Cortical firing and sleep homeostasis
Vladyslav V Vyazovskiy, Umberto Olcese, Yaniv M Lazimy, Ugo Faraguna, Steve K Esser, Justin C Williams, Chiara Cirelli, Giulio Tononi, Vladyslav V Vyazovskiy, Umberto Olcese, Yaniv M Lazimy, Ugo Faraguna, Steve K Esser, Justin C Williams, Chiara Cirelli, Giulio Tononi
Abstract
The need to sleep grows with the duration of wakefulness and dissipates with time spent asleep, a process called sleep homeostasis. What are the consequences of staying awake on brain cells, and why is sleep needed? Surprisingly, we do not know whether the firing of cortical neurons is affected by how long an animal has been awake or asleep. Here, we found that after sustained wakefulness cortical neurons fire at higher frequencies in all behavioral states. During early NREM sleep after sustained wakefulness, periods of population activity (ON) are short, frequent, and associated with synchronous firing, while periods of neuronal silence are long and frequent. After sustained sleep, firing rates and synchrony decrease, while the duration of ON periods increases. Changes in firing patterns in NREM sleep correlate with changes in slow-wave activity, a marker of sleep homeostasis. Thus, the systematic increase of firing during wakefulness is counterbalanced by staying asleep.
Conflict of interest statement
COI statement: All authors indicated no financial conflicts of interest.
Figures
![Figure 1. Cortical activity in sleep and…](https://www.ncbi.nlm.nih.gov/pmc/articles/instance/2819325/bin/nihms173051f1.jpg)
![Figure 2. Effects of vigilance states on…](https://www.ncbi.nlm.nih.gov/pmc/articles/instance/2819325/bin/nihms173051f2.jpg)
![Figure 3. EEG slow wave amplitude is…](https://www.ncbi.nlm.nih.gov/pmc/articles/instance/2819325/bin/nihms173051f3.jpg)
![Figure 4. Homeostatic changes in the patterns…](https://www.ncbi.nlm.nih.gov/pmc/articles/instance/2819325/bin/nihms173051f4.jpg)
![Figure 5. Decreased synchrony between individual neurons…](https://www.ncbi.nlm.nih.gov/pmc/articles/instance/2819325/bin/nihms173051f5.jpg)
Figure 6. Effects of sleep/waking history on…
Figure 6. Effects of sleep/waking history on firing rates
(A) Top left: SWA time course…
Figure 7. Effects of sleep-wake history on…
Figure 7. Effects of sleep-wake history on the firing rates of different neuronal subtypes
(A)…
Figure 8. Effects of sleep deprivation on…
Figure 8. Effects of sleep deprivation on cortical firing
(A) SWA time course during the…
- Resting our cortices by going DOWN to sleep.Mignot E, Huguenard JR. Mignot E, et al. Neuron. 2009 Sep 24;63(6):719-21. doi: 10.1016/j.neuron.2009.09.008. Neuron. 2009. PMID: 19778500
- Local sleep in awake rats.Vyazovskiy VV, Olcese U, Hanlon EC, Nir Y, Cirelli C, Tononi G. Vyazovskiy VV, et al. Nature. 2011 Apr 28;472(7344):443-7. doi: 10.1038/nature10009. Nature. 2011. PMID: 21525926 Free PMC article.
- Why Does Sleep Slow-Wave Activity Increase After Extended Wake? Assessing the Effects of Increased Cortical Firing During Wake and Sleep.Rodriguez AV, Funk CM, Vyazovskiy VV, Nir Y, Tononi G, Cirelli C. Rodriguez AV, et al. J Neurosci. 2016 Dec 7;36(49):12436-12447. doi: 10.1523/JNEUROSCI.1614-16.2016. J Neurosci. 2016. PMID: 27927960 Free PMC article.
- The dynamics of cortical neuronal activity in the first minutes after spontaneous awakening in rats and mice.Vyazovskiy VV, Cui N, Rodriguez AV, Funk C, Cirelli C, Tononi G. Vyazovskiy VV, et al. Sleep. 2014 Aug 1;37(8):1337-47. doi: 10.5665/sleep.3926. Sleep. 2014. PMID: 25083014 Free PMC article.
- Cortical neuronal mechanisms of sleep homeostasis.Vyazovskiy VV. Vyazovskiy VV. Zh Vyssh Nerv Deiat Im I P Pavlova. 2013 Jan-Feb;63(1):13-23. doi: 10.7868/s0044467713010176. Zh Vyssh Nerv Deiat Im I P Pavlova. 2013. PMID: 23697219 Review.
- Infraslow coordination of slow wave activity through altered neuronal synchrony.Dash MB. Dash MB. Sleep. 2019 Dec 24;42(12):zsz170. doi: 10.1093/sleep/zsz170. Sleep. 2019. PMID: 31353415 Free PMC article.
