The entropic braina theory of conscious states informed by neuroimaging research with psychedelic drugs

Picture your brain as a city at rush hour. In ordinary waking life, the traffic lights are coordinated, the main avenues hum along, and there's a central control center keeping everything orderly. That control center, in brain terms, is the default-mode network, or DMN—those midline, high-energy hubs that light up when you're reflecting on yourself, remembering the past, or planning the future. Raichle and colleagues showed just how energetically expensive this network is. The posterior cingulate cortex, or PCC, one of its keystone nodes, runs about 40 percent hotter than the brain's average in blood flow and metabolism. Now, the entropic brain idea says that this tightly run city is only one way the brain can be. There's another mode—primary consciousness—where the rules loosen, the controllers step back, and traffic explores side streets you didn't know existed. Psychedelic states, rapid eye movement sleep, and even early psychosis are placed in this category. The claim is bold but intuitive: normal waking suppresses entropy a little, keeping us slightly sub-critical—orderly and predictable—while primary states crank up entropy and push the system toward criticality, where it becomes more fluid and diverse in the patterns it can express. If you want to test that claim, you need a lever. Psilocybin, the active compound in magic mushrooms, has turned out to be a remarkably precise one. Carhart-Harris and colleagues designed a clean, tightly timed probe: they delivered a small intravenous dose—2 milligrams over 60 seconds—right in the middle of a quiet resting-state scan, and watched what happened. They ran that play twice with separate cohorts of healthy volunteers, 15 people each time. One set used arterial spin labeling to track cerebral blood flow during an 18-minute scan, with the infusion at minute six. The other used the classic blood-oxygen-level-dependent, or BOLD, signal in two 12-minute eyes-closed runs on different days, one with placebo. The headline was unambiguous. After psilocybin, signals didn't go up anywhere. They went down. Blood flow and BOLD activity dropped in high-level association cortices, especially the midline nodes of the default-mode network, and in subcortical hubs like the putamen and thalamus. The places most involved in the brain's internal coordination dimmed. That amplitude story is only the start. What really matters for entropy is not how loud the music is, but how the players coordinate and change over time. Seed-based connectivity analyses showed that coupling inside the default-mode network slackened. Using a medial prefrontal seed and a bilateral hippocampal seed, connectivity within the DMN decreased under psilocybin. Using a right middle frontal gyrus seed, connectivity decreased in the dorsal attention network, a major task-positive system. At the same time, the usual "push and pull" between the DMN and task-positive networks flattened. That loss of strong anticorrelation—the two big city bureaus not pulling against each other as hard—signals a shallower attractor landscape, a system less locked into its usual patterns. Now zoom in on a specific relationship that several teams had suspected was central to the ego's grip on experience: the handshake between the default-mode network and the medial temporal lobes, or MTL. Under psilocybin, that handshake weakens. Psychophysiological interaction analysis centered on the hippocampi showed reduced coupling with cortical DMN nodes. Meanwhile, the medial temporal lobes themselves, particularly the hippocampi and parahippocampal gyri, became more volatile: the amplitude of their BOLD fluctuations rose. It's like the memory and context machinery started to freewheel a bit from the brain's overseers. That decoupling shows up not as one blip, but as a change in the texture of network activity. To capture that texture, the group introduced two time-resolved measures. First, metastability: how much a network's internal synchrony wobbles over time. They computed the variance of that synchrony for each of nine canonical resting-state networks, then compared drug to baseline. After psilocybin, several high-level networks showed significant increases in metastability when tested against a Bonferroni-corrected threshold with a p-value below 0.006. Sensory and motor systems? Much less affected. The instability was not everywhere; it was concentrated where abstract, associative processing lives. That's a useful clue. Second, they asked how the short-lived patterns of connection among key limbic and paralimbic nodes diversify. They focused on four regions: the left and right hippocampi and the left and right anterior cingulate cortices. At any moment, those four nodes can be connected in 64 possible configurations, or motifs. Under psilocybin, the brain visited more of them. Some motifs appeared only in the drug state. When they treated the stream of motifs like a sentence and computed how predictable the sequence is, entropy rises. The motif story is compelling because it translates a vague idea—more possible brain states—into something you can actually count. Oscillations tell the same story from a different angle. In magnetoencephalography, or MEG, where you track the brain's rhythmic power directly, activity dropped broadly across frequencies in association cortices, including the posterior cingulate. One link stood out with unusual strength: decreased alpha-band power in the posterior cingulate predicted how intensely people felt their ego dissolve. That single measure accounted for about 66 percent of the variance in ego-disintegration ratings and, together with a correlation with magical thinking, survived a tough Bonferroni correction set for 23 