Rotating waves during human sleep spindles organize global patterns of activity that repeat precisely through the night

Author:

Muller Lyle1ORCID,Piantoni Giovanni2ORCID,Koller Dominik1,Cash Sydney S2,Halgren Eric34,Sejnowski Terrence J1ORCID

Affiliation:

1. Computational Neurobiology Laboratory, Salk Institute for Biological Studies, La Jolla, United States

2. Department of Neurology, Massachusetts General Hospital, Harvard Medical School, Boston, United States

3. Department of Radiology, University of California, San Diego, San Diego, United States

4. Department of Neurosciences, University of California, San Diego, San Diego, United States

Abstract

During sleep, the thalamus generates a characteristic pattern of transient, 11-15 Hz sleep spindle oscillations, which synchronize the cortex through large-scale thalamocortical loops. Spindles have been increasingly demonstrated to be critical for sleep-dependent consolidation of memory, but the specific neural mechanism for this process remains unclear. We show here that cortical spindles are spatiotemporally organized into circular wave-like patterns, organizing neuronal activity over tens of milliseconds, within the timescale for storing memories in large-scale networks across the cortex via spike-time dependent plasticity. These circular patterns repeat over hours of sleep with millisecond temporal precision, allowing reinforcement of the activity patterns through hundreds of reverberations. These results provide a novel mechanistic account for how global sleep oscillations and synaptic plasticity could strengthen networks distributed across the cortex to store coherent and integrated memories.

Funder

Swartz Foundation

Howard Hughes Medical Institute

Office of Naval Research

National Institutes of Health

Bial Foundation

Publisher

eLife Sciences Publications, Ltd

Subject

General Immunology and Microbiology,General Biochemistry, Genetics and Molecular Biology,General Medicine,General Neuroscience

Reference53 articles.

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4. CircStat: a Matlab toolbox for circular statistics;Berens;Journal of Statistical Software,2009

5. Synaptic modifications in cultured hippocampal neurons: dependence on spike timing, synaptic strength, and postsynaptic cell type;Bi;Journal of Neuroscience,1998

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