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Differential contributions of synaptic and intrinsic inhibitory currents to speech segmentation via flexible phase-locking in neural oscillators

Current hypotheses suggest that speech segmentation—the initial division and grouping of the speech stream into candidate phrases, syllables, and phonemes for further linguistic processing—is executed by a hierarchy of oscillators in auditory cortex. Theta (∼3-12 Hz) rhythms play a key role by phase...

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Autores principales: Pittman-Polletta, Benjamin R., Wang, Yangyang, Stanley, David A., Schroeder, Charles E., Whittington, Miles A., Kopell, Nancy J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8104450/
https://www.ncbi.nlm.nih.gov/pubmed/33852573
http://dx.doi.org/10.1371/journal.pcbi.1008783
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author Pittman-Polletta, Benjamin R.
Wang, Yangyang
Stanley, David A.
Schroeder, Charles E.
Whittington, Miles A.
Kopell, Nancy J.
author_facet Pittman-Polletta, Benjamin R.
Wang, Yangyang
Stanley, David A.
Schroeder, Charles E.
Whittington, Miles A.
Kopell, Nancy J.
author_sort Pittman-Polletta, Benjamin R.
collection PubMed
description Current hypotheses suggest that speech segmentation—the initial division and grouping of the speech stream into candidate phrases, syllables, and phonemes for further linguistic processing—is executed by a hierarchy of oscillators in auditory cortex. Theta (∼3-12 Hz) rhythms play a key role by phase-locking to recurring acoustic features marking syllable boundaries. Reliable synchronization to quasi-rhythmic inputs, whose variable frequency can dip below cortical theta frequencies (down to ∼1 Hz), requires “flexible” theta oscillators whose underlying neuronal mechanisms remain unknown. Using biophysical computational models, we found that the flexibility of phase-locking in neural oscillators depended on the types of hyperpolarizing currents that paced them. Simulated cortical theta oscillators flexibly phase-locked to slow inputs when these inputs caused both (i) spiking and (ii) the subsequent buildup of outward current sufficient to delay further spiking until the next input. The greatest flexibility in phase-locking arose from a synergistic interaction between intrinsic currents that was not replicated by synaptic currents at similar timescales. Flexibility in phase-locking enabled improved entrainment to speech input, optimal at mid-vocalic channels, which in turn supported syllabic-timescale segmentation through identification of vocalic nuclei. Our results suggest that synaptic and intrinsic inhibition contribute to frequency-restricted and -flexible phase-locking in neural oscillators, respectively. Their differential deployment may enable neural oscillators to play diverse roles, from reliable internal clocking to adaptive segmentation of quasi-regular sensory inputs like speech.
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spelling pubmed-81044502021-05-18 Differential contributions of synaptic and intrinsic inhibitory currents to speech segmentation via flexible phase-locking in neural oscillators Pittman-Polletta, Benjamin R. Wang, Yangyang Stanley, David A. Schroeder, Charles E. Whittington, Miles A. Kopell, Nancy J. PLoS Comput Biol Research Article Current hypotheses suggest that speech segmentation—the initial division and grouping of the speech stream into candidate phrases, syllables, and phonemes for further linguistic processing—is executed by a hierarchy of oscillators in auditory cortex. Theta (∼3-12 Hz) rhythms play a key role by phase-locking to recurring acoustic features marking syllable boundaries. Reliable synchronization to quasi-rhythmic inputs, whose variable frequency can dip below cortical theta frequencies (down to ∼1 Hz), requires “flexible” theta oscillators whose underlying neuronal mechanisms remain unknown. Using biophysical computational models, we found that the flexibility of phase-locking in neural oscillators depended on the types of hyperpolarizing currents that paced them. Simulated cortical theta oscillators flexibly phase-locked to slow inputs when these inputs caused both (i) spiking and (ii) the subsequent buildup of outward current sufficient to delay further spiking until the next input. The greatest flexibility in phase-locking arose from a synergistic interaction between intrinsic currents that was not replicated by synaptic currents at similar timescales. Flexibility in phase-locking enabled improved entrainment to speech input, optimal at mid-vocalic channels, which in turn supported syllabic-timescale segmentation through identification of vocalic nuclei. Our results suggest that synaptic and intrinsic inhibition contribute to frequency-restricted and -flexible phase-locking in neural oscillators, respectively. Their differential deployment may enable neural oscillators to play diverse roles, from reliable internal clocking to adaptive segmentation of quasi-regular sensory inputs like speech. Public Library of Science 2021-04-14 /pmc/articles/PMC8104450/ /pubmed/33852573 http://dx.doi.org/10.1371/journal.pcbi.1008783 Text en © 2021 Pittman-Polletta et al https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Pittman-Polletta, Benjamin R.
Wang, Yangyang
Stanley, David A.
Schroeder, Charles E.
Whittington, Miles A.
Kopell, Nancy J.
Differential contributions of synaptic and intrinsic inhibitory currents to speech segmentation via flexible phase-locking in neural oscillators
title Differential contributions of synaptic and intrinsic inhibitory currents to speech segmentation via flexible phase-locking in neural oscillators
title_full Differential contributions of synaptic and intrinsic inhibitory currents to speech segmentation via flexible phase-locking in neural oscillators
title_fullStr Differential contributions of synaptic and intrinsic inhibitory currents to speech segmentation via flexible phase-locking in neural oscillators
title_full_unstemmed Differential contributions of synaptic and intrinsic inhibitory currents to speech segmentation via flexible phase-locking in neural oscillators
title_short Differential contributions of synaptic and intrinsic inhibitory currents to speech segmentation via flexible phase-locking in neural oscillators
title_sort differential contributions of synaptic and intrinsic inhibitory currents to speech segmentation via flexible phase-locking in neural oscillators
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8104450/
https://www.ncbi.nlm.nih.gov/pubmed/33852573
http://dx.doi.org/10.1371/journal.pcbi.1008783
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