Citation

Meisel C, Klaus A, Vyazovskiy VV, Plenz D. J. Neurosci. 2017; 37(42): 10114-10124.

Affiliation

Section on Critical Brain Dynamics, National Institute of Mental Health, Bethesda, Maryland 20892, USA.

Copyright

(Copyright © 2017, Society for Neuroscience)

DOI

10.1523/JNEUROSCI.0448-17.2017

PMID

28947577

Abstract

Increasing evidence suggests that cortical dynamics during wake exhibits long-range temporal correlations suitable to integrate inputs over extended periods of time to increase the signal-to-noise ratio in decision-making and working memory tasks. Accordingly, sleep has been suggested as a state characterized by a breakdown of long-range correlations; detailed measurements of neuronal timescales that support this view, however, have so far been lacking. Here we show that the cortical timescales measured at the individual neuron-level in freely-behaving, male rats change as a function of vigilance state and time awake. While quiet wake and REM sleep are characterized by similar, long timescales, these long timescales are abrogated in non-REM sleep. We observe that cortex dynamics exhibits rapid transitions between long-timescale states and sleep-like states governed by short timescales even during wake. This becomes particularly evident during sleep deprivation where the interplay between these states can lead to an increasing disruption of long timescales which are restored after sleep. Experiments and modeling identify the intrusion of neuronal offline periods as mechanism that disrupts the long timescales arising from reverberating cortical network activity. Our results provide novel mechanistic and functional links between behavioural manifestations of sleep, waking and sleep deprivation, and specific measurable changes in the network dynamics relevant for characterizing the brains changing information processing capabilities. They suggest a network-level function of sleep, to reorganize cortical networks towards states governed by long timescales to ensure efficient information integration for the time awake.SIGNIFICANCE STATEMENTThe lack of sleep deteriorates several key cognitive functions, yet the neuronal underpinnings of these deficits have remained elusive. Cognitive capabilities are generally believed to benefit from a neural circuit's ability to reliably integrate information. Persistent network activity characterized by long timescales may provide the basis for this integration in cortex. Here we show that long-range temporal correlations indicated by slowly decaying autocorrelation functions in neuronal activity are dependent on vigilance states. While wake and REM sleep exhibit long timescales, these long-range correlations break down during NREM sleep. Our findings thus suggest two distinct states in terms of timescale dynamics. During extended wake, the rapid switching to sleep-like states with short timescales can lead to an overall decline in cortical timescales.

Copyright © 2017 the authors.

Language: en