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

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

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 neurodynamics, 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. Indeed, since there is a greater repertoire of connectivity motifs in the psychedelic state than in normal waking consciousness, this implies that primary states may exhibit "criticality," i.e., the property of being poised at a "critical" point in a transition zone between order and disorder where certain phenomena such as power-law scaling appear. Moreover, if primary states are critical, then this suggests that entropy is suppressed in normal waking consciousness, meaning that the brain operates just below criticality. It is argued that this entropy suppression furnishes normal waking 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 organized 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 rapid eye movement (REM) sleep and early psychosis and comparing these with non-primary states such as normal waking consciousness and the anaesthetized state.

Keywords: 5-HT2A receptor; REM sleep; consciousness; criticality; default mode network; entropy; metastability; serotonin.

Figures

Figure 1
Figure 1
Relative publications on psychoanalysis and cognitive psychology. Annual publications in major medical science journals referenced in the leading database, PubMed. Articles were retrieved by entering the search terms “psychoanalysis” and “cognitive psychology” in separate searches using the default search parameters of PubMed. It is worth noting that psychoanalysis has a different publication culture to cognitive neuroscience. Articles on psychoanalysis are not always available via PubMed and many psychoanalytic writings are published in books rather than academic journals. With these caveats entered however, the publication count shown above still helps to illustrate the general point that psychoanalysis has failed to gain a significant foothold in mainstream analytical science.
Figure 2
Figure 2
The effect of psilocybin on fMRI and MEG measures of brain activity. (A) Decreased CBF post-psilocybin. (B) Ventromedial PFC (red) resting state functional connectivity (RSFC) at baseline (top, orange) and decreases post-psilocybin (bottom, blue). (C) Dorsolateral PFC (red) RSFC at baseline (top, orange) and decreases post-psilocybin (bottom, blue). (D) Hippocampal (red) RSFC at baseline (top, orange) and decreases post-psilocybin (bottom, blue). (E) Decreases in oscillatory power (purple) post-psilocybin measured with MEG. All spatial maps were whole-brain cluster corrected Z > 2.3. p < 0.05.
Figure 3
Figure 3
Increased variance/amplitude fluctuations in the hippocampus post-psilocybin. The charts on the left show the complete time series from the hippocampus (left in blue, right in green) in 3 different individual subjects during the 12 min scan in which they received psilocybin. The transparent red vertical line indicates the beginning and duration of the 60 s infusion of psilocybin. The images on the right show the right hippocampal region where the increases in variance were especially marked.
Figure 4
Figure 4
Decreased PCC alpha power predicts ego-disintegration and magical thinking after psilocybin. Top: Decreased PCC alpha power v ratings of ego-disintegration. Bottom: Decreased PCC alpha power vs. ratings of magical/supernatural thinking. Both correlations were significant after correction for multiple comparisons (0.05/23 = 0.002). These charts are derived from data discussed in Muthukumaraswamy et al. (2013).
Figure 5
Figure 5
Psilocybin promotes unconstrained thinking and decreases blood flow, venous oxygenation and oscillatory power in the DMN. This chart shows the average (+SE) ratings for the item “my thoughts wandered freely” in 3 neuroimaging studies, each involving the administration of psilocybin and placebo to 15 healthy volunteers. Ratings were given within 30 min of the end of the relevant resting state scans. This particular item was one of the highest rated items in all 3 studies and nicely communicates the quality of cognition that predominates in the psychedelic state. The brain image on the left displays the mean regional decreases in CBF post-psilocybin in the ASL study; the central image displays the mean regional decreases in BOLD signal post-psilocybin in the BOLD study; and the image on the right displays the mean regional decreases in alpha power post-psilocybin in the MEG study. All images were derived using a whole brain corrected threshold of p < 0.05.
Figure 6
Figure 6
Changes in network metastability and entropy post-infusion of psilocybin. (A) This chart displays the mean variance of the internal synchrony of 9 brain networks for the sample of 15 healthy volunteers, as a percentage change post vs. pre-infusion. A post-infusion increase in metastability for a specific network indicates that the mean signal in that network is a poor model of the activity in its constituent voxels, implying that the network is behaving more “chaotically” post-infusion than pre. Bonferonni correction gave a revised statistical threshold of p < 0.006 (0.05/9). One-sample (2-tailed) t-tests were performed, comparing the % change against zero. The significant networks are labeled with an asterisk. (B,C) These probability distributions were derived from data from the same single subject, by discretizing a measure of the internal synchrony of the DMN across time into bins. These bins reflect the distance a data point is from the mean and this gives a probability distribution of the variance of internal synchrony within a network for a given time period (e.g., a 5 min period of scanning). The probability distributions shown in Chart B were produced from placebo data where it is clear that prediction of internal network synchrony of the DMN across time is similar before and after infusion (i.e., the blue and green curves). The probability distributions shown in Chart C were derived using psilocybin data and here it is evident that following infusion of psilocybin (i.e., the green curve), prediction of internal network synchrony within the DMN is more difficult compared to pre infusion (the blue curve). When the entropy change was calculated for the group, significantly greater increases in entropy were found in the same networks highlighted in (A) (post-psilocybin vs. pre) vs. (post-placebo vs. pre).
Figure 7
Figure 7
Spectrum of cognitive states. This schematic is intended to summarize much of what this paper has tried to communicate. It shows an “inverted u” relationship between entropy and cognition such that too high a value implies high flexibility but high disorder, whereas too low a value implies ordered but inflexible cognition. It is proposed that normal waking consciousness inhabits a position that is close to criticality but slightly sub-critical and primary states move brain activity and associated cognition toward a state of increased system entropy i.e., brain activity becomes more random and cognition becomes more flexible. It is proposed that primary states may actually be closer to criticality proper than secondary consciousness/normal waking consciousness.
Figure 8
Figure 8
Gas expansion post-release of constraints as a metaphor for increased entropy in primary states. (A) Entropy is low while the gas is constrained. (B) Entropy increases once constraints are released. In an information theoretical sense, entropy/uncertainty is increased post-expansion because it is more difficult to predict the spatial location of a single molecule. In primary vs. secondary states, it is hypothesized that the biological parameters known to define key brain states (e.g., the default-mode) become more variant or less predictable, thus causing the subject to become less certain in themselves and their experience of the world.

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