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J Neurosci. 2018 Nov 14;38(46):9989-10001. doi: 10.1523/JNEUROSCI.0476-18.2018. Epub 2018 Sep 21.

Theta Bursts Precede, and Spindles Follow, Cortical and Thalamic Downstates in Human NREM Sleep.

Author information

1
Department of Neurosciences, University of California San Diego, La Jolla, California 92093, cegonzalez@ucsd.edu.
2
University California Berkeley, Berkeley, California 94720.
3
Department of Neurosciences, University of California San Diego, La Jolla, California 92093.
4
Department of Neurology, Massachusetts General Hospital and Harvard Medical School, Harvard University, Boston, Massachusetts 02114.
5
Aix-Marseille Université, Marseille 13385, France.
6
Central Integration of Pain, Lyon Neuroscience Research Center, INSERM, U1028, CNRS, UMR5292, Université Claude Bernard, Lyon, Bron, France, and.
7
Departments of Radiology and Neurosciences, University of California, San Diego, California 92093.

Abstract

Since their discovery, slow oscillations have been observed to group spindles during non-REM sleep. Previous studies assert that the slow-oscillation downstate (DS) is preceded by slow spindles (10-12 Hz) and followed by fast spindles (12-16 Hz). Here, using both direct transcortical recordings in patients with intractable epilepsy (n = 10, 8 female), as well as scalp EEG recordings from a healthy cohort (n = 3, 1 female), we find in multiple cortical areas that both slow and fast spindles follow the DS. Although discrete oscillations do precede DSs, they are theta bursts (TBs) centered at 5-8 Hz. TBs were more pronounced for DSs in NREM stage 2 (N2) sleep compared with N3. TB with similar properties occur in the thalamus, but unlike spindles they have no clear temporal relationship with cortical TB. These differences in corticothalamic dynamics, as well as differences between spindles and theta in coupling high-frequency content, are consistent with NREM theta having separate generative mechanisms from spindles. The final inhibitory cycle of the TB coincides with the DS peak, suggesting that in N2, TB may help trigger the DS. Since the transition to N1 is marked by the appearance of theta, and the transition to N2 by the appearance of DS and thus spindles, a role of TB in triggering DS could help explain the sequence of electrophysiological events characterizing sleep. Finally, the coordinated appearance of spindles and DSs are implicated in memory consolidation processes, and the current findings redefine their temporal coupling with theta during NREM sleep.SIGNIFICANCE STATEMENT Sleep is characterized by large slow waves which modulate brain activity. Prominent among these are downstates (DSs), periods of a few tenths of a second when most cells stop firing, and spindles, oscillations at ∼12 times a second lasting for ∼a second. In this study, we provide the first detailed description of another kind of sleep wave: theta bursts (TBs), a brief oscillation at ∼six cycles per second. We show, recording during natural sleep directly from the human cortex and thalamus, as well as on the scalp, that TBs precede, and spindles follow DSs. TBs may help trigger DSs in some circumstances, and could organize cortical and thalamic activity so that memories can be consolidated during sleep.

KEYWORDS:

corticothalamic; downstates; iEEG; sleep; spindles; theta

PMID:
30242045
PMCID:
PMC6234298
DOI:
10.1523/JNEUROSCI.0476-18.2018
[Indexed for MEDLINE]
Free PMC Article

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