Journal article
Differential contributions of synaptic and intrinsic inhibitory currents to speech segmentation via flexible phase-locking in neural oscillators
PLoS computational biology, Vol.17(4), pp.e1008783-e1008783
04/2021
DOI: 10.1371/journal.pcbi.1008783
PMCID: PMC8104450
PMID: 33852573
Abstract
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.
Details
- Title: Subtitle
- Differential contributions of synaptic and intrinsic inhibitory currents to speech segmentation via flexible phase-locking in neural oscillators
- Creators
- Benjamin R Pittman-Polletta - Department of Mathematics & Statistics, Boston University, Boston, Massachusetts, United States of AmericaYangyang Wang - University of Iowa, MathematicsDavid A Stanley - Department of Mathematics & Statistics, Boston University, Boston, Massachusetts, United States of AmericaCharles E Schroeder - Translational Neuroscience Division, Center for Biomedical Imaging and Neuromodulation, Nathan S. Kline Institute for Psychiatric Research, Orangeburg, New York, United States of AmericaMiles A Whittington - Hull York Medical School, York, United KingdomNancy J Kopell - Department of Mathematics & Statistics, Boston University, Boston, Massachusetts, United States of America
- Resource Type
- Journal article
- Publication Details
- PLoS computational biology, Vol.17(4), pp.e1008783-e1008783
- DOI
- 10.1371/journal.pcbi.1008783
- PMID
- 33852573
- PMCID
- PMC8104450
- NLM abbreviation
- PLoS Comput Biol
- ISSN
- 1553-734X
- eISSN
- 1553-7358
- Grant note
- R01 MH111439 / NIMH NIH HHS Wellcome Trust P50 MH109429 / NIMH NIH HHS
- Language
- English
- Date published
- 04/2021
- Academic Unit
- Iowa Neuroscience Institute; Mathematics
- Record Identifier
- 9984070637202771
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