Local sleep in awake rats

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Abstract

In an awake state, neurons in the cerebral cortex fire irregularly and electroencephalogram (EEG) recordings display low-amplitude, high-frequency fluctuations. During sleep, neurons oscillate between ‘on’ periods, when they fire as in an awake brain, and ‘off’ periods, when they stop firing altogether and the EEG displays high-amplitude slow waves. However, what happens to neuronal firing after a long period of being awake is not known. Here we show that in freely behaving rats after a long period in an awake state, cortical neurons can go briefly ‘offline’ as in sleep, accompanied by slow waves in the local EEG. Neurons often go offline in one cortical area but not in another, and during these periods of ‘local sleep’, the incidence of which increases with the duration of the awake state, rats are active and display an ‘awake’ EEG. However, they are progressively impaired in a sugar pellet reaching task. Thus, although both the EEG and behaviour indicate wakefulness, local populations of neurons in the cortex may be falling asleep, with negative consequences for performance.

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Figure 1: Off periods during sleep and awake states.
Figure 2: Local off periods in awake rats.
Figure 3: Off periods in awake rats affect performance.

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Acknowledgements

This work was supported by NIMH P20 MH077967 (C.C.), NIH Director’s Pioneer award (G.T.) and AFOSR FA9550-08-1-0244 (G.T.). We thank A. Nelson, M. Dash and U. Faraguna for help with the experiments, L. Krugner-Higby for advice about surgical procedures and P. Frumento for advice on statistical procedures.

Author information

G.T. and C.C. conceived and directed the study, G.T., C.C. and V.V.V. designed the experiments and wrote the manuscript, V.V.V. and E.C.H. performed the experiments, V.V.V. and U.O. performed data analysis, Y.N. contributed to experiments and writing.

Correspondence to Giulio Tononi.

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The authors declare no competing financial interests.

Supplementary information

Supplementary information

This file contains Supplementary Figures 1-5 with legends, legends for Supplementary Movies 1-2, Supplementary Materials and additional references. (PDF 827 kb)

Supplementary Movie 1

This movie shows a representative example of a successful reach (hit), where the rat successfully grasps the pellet. (MOV 2742 kb)

Supplementary Movie 2

This movie shoes a representative example of two consecutive unsuccessful reaches (misses), where the rat fails to grasp the pellets, but knocks them off the shelf. Note that the rat is clearly behaviorally awake throughout both trials. (MOV 3305 kb)

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