- Sleep/wake changes in perturbational complexity in rats and mice.Cavelli ML, Mao R, Findlay G, Driessen K, Bugnon T, Tononi G, Cirelli C. Cavelli ML, et al. iScience. 2023 Feb 13;26(3):106186. doi: 10.1016/j.isci.2023.106186. eCollection 2023 Mar 17. iScience. 2023. PMID: 36895652 Free PMC article.
- Sleep loss diminishes hippocampal reactivation and replay.Diba K, Giri B, Kaya U, Maboudi K, Abel T. Diba K, et al. Res Sq. 2023 Feb 16:rs.3.rs-2540186. doi: 10.21203/rs.3.rs-2540186/v1. Preprint. Res Sq. 2023. PMID: 36824950 Free PMC article.
- Detection of neuronal OFF periods as low amplitude neural activity segments.Harding CD, Guillaumin MCC, Krone LB, Kahn MC, Blanco-Duque C, Mikutta C, Vyazovskiy VV. Harding CD, et al. BMC Neurosci. 2023 Feb 21;24(1):13. doi: 10.1186/s12868-023-00780-w. BMC Neurosci. 2023. PMID: 36809980 Free PMC article.
- Brain-derived neurotrophic factor Val66Met polymorphism modulates the effects of circadian desynchronization on activity and sleep in male mice.Phillips DJ, Blaine S, Wallace NK, Karatsoreos IN. Phillips DJ, et al. Front Neurosci. 2023 Jan 9;16:1013673. doi: 10.3389/fnins.2022.1013673. eCollection 2022. Front Neurosci. 2023. PMID: 36699530 Free PMC article.
- Remembering and forgetting in sleep: Selective synaptic plasticity during sleep driven by scaling factors Homer1a and Arc.Diering GH. Diering GH. Neurobiol Stress. 2022 Dec 31;22:100512. doi: 10.1016/j.ynstr.2022.100512. eCollection 2023 Jan. Neurobiol Stress. 2022. PMID: 36632309 Free PMC article.
- Research Support, N.I.H., Extramural
- Research Support, U.S. Gov't, Non-P.H.S.
- Action Potentials / physiology*
- Animals
- Behavior, Animal
- Brain Mapping
- Cerebral Cortex / cytology*
- Cerebral Cortex / physiology
- Computer Simulation
- Electroencephalography / methods
- Fourier Analysis
- Homeostasis / physiology*
- Male
- Models, Neurological
- Neurons / physiology*
- Polysomnography
- Rats
- Rats, Inbred WKY
- Signal Processing, Computer-Assisted
- Sleep / physiology*
- Sleep Deprivation / physiopathology
- Time Factors
- Wakefulness / physiology
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The PubMed wordmark and PubMed logo are registered trademarks of the U.S. Department of Health and Human Services (HHS). Unauthorized use of these marks is strictly prohibited.
National Library of Medicine
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![Figure 6. Effects of sleep/waking history on…](https://www.ncbi.nlm.nih.gov/pmc/articles/instance/2819325/bin/nihms173051f6.jpg)
Figure 7. Effects of sleep-wake history on…
Figure 7. Effects of sleep-wake history on the firing rates of different neuronal subtypes
(A)…
Figure 8. Effects of sleep deprivation on…
Figure 8. Effects of sleep deprivation on cortical firing
(A) SWA time course during the…
- Resting our cortices by going DOWN to sleep.Mignot E, Huguenard JR. Mignot E, et al. Neuron. 2009 Sep 24;63(6):719-21. doi: 10.1016/j.neuron.2009.09.008. Neuron. 2009. PMID: 19778500
- Local sleep in awake rats.Vyazovskiy VV, Olcese U, Hanlon EC, Nir Y, Cirelli C, Tononi G. Vyazovskiy VV, et al. Nature. 2011 Apr 28;472(7344):443-7. doi: 10.1038/nature10009. Nature. 2011. PMID: 21525926 Free PMC article.
- Why Does Sleep Slow-Wave Activity Increase After Extended Wake? Assessing the Effects of Increased Cortical Firing During Wake and Sleep.Rodriguez AV, Funk CM, Vyazovskiy VV, Nir Y, Tononi G, Cirelli C. Rodriguez AV, et al. J Neurosci. 2016 Dec 7;36(49):12436-12447. doi: 10.1523/JNEUROSCI.1614-16.2016. J Neurosci. 2016. PMID: 27927960 Free PMC article.
