The entropic brain: a theory of conscious states informed by neuroimaging research with psychedelic drugs

Robin Carhart‐Harris, Robert Leech, Peter J. Hellyer, Murray Shanahan, Amanda Feilding, Enzo Tagliazucchi, Dante R. Chialvo, David Nutt

Frontiers in Human Neuroscience · 2014 · 1.3K citations · 162 references

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TL;DR

Entropy, a measure of uncertainty, is linked to disorder and is a hallmark of systems at self‑organised criticality, a state thought to underlie primitive consciousness such as the psychedelic state. The study aims to test whether elevated entropy characterises primary states of consciousness, such as the psychedelic state, by comparing brain activity across primary and non‑primary states. The authors analyse neural dynamics by measuring entropy of functional connectivity motifs and the collapse of default‑mode network activity and its decoupling from medial temporal lobes during primary states. Neuroimaging of psilocybin shows that primary states exhibit elevated entropy in functional connectivity motifs, whereas normal waking consciousness suppresses entropy, conferring constrained metacognitive functions such as reality‑testing and self.

Abstract

Entropy is a dimensionless quantity that is used for measuring uncertainty about the state of a system but it can also imply physical qualities, where high entropy is synonymous with high disorder. Entropy is applied here in the context of states of consciousness and their associated neural dynamics, with a particular focus on the psychedelic state. The psychedelic state is considered an exemplar of a primitive or primary state of consciousness that preceded the development of modern, adult, human, normal waking consciousness. Based on neuroimaging data with psilocybin, a classic psychedelic drug, it is argued that the defining feature of ‘primary states’ is elevated entropy in certain aspects of brain function, such as the repertoire of functional connectivity motifs that form and fragment across time. It is noted that elevated entropy in this sense, is a characteristic of systems exhibiting ‘self-organised criticality’, i.e., a property of systems that gravitate towards a ‘critical’ point in a transition zone between order and disorder in which certain phenomena such as power-law scaling appear. This implies that entropy is suppressed in normal waking consciousness, meaning that the brain operates just below criticality. It is argued that this entropy suppression furnishes consciousness with a constrained quality and associated metacognitive functions, including reality-testing and self-awareness. It is also proposed that entry into primary states depends on a collapse of the normally highly organised activity within the default-mode network (DMN) and a decoupling between the DMN and the medial temporal lobes (which are normally significantly coupled). These hypotheses can be tested by examining brain activity and associated cognition in other candidate primary states such as REM sleep and early psychosis and comparing these with non-primary states such as normal waking consciousness and the anaesthetised state.

References

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