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The brain is a non-equilibrium system whose dynamics change in different brain states, such as wakefulness and deep sleep. Thermodynamics provides the tools for revealing these non-equilibrium dynamics. We used violations of the fluctuation-dissipation theorem to describe the hierarchy of non-equilibrium dynamics associated with different brain states. Together with a whole-brain model fitted to empirical human neuroimaging data, and deriving the appropriate analytical expressions, we were able to capture the deviation from equilibrium in different brain states that arises from asymmetric interactions and hierarchical organisation., Comment: 15 pages of the main ms with 2 figures and 8 pages of supplementary material including 1 figure

The cognitive functions of human and non-human primates rely on the dynamic interplay of distributed neural assemblies. As such, it seems unlikely that cognition can be supported by macroscopic brain dynamics at the proximity of thermodynamic equilibrium. We confirmed this hypothesis by investigating electrocorticography data from non human primates undergoing different states of unconsciousness (sleep, and anesthesia with propofol, ketamine, and ketamine plus medetomidine), and funcional magnetic resonance imaging data from humans, both during deep sleep and under propofol anesthesia. Systematically, all states of reduced consciousness unfolded at higher proximity to equilibrium dynamics than conscious wakefulness, as demonstrated by entropy production and the curl of probability flux in phase space. Our results establish non-equilibrium macroscopic brain dynamics as a robust signature of consciousness, opening the way for the characterization of cognition and awareness using tools from statistical mechanics.

The scope of human consciousness includes states departing from what most of us experience as ordinary wakefulness. These altered states of consciousness constitute a prime opportunity to study how global changes in brain activity relate to different varieties of subjective experience. We consider the problem of explaining how global signatures of altered consciousness arise from the interplay between large-scale connectivity and local dynamical rules that can be traced to known properties of neural tissue. For this purpose, we advocate a research program aimed at bridging the gap between bottom-up generative models of whole-brain activity and the top-down signatures proposed by theories of consciousness. Throughout this paper, we define altered states of consciousness, discuss relevant signatures of consciousness observed in brain activity, and introduce whole-brain models to explore the mechanisms of altered consciousness from the bottom-up. We discuss the potential of our proposal in view of the current state of the art, give specific examples of how this research agenda might play out, and emphasise how a systematic investigation of altered states of consciousness via bottom-up modelling may help us better understand the biophysical, informational, and dynamical underpinnings of consciousness.

We consider the problem of encoding pairwise correlations between coupled dynamical systems in a low-dimensional latent space based on few distinct observations. We used variational autoencoders (VAE) to embed temporal correlations between coupled nonlinear oscillators that model brain states in the wake-sleep cycle into a two-dimensional manifold. Training a VAE with samples generated using two different parameter combinations resulted in an embedding that represented the whole repertoire of collective dynamics, as well as the topology of the underlying connectivity network. We first followed this approach to infer the trajectory of brain states measured from wakefulness to deep sleep from the two endpoints of this trajectory; next, we showed that the same architecture was capable of representing the pairwise correlations of generic Landau-Stuart oscillators coupled by complex network topology

Global brain activity self-organizes into discrete patterns characterized by distinct behavioral observables and modes of information processing. The human thalamocortical system is a densely connected network where local neural activation reciprocally influences coordinated collective dynamics. We introduce a semi-empirical model to investigate the relationship between regional activation and long-range functional connectivity in the different brain states visited during the natural wake-sleep cycle. Our model combines functional magnetic resonance imaging (fMRI) data, in vivo estimates of structural connectivity, and anatomically-informed priors that constrain the independent variation of regional activation. As expected, priors based on functionally coherent networks resulted in the best fit between empirical and simulated brain activity. We show that sleep progressively divided the cortex into regions presenting opposite dynamical behavior: frontoparietal regions approached a bifurcation towards local oscillatory dynamics, while sensorimotor regions presented stable dynamics governed by noise. In agreement with human electrophysiological experiments, sleep onset induced subcortical deactivation and uncoupling, which was subsequently reversed for deeper stages. Finally, we introduced external forcing of variable intensity to simulate external perturbations, and identifiedthe key regionsespecially relevant for the recovery of wakefulness from deep sleep. Our model represents sleep as a state where long-range decoupling and regional deactivation coexist with the latent capacity for a rapid transition towards wakefulness. The mechanistic insights provided by our simulations allow the in silico parametric exploration of such transitions in terms of external perturbations, with potential applications for the control of physiological and pathological brain states.