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Reduced neural feedback signaling despite robust neuron and gamma auditory responses during human sleep

During sleep, sensory stimuli rarely trigger a behavioral response or conscious perception. However, it remains unclear whether sleep inhibits specific aspects of sensory processing, such as feedforward or feedback signaling. Here, we presented auditory stimuli (for example, click-trains, words, mus...

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Autores principales: Hayat, Hanna, Marmelshtein, Amit, Krom, Aaron J., Sela, Yaniv, Tankus, Ariel, Strauss, Ido, Fahoum, Firas, Fried, Itzhak, Nir, Yuval
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group US 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9276533/
https://www.ncbi.nlm.nih.gov/pubmed/35817847
http://dx.doi.org/10.1038/s41593-022-01107-4
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author Hayat, Hanna
Marmelshtein, Amit
Krom, Aaron J.
Sela, Yaniv
Tankus, Ariel
Strauss, Ido
Fahoum, Firas
Fried, Itzhak
Nir, Yuval
author_facet Hayat, Hanna
Marmelshtein, Amit
Krom, Aaron J.
Sela, Yaniv
Tankus, Ariel
Strauss, Ido
Fahoum, Firas
Fried, Itzhak
Nir, Yuval
author_sort Hayat, Hanna
collection PubMed
description During sleep, sensory stimuli rarely trigger a behavioral response or conscious perception. However, it remains unclear whether sleep inhibits specific aspects of sensory processing, such as feedforward or feedback signaling. Here, we presented auditory stimuli (for example, click-trains, words, music) during wakefulness and sleep in patients with epilepsy, while recording neuronal spiking, microwire local field potentials, intracranial electroencephalogram and polysomnography. Auditory stimuli induced robust and selective spiking and high-gamma (80–200 Hz) power responses across the lateral temporal lobe during both non-rapid eye movement (NREM) and rapid eye movement (REM) sleep. Sleep only moderately attenuated response magnitudes, mainly affecting late responses beyond early auditory cortex and entrainment to rapid click-trains in NREM sleep. By contrast, auditory-induced alpha–beta (10–30 Hz) desynchronization (that is, decreased power), prevalent in wakefulness, was strongly reduced in sleep. Thus, extensive auditory responses persist during sleep whereas alpha–beta power decrease, likely reflecting neural feedback processes, is deficient. More broadly, our findings suggest that feedback signaling is key to conscious sensory processing.
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spelling pubmed-92765332022-07-14 Reduced neural feedback signaling despite robust neuron and gamma auditory responses during human sleep Hayat, Hanna Marmelshtein, Amit Krom, Aaron J. Sela, Yaniv Tankus, Ariel Strauss, Ido Fahoum, Firas Fried, Itzhak Nir, Yuval Nat Neurosci Article During sleep, sensory stimuli rarely trigger a behavioral response or conscious perception. However, it remains unclear whether sleep inhibits specific aspects of sensory processing, such as feedforward or feedback signaling. Here, we presented auditory stimuli (for example, click-trains, words, music) during wakefulness and sleep in patients with epilepsy, while recording neuronal spiking, microwire local field potentials, intracranial electroencephalogram and polysomnography. Auditory stimuli induced robust and selective spiking and high-gamma (80–200 Hz) power responses across the lateral temporal lobe during both non-rapid eye movement (NREM) and rapid eye movement (REM) sleep. Sleep only moderately attenuated response magnitudes, mainly affecting late responses beyond early auditory cortex and entrainment to rapid click-trains in NREM sleep. By contrast, auditory-induced alpha–beta (10–30 Hz) desynchronization (that is, decreased power), prevalent in wakefulness, was strongly reduced in sleep. Thus, extensive auditory responses persist during sleep whereas alpha–beta power decrease, likely reflecting neural feedback processes, is deficient. More broadly, our findings suggest that feedback signaling is key to conscious sensory processing. Nature Publishing Group US 2022-07-11 2022 /pmc/articles/PMC9276533/ /pubmed/35817847 http://dx.doi.org/10.1038/s41593-022-01107-4 Text en © The Author(s) 2022, corrected publication 2022 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Hayat, Hanna
Marmelshtein, Amit
Krom, Aaron J.
Sela, Yaniv
Tankus, Ariel
Strauss, Ido
Fahoum, Firas
Fried, Itzhak
Nir, Yuval
Reduced neural feedback signaling despite robust neuron and gamma auditory responses during human sleep
title Reduced neural feedback signaling despite robust neuron and gamma auditory responses during human sleep
title_full Reduced neural feedback signaling despite robust neuron and gamma auditory responses during human sleep
title_fullStr Reduced neural feedback signaling despite robust neuron and gamma auditory responses during human sleep
title_full_unstemmed Reduced neural feedback signaling despite robust neuron and gamma auditory responses during human sleep
title_short Reduced neural feedback signaling despite robust neuron and gamma auditory responses during human sleep
title_sort reduced neural feedback signaling despite robust neuron and gamma auditory responses during human sleep
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9276533/
https://www.ncbi.nlm.nih.gov/pubmed/35817847
http://dx.doi.org/10.1038/s41593-022-01107-4
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