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Spatiotemporal Analysis of Local Field Potentials and Unit Discharges in Cat Cerebral Cortex during Natural Wake and Sleep States
Open accessAbstract
The electroencephalogram displays various oscillation patterns during wake and sleep states, but their spatiotemporal distribution is not completely known. Local field potentials (LFPs) and multiunits were recorded simultaneously in the cerebral cortex (areas 5-7) of naturally sleeping and awake cats. Slow-wave sleep (SWS) was characterized by oscillations in the slow (<1 Hz) and delta (1-4 Hz) frequency range. The high-amplitude slow-wave complexes consisted in a positivity of depth LFP, associated with neuronal silence, followed by a sharp LFP negativity, correlated with an increase of firing. This pattern was of remarkable spatiotemporal coherence, because silences and increased firing occurred simultaneously in units recorded within a 7 mm distance in the cortex. During wake and rapid-eye-movement (REM) sleep, single units fired tonically, whereas LFPs displayed low-amplitude fast activities with increased power in fast frequencies (15-75 Hz). In contrast with the widespread synchronization during SWS, fast oscillations during REM and wake periods were synchronized only within neighboring electrodes and small time windows (100-500 msec). This local synchrony occurred in an apparent irregular manner, both spatially and temporally. Brief periods (<1 sec) of fast oscillations were also present during SWS in between slow-wave complexes. During these brief periods, the spatial and temporal coherence, as well as the relation between units and LFPs, was identical to that of fast oscillations of wake or REM sleep. These results show that natural SWS in cats is characterized by slow-wave complexes, synchronized over large cortical territories, interleaved with brief periods of fast oscillations, characterized by local synchrony, and of characteristics similar to that of the sustained fast oscillations of activated states.
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“In the scalp EEG, the negative peak of the slow oscillation coincides with the beginning of the down-to-up state transition (281, 993, 1261), whereas the depolarizing phase of sustained firing corre-lates with the positive EEG deflection (33,998,1268).”
From About Sleep's Role in Memory (2013) · cites this paper as [281]
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“Internal brain state can fluctuate even in the absence of overt behavioral changes – most notably in the well-characterized transitions between sleep and waking and within different stages of sleep.”
From Waking state: rapid variations modulate neural and behavioral responses (2015) · cites this paper as Destexhe et al., 1999
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“Falling asleep, or moving from slow wave sleep into rapid eye movement sleep, results in profound changes in the operation of the brain (Figure 1), including changes in spontaneous activity, the ability to execute motor commands, responses to sensory stimuli and the fidelity of internal representations of the world”
From Waking state: rapid variations modulate neural and behavioral responses (2015) · cites this paper as Destexhe et al., 1999
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“Gain modulation mechanisms are also robustly engaged by changes in internal state32–35.”
From Mechanisms underlying gain modulation in the cortex (2020) · cites this paper as [34]
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Metadata
- Authors
- Destexhe, A., Contreras, D., & Steriade, M.
- Affiliations
- Université Laval (CA)
- ORCID
- Contreras, Diego
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 1999-06-01
- Volume
- 19
- Issue
- 11
- Pages
- 4595-4608
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6782626
- OpenAlex
- W2146493929
- Cited by
- 573
- References
- 49
- Citations by year
- 2026: 5 · 2025: 9 · 2024: 13 · 2023: 35 · 2022: 20 · 2021: 19 · 2020: 18 · 2019: 29 · 2018: 17 · 2017: 21 · 2016: 25 · 2015: 35 · 2014: 34 · 2013: 24 · 2012: 20
- FWCI
- 7.04
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- HAL (submittedVersion)
- Funders
- Medical Research Council Canada
- Medical Research Council
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Sleep and Wakefulness Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- local field potentials, single-unit activity, slow-wave sleep, REM sleep, wakefulness, cortical synchronization, spatiotemporal coherence, fast oscillations, cat cerebral cortex, sleep oscillations
- MeSH terms
- Animals, Brain Mapping, Cats, Cortical Synchronization, Electroencephalography, Membrane Potentials, Neurons, Oscillometry, Sleep, Wakefulness
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