A New Hypothesis for Sleep: Tuning for Criticality

Abstract

We propose that the critical function of sleep is to prevent uncontrolled neuronal feedback while allowing rapid responses and prolonged retention of short-term memories. Through learning, the brain is tuned to react optimally to environmental challenges. Optimal behavior often requires rapid responses and the prolonged retention of short-term memories. At a neuronal level, these correspond to recurrent activity in local networks. Unfortunately, when a network exhibits recurrent activity, small changes in the parameters or conditions can lead to runaway oscillations. Thus, the very changes that improve the processing performance of the network can put it at risk of runaway oscillation. To prevent this, stimulus-dependent network changes should be permitted only when there is a margin of safety around the current network parameters. We propose that the essential role of sleep is to establish this margin by exposing the network to a variety of inputs, monitoring for erratic behavior, and adjusting the parameters. When sleep is not possible, an emergency mechanism must come into play, preventing runaway behavior at the expense of processing efficiency. This is tiredness.

More Severe Insomnia Complaints in People with Stronger Long-Range Temporal Correlations in Wake Resting-State EEG

“…In the present paper, we speculate that stronger LRTC in people experiencing more severe insomnia complaints reflect increased excitability of cortical networks. This is in agreement with recent reports on decreasing LRTC with sleep depth (Tagliazucchi et al, 2013; Kantelhardt et al, 2015), and with the hypothesis that sleep contributes to the homeostasis between excitatory and inhibitory processes in the brain (Pearlmutter and Houghton, 2009). …”

“…We speculate that poor sleep quality may insufficiently reduce LRTC during subsequent wakefulness, by insufficiently reducing the excitation to inhibition ratio in neuronal networks. This interpretation is consistent with the hypothesis that sleep plays a key role in keeping the wake brain sufficiently far from dynamics dominated by excitation, to provide a safe margin from uncontrolled runaway activity (Pearlmutter and Houghton, 2009)…”

“…Below the critical point the network is dominated by inhibition, whereas above it, by excitation (Poil et al, 2012). Convergent evidence based on several species and recording techniques as well as computer models (Priesemann et al, 2014) confirms the hypothesis that physiological brain dynamics are typically poised near and below the critical point (Pearlmutter and Houghton, 2009; Carhart-Harris et al, 2014). Under this hypothesis, stronger LRTC are therefore indicative of a higher excitation to inhibition ratio (Poil et al, 2012) (see Figure 1).…”

“…Sleep is hypothesized to regulate the complex organization of brain dynamics (Pearlmutter and Houghton, 2009), by keeping excitatory and inhibitory processes balanced (Huber et al, 2013). While prolonged wakefulness increases brain excitability, sleep reduces it, preventing an imbalance towards excitation that would favor runaway seizure-like activity (Meisel et al, 2013, 2015).…”

Self-organized criticality as a fundamental property of neural systems

“…Recent results suggest that also in humans, brain dynamics is close to criticality, yet slightly subcritical (Priesemann et al, 2013, 2014), a possibility first raised by Pearlmutter and Houghton (2009). Resting state dynamics from human brains reveal events analogous to neuronal avalanches whose dynamics fluctuate closely around criticality (EEG Allegrini et al, 2010, fMRI Tagliazucchi et al, 2012, MEG Shriki et al, 2013, EEG and MEG during rest and tasks Palva et al, 2013).…”