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Dynamics of human cortical ensembles are set by circadian system and sleep homeostasis

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Academic year: 2021

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Dynamics of human cortical ensembles are set by circadian system and sleep homeostasis Sarah L. Chellappa1*, Julien Q. M. Ly1*, Giulia Gaggioni1*, Soterios Papachilleos1, Chloé Borsu1,

Alexander Brzozowski1, Simon N. Archer3, Mario Rosanova2, Simone Sarasso2, Derk-Jan Dijk3,

Pierre Maquet1, Marcello Massimini2, Christophe Phillips1, Rosalyn J. Moran4, Gilles Vandewalle1 1 Cyclotron Research Centre, University of Liège, Liège, Belgium

2 Department of Biomedical and Clinical Sciences, Università degli Studi di Milano, Milan, Italy 3

Surrey Sleep Research Centre, University of Surrey, Guildford, UK

4 Virginia Tech Carilion Research Institute, Virginia Tech, Roanoke, VA, USA

Objectives: Animal and human studies indicate linear alterations in inhibitory/excitatory neurotransmission during sleep and wakefulness, suggesting an exclusive sleep homeostatic influence. However, recent data posit a circadian, non-linear influence on neuronal function. We investigated whether this circadian drive impacts on human brain function in vivo.

Methods: We applied neural mass models using dynamic causal modeling (DCM), a Bayesian technique for neuronal identification, to transcranial magnetic stimulation (TMS)-evoked EEG signals from the prefrontal cortex (PFC, highly sensitive to sleep pressure). Twenty-two healthy young participants (18-30y) underwent 8 TMS-EEG recordings, during 28-h of sustained wakefulness, under stringent constant routine conditions. All significant effects are Pcorr< 0.05. Results: Using DCM, we estimated GABAergic/glutamatergic functions, inhibitory/excitatory drives, and inhibitory/excitatory action potentials across PFC neuronal subpopulations. Overall control (self-inhibitory gain) within superficial pyramidal cells and inhibitory interneurons decreased with time awake, with nadir and peak in the circadian evening wake-maintenance zone and early morning sleep-maintenance zone, respectively. Conversely, GABAergic function and inhibitory action potentials across neuronal subpopulations increased with time awake, with local decrease and increase during wake- and sleep-maintenance zones, respectively. Excitatory action potentials slightly increased with time, with local decrease in the wake-maintenance zone. All time-courses were best predicted by the interaction of sine-wave (circadian) and linear (sleep homeostasis) functions.

Conclusions: Our results provide a proof-of-principle that inhibitory/excitatory changes in neuronal subpopulations reflect the interaction of circadian system and sleep homeostasis. Ultimately, the data provide a unique window on the hidden neuronal milieu setting the temporal organization of human brain function.

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