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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 references 128

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          Neuronal oscillations in cortical networks.

          Clocks tick, bridges and skyscrapers vibrate, neuronal networks oscillate. Are neuronal oscillations an inevitable by-product, similar to bridge vibrations, or an essential part of the brain's design? Mammalian cortical neurons form behavior-dependent oscillating networks of various sizes, which span five orders of magnitude in frequency. These oscillations are phylogenetically preserved, suggesting that they are functionally relevant. Recent findings indicate that network oscillations bias input selection, temporally link neurons into assemblies, and facilitate synaptic plasticity, mechanisms that cooperatively support temporal representation and long-term consolidation of information.
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            A mechanism for cognitive dynamics: neuronal communication through neuronal coherence.

             Pascal Fries (2005)
            At any one moment, many neuronal groups in our brain are active. Microelectrode recordings have characterized the activation of single neurons and fMRI has unveiled brain-wide activation patterns. Now it is time to understand how the many active neuronal groups interact with each other and how their communication is flexibly modulated to bring about our cognitive dynamics. I hypothesize that neuronal communication is mechanistically subserved by neuronal coherence. Activated neuronal groups oscillate and thereby undergo rhythmic excitability fluctuations that produce temporal windows for communication. Only coherently oscillating neuronal groups can interact effectively, because their communication windows for input and for output are open at the same times. Thus, a flexible pattern of coherence defines a flexible communication structure, which subserves our cognitive flexibility.
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              The cortical organization of speech processing.

              Despite decades of research, the functional neuroanatomy of speech processing has been difficult to characterize. A major impediment to progress may have been the failure to consider task effects when mapping speech-related processing systems. We outline a dual-stream model of speech processing that remedies this situation. In this model, a ventral stream processes speech signals for comprehension, and a dorsal stream maps acoustic speech signals to frontal lobe articulatory networks. The model assumes that the ventral stream is largely bilaterally organized--although there are important computational differences between the left- and right-hemisphere systems--and that the dorsal stream is strongly left-hemisphere dominant.
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                Author and article information

                Journal
                Front Psychol
                Front Psychol
                Front. Psychology
                Frontiers in Psychology
                Frontiers Research Foundation
                1664-1078
                06 September 2012
                2012
                : 3
                Affiliations
                1simpleCenter for Cognitive Neuroscience and Department of Neurology, University of Pennsylvania Philadelphia, PA, USA
                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
                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.

                Counts
                Figures: 8, Tables: 1, Equations: 0, References: 137, Pages: 17, Words: 14521
                Categories
                Psychology
                Review Article

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