Abstract
Several neuropsychiatric and neurological disorders have recently been characterized as dysfunctions arising from a ‘final common pathway’ of imbalanced excitation to inhibition within cortical networks. How the regulation of a cortical E/I ratio is affected by sleep and the circadian rhythm however, remains to be established. Here we addressed this issue through the analyses of TMS-evoked responses recorded over a 29 h sleep deprivation protocol conducted in young and healthy volunteers. Spectral analyses of TMS-evoked responses in frontal cortex revealed non-linear changes in gamma band evoked oscillations, compatible with an influence of circadian timing on inhibitory interneuron activity. In silico inferences of cell-to-cell excitatory and inhibitory connectivity and GABA/Glutamate receptor time constant based on neural mass modeling within the Dynamic causal modeling framework, further suggested excitation/inhibition balance was under a strong circadian influence. These results indicate that circadian changes in EEG spectral properties, in measure of excitatory/inhibitory connectivity and in GABA/glutamate receptor function could support the maintenance of cognitive performance during a normal waking day, but also during overnight wakefulness. More generally, these findings demonstrate a slow daily regulation of cortical excitation/inhibition balance, which depends on circadian-timing and prior sleep-wake history.
Highlights
Neuronal function sustaining human cognition depends on the balanced and recurrent activity of excitatory and inhibitory circuits[1]
Our aim is to assess the dynamics in human cortical excitation/inhibition balance over the 24 h day
Both spectral and model-based indices reveal a slow, daily regulation of excitation/inhibition balance within a cortical column, which operates at a different time-scale than established fast homeostatic regulation[3]
Summary
Neuronal function sustaining human cognition depends on the balanced and recurrent activity of excitatory and inhibitory circuits[1]. Prior sleep-wake history, and circadian processes interact and regulate cognitive brain function across the course of a day[6,7]. This interaction maintains stable cognitive performance during a normal ~16 h waking day, despite the changes in neuronal structure and the intra/extracellular milieu[8] associated with wakefulness, because of a circadian drive for wakefulness which progressively opposes sleep need accumulation, up to the evening hours. Human studies reported that cortical excitability, i.e. amplitude and slope of scalp EEG responses to stimulations, is not stable and depends on both sleep homeostasis and the circadian system[16,17]. We further postulated that this mesoscopic non-linear neuronal network dynamics would be related to changes in cortical excitability and behavioral measures acquired during the sleep deprivation protocol
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