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J Neurosci. 2018 Mar 21;38(12):3013-3025. doi: 10.1523/JNEUROSCI.2241-17.2018. Epub 2018 Feb 15.

Heterogeneous Origins of Human Sleep Spindles in Different Cortical Layers.

Author information

1
Department of Radiology, University of California at San Diego, La Jolla, California 92093.
2
Institute of Cognitive Neuroscience and Psychology, Research Center for Natural Sciences, Hungarian Academy of Science, Budapest, Hungary 1117.
3
Péter Pázmány Catholic University, Faculty of Information Technology and Bionics, Budapest, Hungary 1117.
4
Department of Functional Neurosurgery, National Institute of Clinical Neurosciences, Budapest, Hungary 1145.
5
Departments of Neurosurgery, Boston Children's Hospital and Harvard Medical School, Boston, Massachusetts 02115.
6
Comprehensive Epilepsy Center, New York University School of Medicine, New York, New York 10016.
7
Epilepsy Centrum, National Institute of Clinical Neurosciences, Budapest, Hungary 1145.
8
Department of Neurology, Epilepsy Division, Massachusetts General Hospital, Harvard Medical School, Boston, Massachusetts 02114, and.
9
Department of Radiology, University of California at San Diego, La Jolla, California 92093, ehalgren@ucsd.edu.
10
Department of Neuroscience, University of California at San Diego, La Jolla, California 92093.

Abstract

Sleep spindles are a cardinal feature in human NREM sleep and may be important for memory consolidation. We studied the intracortical organization of spindles in men and women by recording spontaneous sleep spindles from different cortical layers using linear microelectrode arrays. Two patterns of spindle generation were identified using visual inspection, and confirmed with factor analysis. Spindles (10-16 Hz) were largest and most common in upper and middle channels, with limited involvement of deep channels. Many spindles were observed in only upper or only middle channels, but approximately half occurred in both. In spindles involving both middle and upper channels, the spindle envelope onset in middle channels led upper by ∼25-50 ms on average. The phase relationship between spindle waves in upper and middle channels varied dynamically within spindle epochs, and across individuals. Current source density analysis demonstrated that upper and middle channel spindles were both generated by an excitatory supragranular current sink while an additional deep source was present for middle channel spindles only. Only middle channel spindles were accompanied by deep low (25-50 Hz) and high (70-170 Hz) gamma activity. These results suggest that upper channel spindles are generated by supragranular pyramids, and middle channel by infragranular. Possibly, middle channel spindles are generated by core thalamocortical afferents, and upper channel by matrix. The concurrence of these patterns could reflect engagement of cortical circuits in the integration of more focal (core) and distributed (matrix) aspects of memory. These results demonstrate that at least two distinct intracortical systems generate human sleep spindles.SIGNIFICANCE STATEMENT Bursts of ∼14 Hz oscillations, lasting ∼1 s, have been recognized for over 80 years as cardinal features of mammalian sleep. Recent findings suggest that they play a key role in organizing cortical activity during memory consolidation. We used linear microelectrode arrays to study their intracortical organization in humans. We found that spindles could be divided into two types. One mainly engages upper layers of the cortex, which are considered to be specialized for associative activity. The other engages both upper and middle layers, including those devoted to sensory input. The interaction of these two spindle types may help organize the interaction of sensory and associative aspects of memory consolidation.

KEYWORDS:

cortex; human; layer; memory; spindle

PMID:
29449429
PMCID:
PMC5864151
DOI:
10.1523/JNEUROSCI.2241-17.2018
[Indexed for MEDLINE]
Free PMC Article

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