Cargando…

Detection of neuronal OFF periods as low amplitude neural activity segments

BACKGROUND: During non-rapid eye movement sleep (NREM), alternating periods of synchronised high (ON period) and low (OFF period) neuronal activity are associated with high amplitude delta band (0.5–4 Hz) oscillations in neocortical electrophysiological signals termed slow waves. As this oscillation...

Descripción completa

Detalles Bibliográficos
Autores principales: Harding, Christian D., Guillaumin, Mathilde C. C., Krone, Lukas B., Kahn, Martin C., Blanco-Duque, Cristina, Mikutta, Christian, Vyazovskiy, Vladyslav V.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9942432/
https://www.ncbi.nlm.nih.gov/pubmed/36809980
http://dx.doi.org/10.1186/s12868-023-00780-w
_version_ 1784891498980966400
author Harding, Christian D.
Guillaumin, Mathilde C. C.
Krone, Lukas B.
Kahn, Martin C.
Blanco-Duque, Cristina
Mikutta, Christian
Vyazovskiy, Vladyslav V.
author_facet Harding, Christian D.
Guillaumin, Mathilde C. C.
Krone, Lukas B.
Kahn, Martin C.
Blanco-Duque, Cristina
Mikutta, Christian
Vyazovskiy, Vladyslav V.
author_sort Harding, Christian D.
collection PubMed
description BACKGROUND: During non-rapid eye movement sleep (NREM), alternating periods of synchronised high (ON period) and low (OFF period) neuronal activity are associated with high amplitude delta band (0.5–4 Hz) oscillations in neocortical electrophysiological signals termed slow waves. As this oscillation is dependent crucially on hyperpolarisation of cortical cells, there is an interest in understanding how neuronal silencing during OFF periods leads to the generation of slow waves and whether this relationship changes between cortical layers. A formal, widely adopted definition of OFF periods is absent, complicating their detection. Here, we grouped segments of high frequency neural activity containing spikes, recorded as multiunit activity from the neocortex of freely behaving mice, on the basis of amplitude and asked whether the population of low amplitude (LA) segments displayed the expected characteristics of OFF periods. RESULTS: Average LA segment length was comparable to previous reports for OFF periods but varied considerably, from as short as 8 ms to > 1 s. LA segments were longer and occurred more frequently in NREM but shorter LA segments also occurred in half of rapid eye movement sleep (REM) epochs and occasionally during wakefulness. LA segments in all states were associated with a local field potential (LFP) slow wave that increased in amplitude with LA segment duration. We found that LA segments > 50 ms displayed a homeostatic rebound in incidence following sleep deprivation whereas short LA segments (< 50 ms) did not. The temporal organisation of LA segments was more coherent between channels located at a similar cortical depth. CONCLUSION: We corroborate previous studies showing neural activity signals contain uniquely identifiable periods of low amplitude with distinct characteristics from the surrounding signal known as OFF periods and attribute the new characteristics of vigilance-state-dependent duration and duration-dependent homeostatic response to this phenomenon. This suggests that ON/OFF periods are currently underdefined and that their appearance is less binary than previously considered, instead representing a continuum. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12868-023-00780-w.
format Online
Article
Text
id pubmed-9942432
institution National Center for Biotechnology Information
language English
publishDate 2023
publisher BioMed Central
record_format MEDLINE/PubMed
spelling pubmed-99424322023-02-22 Detection of neuronal OFF periods as low amplitude neural activity segments Harding, Christian D. Guillaumin, Mathilde C. C. Krone, Lukas B. Kahn, Martin C. Blanco-Duque, Cristina Mikutta, Christian Vyazovskiy, Vladyslav V. BMC Neurosci Research BACKGROUND: During non-rapid eye movement sleep (NREM), alternating periods of synchronised high (ON period) and low (OFF period) neuronal activity are associated with high amplitude delta band (0.5–4 Hz) oscillations in neocortical electrophysiological signals termed slow waves. As this oscillation is dependent crucially on hyperpolarisation of cortical cells, there is an interest in understanding how neuronal silencing during OFF periods leads to the generation of slow waves and whether this relationship changes between cortical layers. A formal, widely adopted definition of OFF periods is absent, complicating their detection. Here, we grouped segments of high frequency neural activity containing spikes, recorded as multiunit activity from the neocortex of freely behaving mice, on the basis of amplitude and asked whether the population of low amplitude (LA) segments displayed the expected characteristics of OFF periods. RESULTS: Average LA segment length was comparable to previous reports for OFF periods but varied considerably, from as short as 8 ms to > 1 s. LA segments were longer and occurred more frequently in NREM but shorter LA segments also occurred in half of rapid eye movement sleep (REM) epochs and occasionally during wakefulness. LA segments in all states were associated with a local field potential (LFP) slow wave that increased in amplitude with LA segment duration. We found that LA segments > 50 ms displayed a homeostatic rebound in incidence following sleep deprivation whereas short LA segments (< 50 ms) did not. The temporal organisation of LA segments was more coherent between channels located at a similar cortical depth. CONCLUSION: We corroborate previous studies showing neural activity signals contain uniquely identifiable periods of low amplitude with distinct characteristics from the surrounding signal known as OFF periods and attribute the new characteristics of vigilance-state-dependent duration and duration-dependent homeostatic response to this phenomenon. This suggests that ON/OFF periods are currently underdefined and that their appearance is less binary than previously considered, instead representing a continuum. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12868-023-00780-w. BioMed Central 2023-02-21 /pmc/articles/PMC9942432/ /pubmed/36809980 http://dx.doi.org/10.1186/s12868-023-00780-w Text en © The Author(s) 2023, corrected publication 2023 https://creativecommons.org/licenses/by/4.0/Open AccessThis 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 licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence 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 licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Harding, Christian D.
Guillaumin, Mathilde C. C.
Krone, Lukas B.
Kahn, Martin C.
Blanco-Duque, Cristina
Mikutta, Christian
Vyazovskiy, Vladyslav V.
Detection of neuronal OFF periods as low amplitude neural activity segments
title Detection of neuronal OFF periods as low amplitude neural activity segments
title_full Detection of neuronal OFF periods as low amplitude neural activity segments
title_fullStr Detection of neuronal OFF periods as low amplitude neural activity segments
title_full_unstemmed Detection of neuronal OFF periods as low amplitude neural activity segments
title_short Detection of neuronal OFF periods as low amplitude neural activity segments
title_sort detection of neuronal off periods as low amplitude neural activity segments
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9942432/
https://www.ncbi.nlm.nih.gov/pubmed/36809980
http://dx.doi.org/10.1186/s12868-023-00780-w
work_keys_str_mv AT hardingchristiand detectionofneuronaloffperiodsaslowamplitudeneuralactivitysegments
AT guillauminmathildecc detectionofneuronaloffperiodsaslowamplitudeneuralactivitysegments
AT kronelukasb detectionofneuronaloffperiodsaslowamplitudeneuralactivitysegments
AT kahnmartinc detectionofneuronaloffperiodsaslowamplitudeneuralactivitysegments
AT blancoduquecristina detectionofneuronaloffperiodsaslowamplitudeneuralactivitysegments
AT mikuttachristian detectionofneuronaloffperiodsaslowamplitudeneuralactivitysegments
AT vyazovskiyvladyslavv detectionofneuronaloffperiodsaslowamplitudeneuralactivitysegments