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High-frequency oscillations in human and monkey neocortex during the wake-sleep cycle.

Author: Le Van Quyen M¹, Muller LE 2nd², Telenczuk B³, Halgren E⁴, Cash S⁵, Hatsopoulos NG⁶, Dehghani N⁷, Destexhe A⁸
Affiliation:
¹Institut du Cerveau et de la Moelle Epinière, UMRS 1127, CNRS UMR 7225, Hôpital de la Pitié-Salpêtrière, 75013 Paris, France;
²Computational Neurobiology Laboratory, Salk Institute, La Jolla, CA 92037;
³Laboratory of Computational Neuroscience, Unité de Neurosciences, Information, et Complexité, CNRS, 91190 Gif-sur-Yvette, France;
⁴Multimodal Imaging Laboratory, Department of Neurosciences, University of California, San Diego, La Jolla, CA 92093; Multimodal Imaging Laboratory, Department of Radiology, University of California, San Diego, La Jolla, CA 92093;
⁵Department of Neurology, Massachusetts General Hospital, Boston, MA 02114; Department of Neurology, Harvard Medical School, Boston, MA 02115;
⁶Department of Organismal Biology and Anatomy, Committee on Computational Neuroscience, University of Chicago, Chicago, IL 60637;
⁷Wyss Institute for Biologically Inspired Engineering, Harvard University, Boston, MA 02115; New England Complex Systems Institute, Cambridge, MA 02142 nima.dehghani@wyss.harvard.edu destexhe@unic.cnrs-gif.fr.
⁸Laboratory of Computational Neuroscience, Unité de Neurosciences, Information, et Complexité, CNRS, 91190 Gif-sur-Yvette, France; nima.dehghani@wyss.harvard.edu destexhe@unic.cnrs-gif.fr.
Conference/Journal: Proc Natl Acad Sci U S A.
Date published: 2016 Aug 1
Other: Pages: 201523583 , Word Count: 211

Beta (β)- and gamma (γ)-oscillations are present in different cortical areas and are thought to be inhibition-driven, but it is not known if these properties also apply to γ-oscillations in humans. Here, we analyze such oscillations in high-density microelectrode array recordings in human and monkey during the wake-sleep cycle. In these recordings, units were classified as excitatory and inhibitory cells. We find that γ-oscillations in human and β-oscillations in monkey are characterized by a strong implication of inhibitory neurons, both in terms of their firing rate and their phasic firing with the oscillation cycle. The β- and γ-waves systematically propagate across the array, with similar velocities, during both wake and sleep. However, only in slow-wave sleep (SWS) β- and γ-oscillations are associated with highly coherent and functional interactions across several millimeters of the neocortex. This interaction is specifically pronounced between inhibitory cells. These results suggest that inhibitory cells are dominantly involved in the genesis of β- and γ-oscillations, as well as in the organization of their large-scale coherence in the awake and sleeping brain. The highest oscillation coherence found during SWS suggests that fast oscillations implement a highly coherent reactivation of wake patterns that may support memory consolidation during SWS.

KEYWORDS: excitation; inhibition; state-dependent firing; synchrony; wave propagation

PMID: 27482084 DOI: 10.1073/pnas.1523583113

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High-frequency oscillations in human and monkey neocortex during the wake-sleep cycle.