- The dynamics of cortical neuronal activity in the first minutes after spontaneous awakening in rats and mice.Vyazovskiy VV, Cui N, Rodriguez AV, Funk C, Cirelli C, Tononi G. Vyazovskiy VV, et al. Sleep. 2014 Aug 1;37(8):1337-47. doi: 10.5665/sleep.3926. Sleep. 2014. PMID: 25083014 Free PMC article.
- Cortical neuronal mechanisms of sleep homeostasis.Vyazovskiy VV. Vyazovskiy VV. Zh Vyssh Nerv Deiat Im I P Pavlova. 2013 Jan-Feb;63(1):13-23. doi: 10.7868/s0044467713010176. Zh Vyssh Nerv Deiat Im I P Pavlova. 2013. PMID: 23697219 Review.
- Infraslow coordination of slow wave activity through altered neuronal synchrony.Dash MB. Dash MB. Sleep. 2019 Dec 24;42(12):zsz170. doi: 10.1093/sleep/zsz170. Sleep. 2019. PMID: 31353415 Free PMC article.
- Sleep/wake changes in perturbational complexity in rats and mice.Cavelli ML, Mao R, Findlay G, Driessen K, Bugnon T, Tononi G, Cirelli C. Cavelli ML, et al. iScience. 2023 Feb 13;26(3):106186. doi: 10.1016/j.isci.2023.106186. eCollection 2023 Mar 17. iScience. 2023. PMID: 36895652 Free PMC article.
- Sleep loss diminishes hippocampal reactivation and replay.Diba K, Giri B, Kaya U, Maboudi K, Abel T. Diba K, et al. Res Sq. 2023 Feb 16:rs.3.rs-2540186. doi: 10.21203/rs.3.rs-2540186/v1. Preprint. Res Sq. 2023. PMID: 36824950 Free PMC article.
- Detection of neuronal OFF periods as low amplitude neural activity segments.Harding CD, Guillaumin MCC, Krone LB, Kahn MC, Blanco-Duque C, Mikutta C, Vyazovskiy VV. Harding CD, et al. BMC Neurosci. 2023 Feb 21;24(1):13. doi: 10.1186/s12868-023-00780-w. BMC Neurosci. 2023. PMID: 36809980 Free PMC article.
- Brain-derived neurotrophic factor Val66Met polymorphism modulates the effects of circadian desynchronization on activity and sleep in male mice.Phillips DJ, Blaine S, Wallace NK, Karatsoreos IN. Phillips DJ, et al. Front Neurosci. 2023 Jan 9;16:1013673. doi: 10.3389/fnins.2022.1013673. eCollection 2022. Front Neurosci. 2023. PMID: 36699530 Free PMC article.
- Remembering and forgetting in sleep: Selective synaptic plasticity during sleep driven by scaling factors Homer1a and Arc.Diering GH. Diering GH. Neurobiol Stress. 2022 Dec 31;22:100512. doi: 10.1016/j.ynstr.2022.100512. eCollection 2023 Jan. Neurobiol Stress. 2022. PMID: 36632309 Free PMC article.
- Research Support, N.I.H., Extramural
- Research Support, U.S. Gov't, Non-P.H.S.
- Action Potentials / physiology*
- Animals
- Behavior, Animal
- Brain Mapping
- Cerebral Cortex / cytology*
- Cerebral Cortex / physiology
- Computer Simulation
- Electroencephalography / methods
- Fourier Analysis
- Homeostasis / physiology*
- Male
- Models, Neurological
- Neurons / physiology*
- Polysomnography
- Rats
- Rats, Inbred WKY
- Signal Processing, Computer-Assisted
- Sleep / physiology*
- Sleep Deprivation / physiopathology
- Time Factors
- Wakefulness / physiology
- DP1 OD000579/OD/NIH HHS/United States
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- P20 MH077967-02/MH/NIMH NIH HHS/United States
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The PubMed wordmark and PubMed logo are registered trademarks of the U.S. Department of Health and Human Services (HHS). Unauthorized use of these marks is strictly prohibited.
National Library of Medicine
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Bethesda, MD 20894
![Figure 7. Effects of sleep-wake history on…](https://www.ncbi.nlm.nih.gov/pmc/articles/instance/2819325/bin/nihms173051f7.jpg)
Figure 8. Effects of sleep deprivation on…
Figure 8. Effects of sleep deprivation on cortical firing
(A) SWA time course during the…
- Resting our cortices by going DOWN to sleep.Mignot E, Huguenard JR. Mignot E, et al. Neuron. 2009 Sep 24;63(6):719-21. doi: 10.1016/j.neuron.2009.09.008. Neuron. 2009. PMID: 19778500
- Local sleep in awake rats.Vyazovskiy VV, Olcese U, Hanlon EC, Nir Y, Cirelli C, Tononi G. Vyazovskiy VV, et al. Nature. 2011 Apr 28;472(7344):443-7. doi: 10.1038/nature10009. Nature. 2011. PMID: 21525926 Free PMC article.
