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Unilateral Cortical Spreading Depression Affects Sleep Need and Induces Molecular and Electrophysiological Signs of Synaptic Potentiation In Vivo

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Faraguna, U., Nelson, A., Vyazovskiy, V. V., Cirelli, C., Tononi, G.·2010·Cerebral Cortex

Abstract

Cortical spreading depression (CSD) is an electrophysiological phenomenon first described by Leao in 1944 as a suppression of spontaneous electroencephalographic activity, traveling across the cerebral cortex. In vitro studies suggest that CSD may induce synaptic potentiation. One recent study also found that CSD is followed by a non-rapid eye movement (NREM) sleep duration increase, suggesting an increased need for sleep. Recent experiments in animals and humans show that the occurrence of synaptic potentiation increases subsequent sleep need as measured by larger slow wave activity (SWA) during NREM sleep, prompting the question whether CSD can affect NREM SWA. Here, we find that, in freely moving rats, local CSD induction increases corticocortical evoked responses and strongly induces brain derived neurotrophic factor (BDNF) in the affected cortical hemisphere but not in the contralateral one, consistent with synaptic potentiation in vivo. Moreover, for several hours after CSD, large slow waves occur in the affected hemisphere during rapid eye movement sleep and quiet waking but disappear during active exploration. Finally, we find that CSD increases NREM sleep duration and SWA, the latter specifically in the affected hemisphere. These effects are consistent with an increase in synaptic strength triggered by CSD, although nonphysiological phenomena associated with CSD may also play a role.

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  • Procedures assumed to induce local net increases in synaptic potentiation (e.g., the cortical application of BDNF and KCl) induced cortical spreading depression and increased SWA during subsequent sleep, whereas BDNF receptor inhibition decreased SWA.

    “Procedures assumed to induce local net increases in synaptic potentiation (e.g., the cortical application of BDNF and KCl) induced cortical spreading depression (81) and increased SWA during subsequent sleep, whereas BDNF receptor inhibition decreased SWA (366,367).”

    From About Sleep's Role in Memory (2013) · cites this paper as [366]

    The Experimental Design and Results passages report that cortical KCl infusion induced CSD in rats, and the Results report increased SWA afterward. The Introduction describes cortical BDNF application as increasing SWA, but does not say it induced CSD; that part of the wording is not supported by this source. The receptor-inhibition statement is attached to other citations, not this one. (LLM, conf=0.86)

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  • About Sleep's Role in Memory

    Rasch, B., & Born, J. (2013) · Physiological Reviews · doi:10.1152/physrev.00032.2012 · Cited by 2,783 · see citing works

    “SWS is hallmarked by slow high-amplitude EEG oscillations (slow wave activity, SWA), whereas REM sleep (also termed paradoxical sleep) is Physiol Rev 93: 681–766, 2013 doi:10.1152/physrev.00032.2012 6810031-9333/13 Copyright © 2013 the American Physiological Society by 10.220.32.247 on O ctober 25, 2016 http://physrev…”
    BackgroundInfluential

Authors
Faraguna, U., Nelson, A., Vyazovskiy, V. V., Cirelli, C., & Tononi, G.
Affiliations
University of Wisconsin–Madison (US)
Venue
Cerebral Cortex
Published
2010-03-26
Volume
20
Issue
12
Pages
2939-2947
ISSN
  • 1047-3211 (ISSN-L)
  • 1460-2199
OpenAlex
W2152103539
Cited by
54
References
58
Citations by year
2026: 4 · 2025: 2 · 2024: 4 · 2023: 3 · 2022: 2 · 2021: 3 · 2020: 3 · 2019: 3 · 2018: 4 · 2017: 6 · 2016: 2 · 2015: 1 · 2014: 6 · 2013: 5 · 2012: 4
FWCI
2.13
Type
journal article
Language
en
Open access
Locations
  • Cerebral Cortex (publishedVersion)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
  • Open Research (University of Surrey) (submittedVersion)
  • CINECA IRIS Institutial research information system (University of Pisa) (submittedVersion)
  • Surrey Research Insight Open Access (The University of Surrey) (submittedVersion)
Funders
  • National Institutes of Health (5p20mh077967-04, DP1OD000579)
  • National Institute of Mental Health (P20MH-077967)
Topics
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Sleep and Wakefulness Research
  • Health Sciences › Medicine › Psychiatry and Mental health › Migraine and Headache Studies
  • Health Sciences › Medicine › Neurology › Traumatic Brain Injury and Neurovascular Disturbances
Keywords
cortical spreading depression, sleep need, synaptic potentiation, slow-wave activity, brain-derived neurotrophic factor, REM sleep, sleep homeostasis, rats
MeSH terms
Animals, Electroencephalography, Male, Neuronal Plasticity, Rats, Inbred WKY, Sleep, Cortical Spreading Depression, Gene Expression, Genes, Immediate-Early, Reverse Transcriptase Polymerase Chain Reaction, Rats

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