing.
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              The temporal structures and functional significance of scale-free brain activity.

              Scale-free dynamics, with a power spectrum following P proportional to f(-beta), are an intrinsic feature of many complex processes in nature. In neural systems, scale-free activity is often neglected in electrophysiological research. Here, we investigate scale-free dynamics in human brain and show that it contains extensive nested frequencies, with the phase of lower frequencies modulating the amplitude of higher frequencies in an upward progression across the frequency spectrum. The functional significance of scale-free brain activity is indicated by task performance modulation and regional variation, with beta being larger in default network and visual cortex and smaller in hippocampus and cerebellum. The precise patterns of nested frequencies in the brain differ from other scale-free dynamics in nature, such as earth seismic waves and stock market fluctuations, suggesting system-specific generative mechanisms. Our findings reveal robust temporal structures and behavioral significance of scale-free brain activity and should motivate future study on its physiological mechanisms and cognitive implications. Copyright 2010 Elsevier Inc. All rights reserved.

                Author and article information

                Journal
                Front Psychol
                Front Psychol
                Front. Psychology
                Frontiers in Psychology
                Frontiers Research Foundation
                1664-1078
                06 September 2012
                2012
                : 3
                : 320
                Affiliations
                [1] 1simpleCenter for Cognitive Neuroscience and Department of Neurology, University of Pennsylvania Philadelphia, PA, USA
                [2] 2simpleMedical Research Council Cognition and Brain Sciences Unit Cambridge, UK
                Author notes

                Edited by: Lucia Melloni, Max Planck Institute for Brain Research, Germany

                Reviewed by: David Poeppel, New York University, USA; Jonas Obleser, Max Planck Institute for Human Cognitive and Brain Sciences, Germany

                *Correspondence: Jonathan E. Peelle, Department of Neurology, University of Pennsylvania, 3400 Spruce Street, Philadelphia, PA 19104, USA. e-mail: peelle@ 123456gmail.com ; Matthew H. Davis, Cognition and Brain Sciences Unit, Medical Research Council, 15 Chaucer Road, Cambridge CB2 7EF, UK. e-mail: matt.davis@ 123456mrc-cbu.cam.ac.uk

                This article was submitted to Frontiers in Language Sciences, a specialty of Frontiers in Psychology.

                Article
                10.3389/fpsyg.2012.00320
                3434440
                22973251
                15a98b52-8c45-43ab-9d88-18ae847445a0
                Copyright © 2012 Peelle and Davis.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in other forums, provided the original authors and source are credited and subject to any copyright notices concerning any third-party graphics etc.

                History
                : 05 April 2012
                : 11 August 2012
                Page count
                Figures: 8, Tables: 1, Equations: 0, References: 137, Pages: 17, Words: 14521
                Categories
                Psychology
                Review Article

                Clinical Psychology & Psychiatry
                theta,speech comprehension,intelligibility,oscillations,speech rate,language,phase locking

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