Global sleep homeostasis reflects temporally and spatially integrated local cortical neuronal activity

Abstract

<jats:p>Sleep homeostasis manifests as a relative constancy of its daily amount and intensity. Theoretical descriptions define ‘Process S’, a variable with dynamics dependent on global sleep-wake history, and reflected in electroencephalogram (EEG) slow wave activity (SWA, 0.5–4 Hz) during sleep. The notion of sleep as a local, activity-dependent process suggests that activity history must be integrated to determine the dynamics of global Process S. Here, we developed novel mathematical models of Process S based on cortical activity recorded in freely behaving mice, describing local Process S as a function of the deviation of neuronal firing rates from a locally defined set-point, independent of global sleep-wake state. Averaging locally derived Processes S and their rate parameters yielded values resembling those obtained from EEG SWA and global vigilance states. We conclude that local Process S dynamics reflects neuronal activity integrated over time, and global Process S reflects local processes integrated over space.</jats:p>

Psilocin acutely disrupts sleep and affects local but not global sleep homeostasis in laboratory mice

“…The sleep-wake history of an individual is tracked by physiological processes in the brain in order to homeostatically regulate global vigilance states, such that, for example, sleep deprivation is compensated by increased subsequent sleep duration and intensity. This phenomenon is termed “Process S”, and with an underlying biological substrate that is not completely certain, measures the magnitude of the homeostatic drive to sleep, and can predict with high accuracy EEG slow wave activity through mathematical models (Daan et al, 1984; Achermann et al, 1993; Guillaumin et al, 2018; Thomas et al, 2020).…”

“…In this regard, the finding of a reduced recovery rate of Process S locally in the LFP targeting prefrontal cortex is of potential importance. The global Process S which manifests in slow wave activity at the EEG level has been suggested to result from the integration across the brain of many local Processes S, which in turn each reflect the recent history of local neuronal activities (Thomas et al, 2020). If the rate of Process S recovery is slowed locally in prefrontal regions, it is possible that recovery may occur more quickly elsewhere in the brain, such as more posterior cortex.…”

“…The brain’s level of homeostatic sleep need is widely recognised to be reflected in the average levels of non-rapid eye movement (NREM) sleep slow wave activity (0.5-4 Hz) in neurophysiological field potentials (Daan et al, 1984; Achermann et al, 1993; Huber et al, 2000), such as can be observed in the electroencephalogram (EEG) or intracortical local field potential (LFP). However, slow wave amplitude and dynamics across the cortical surface reveal a heterogeneity and dependence on both behaviour and neuronal activity levels during previous wakefulness, with evidence for a bidirectional relationship between local neuronal activity and sleep-wake homeostasis (Huber et al, 2004; Rattenborg et al, 2012; Fisher et al, 2016; Thomas et al, 2020; Milinski et al, 2020).…”

Waking experience modulates sleep need in mice

“…Active wakefulness associated with higher neuronal activity (Thomas et al , 2020) or EEG theta power (Vassalli and Franken, 2017) has previously been associated with increased homeostatic sleep pressure. The underlying neurobiological substrate of this association remains to be determined, yet its clear implication is that some behaviours may be associated with faster accumulation of sleep need.…”

“…Thus, it is possible that a well-trained task involving the execution of a stereotypical motor-sequence rather than constantly adapting behaviour may be sustained even during localised changes in cortical activity or ‘local sleep’ in some cortical areas. Since evidence suggests that local cortical neuronal activities represent an important factor in governing global sleep homeostasis (Thomas et al , 2020), engagement in well-trained behaviours may therefore result in an attenuated build-up of sleep need during waking. Consistent with this notion, it has been shown that stereotypic, repetitive wheel running is associated with a substantial prolongation of wake periods (Vyazovskiy et al , 2006), yet this does not lead to an increase in cortical excitability, which was previously associated with increased sleep pressure (Huber et al , 2013; Donlea, Pimentel and Miesenböck, 2014; Fisher et al , 2016; Reichert, Pavón Arocas and Rihel, 2019).…”