- Why Does Sleep Slow-Wave Activity Increase After Extended Wake? Assessing the Effects of Increased Cortical Firing During Wake and Sleep.Rodriguez AV, Funk CM, Vyazovskiy VV, Nir Y, Tononi G, Cirelli C. Rodriguez AV, et al. J Neurosci. 2016 Dec 7;36(49):12436-12447. doi: 10.1523/JNEUROSCI.1614-16.2016. J Neurosci. 2016. PMID: 27927960 Free PMC article.
- The dynamics of cortical neuronal activity in the first minutes after spontaneous awakening in rats and mice.Vyazovskiy VV, Cui N, Rodriguez AV, Funk C, Cirelli C, Tononi G. Vyazovskiy VV, et al. Sleep. 2014 Aug 1;37(8):1337-47. doi: 10.5665/sleep.3926. Sleep. 2014. PMID: 25083014 Free PMC article.
- Cortical neuronal mechanisms of sleep homeostasis.Vyazovskiy VV. Vyazovskiy VV. Zh Vyssh Nerv Deiat Im I P Pavlova. 2013 Jan-Feb;63(1):13-23. doi: 10.7868/s0044467713010176. Zh Vyssh Nerv Deiat Im I P Pavlova. 2013. PMID: 23697219 Review.
- Infraslow coordination of slow wave activity through altered neuronal synchrony.Dash MB. Dash MB. Sleep. 2019 Dec 24;42(12):zsz170. doi: 10.1093/sleep/zsz170. Sleep. 2019. PMID: 31353415 Free PMC article.
- Sleep/wake changes in perturbational complexity in rats and mice.Cavelli ML, Mao R, Findlay G, Driessen K, Bugnon T, Tononi G, Cirelli C. Cavelli ML, et al. iScience. 2023 Feb 13;26(3):106186. doi: 10.1016/j.isci.2023.106186. eCollection 2023 Mar 17. iScience. 2023. PMID: 36895652 Free PMC article.
- Sleep loss diminishes hippocampal reactivation and replay.Diba K, Giri B, Kaya U, Maboudi K, Abel T. Diba K, et al. Res Sq. 2023 Feb 16:rs.3.rs-2540186. doi: 10.21203/rs.3.rs-2540186/v1. Preprint. Res Sq. 2023. PMID: 36824950 Free PMC article.
- Detection of neuronal OFF periods as low amplitude neural activity segments.Harding CD, Guillaumin MCC, Krone LB, Kahn MC, Blanco-Duque C, Mikutta C, Vyazovskiy VV. Harding CD, et al. BMC Neurosci. 2023 Feb 21;24(1):13. doi: 10.1186/s12868-023-00780-w. BMC Neurosci. 2023. PMID: 36809980 Free PMC article.
- Brain-derived neurotrophic factor Val66Met polymorphism modulates the effects of circadian desynchronization on activity and sleep in male mice.Phillips DJ, Blaine S, Wallace NK, Karatsoreos IN. Phillips DJ, et al. Front Neurosci. 2023 Jan 9;16:1013673. doi: 10.3389/fnins.2022.1013673. eCollection 2022. Front Neurosci. 2023. PMID: 36699530 Free PMC article.
- Remembering and forgetting in sleep: Selective synaptic plasticity during sleep driven by scaling factors Homer1a and Arc.Diering GH. Diering GH. Neurobiol Stress. 2022 Dec 31;22:100512. doi: 10.1016/j.ynstr.2022.100512. eCollection 2023 Jan. Neurobiol Stress. 2022. PMID: 36632309 Free PMC article.
- Research Support, N.I.H., Extramural
- Research Support, U.S. Gov't, Non-P.H.S.
- Action Potentials / physiology*
- Animals
- Behavior, Animal
- Brain Mapping
- Cerebral Cortex / cytology*
- Cerebral Cortex / physiology
- Computer Simulation
- Electroencephalography / methods
- Fourier Analysis
- Homeostasis / physiology*
- Male
- Models, Neurological
- Neurons / physiology*
- Polysomnography
- Rats
- Rats, Inbred WKY
- Signal Processing, Computer-Assisted
- Sleep / physiology*
- Sleep Deprivation / physiopathology
- Time Factors
- Wakefulness / physiology
- DP1 OD000579/OD/NIH HHS/United States
- DP1 OD000579-01/OD/NIH HHS/United States
- P20 MH077967-02/MH/NIMH NIH HHS/United States
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![Figure 8. Effects of sleep deprivation on…](https://www.ncbi.nlm.nih.gov/pmc/articles/instance/2819325/bin/nihms173051f8.jpg)
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