symptom items, with a p-value of 0.002. You don't often see a neural feature that cleanly anchors a subjective experience. Here, the alpha rhythm—a kind of idling hum that often reflects top-down inhibition—quieted, and people reported that the boundary of "me" loosened. If you put these threads together—DMN and hippocampal decoupling, increased medial temporal volatility, reduced DMN internal synchrony, greater metastability in association networks, a wider repertoire, and higher entropy of limbic motifs, along with posterior cingulate alpha power downshifts that track ego loss—you get a picture that aligns with the entropic brain hypothesis. The organized, hierarchical oversight of the default-mode network weakens. The networks most involved in self-referential thought and narrative control become less tightly locked. The system explores more configurations. Meanwhile, sensory and motor networks, for the most part, keep doing their jobs. That asymmetry matters. It suggests we're not just seeing global neural chaos; we're seeing a targeted loosening of the brain's high-level governance. There's a tempting way to think about this in everyday terms. In normal waking, the DMN and its partners keep our thoughts coherent, our sense of self intact, and our predictions about the world stable. That's useful. It's also constraining. Psilocybin seems to nudge the brain back toward a more primary mode that William James might have recognized—associations flowing more freely, habitual narratives softened, and attention less corralled by the "me." Participants repeatedly endorsed the feeling that "my thoughts wandered freely," and in several studies, that item ranked among the highest experiences post-psilocybin. The link to network dynamics gives those reports a biological footprint. Two caveats are important here. First, none of the measures in these studies computed Shannon entropy directly on the brain's raw signal. Entropy was inferred from variance-based metastability and from the unpredictability of motif sequences. While they're good proxies for diversification and temporal irregularity, they are still proxies. Second, these were modest samples—15 people per study—with seed choices and thresholds that can shape connectivity results. The teams were careful with corrections, but replication across independent cohorts and labs is the long game. Still, the convergence is striking. In both arterial spin labeling and BOLD functional magnetic resonance imaging, or fMRI, the drug drove only decreases in high-level signals, not increases. In seed-based coupling, both the DMN and dorsal attention network loosened internally. In dynamics, association networks—not sensory and motor networks—grew more metastable, with significance after a stringent correction with a p-value below 0.006. In MEG, broadband power fell in the very regions that orchestrate self-referential processing, and a single posterior cingulate feature tracked ego disintegration with unusual precision. Add in the medial temporal lobes story—variance up, coupling to the DMN down—and you have a set of neural signatures that make sense together. This neural picture maps neatly onto the theoretical split between secondary and primary consciousness that Carhart-Harris and colleagues have proposed. Secondary consciousness—the mode that runs your day—sits just below criticality. It suppresses entropy a bit to keep your model of the world stable and your self-monitoring sharp. Primary states, by contrast, elevate entropy and approach criticality, expanding the brain's repertoire and loosening rigid patterns of thought. Priesemann and collaborators have pointed out that normal waking activity appears to be sub-critical when you model its dynamics. This fits the idea that the brain chooses stability over perfect flexibility most of the time. Where does this go next? The framework makes specific, testable predictions beyond psychedelics. In rapid eye movement sleep and in early psychosis—both proposed primary states—you should see DMN and medial temporal decoupling, increased medial temporal signal variance, and reduced posterior cingulate alpha compared with non-primary states. Those claims can be tackled with simultaneous functional magnetic resonance imaging and electroencephalography or with magnetoencephalography, and with longitudinal work that tracks how these dynamics change across brain development. On the flip side, in non-primary states like deep anesthesia, the expectation is lower entropy and tighter DMN constraint, though the authors are candid that those comparisons need more direct tests. There's a clinical caution folded into all this. If psychedelics relax the brain's internal governors and increase the fluidity of thought, that can be therapeutic—breaking maladaptive ruts and softening rigid self-beliefs. But it also means reality-testing can wobble. Context and support matter. These drug-induced shifts are not toys, and the very dynamism that helps some patients can be destabilizing in the wrong setting. The broader intellectual project here is a bridge. On one side, there are old ideas about primary process thinking—the dreamlike and associative style that psychoanalysts have described for a century. On the other, there is modern network neuroscience with its maps of hubs, anticorrelations, and dynamic motifs. Psilocybin, when used carefully, turns out to be a way to walk back and forth across that bridge under controlled conditions. It pulls the brain toward criticality just enough that we can watch the city explore new routes, then return to rush-hour order. In those excursions, we learn something fundamental: consciousness isn't a single setting. It's a regime the brain can tune, trading a little order for possibility, or a little possibility for order, depending on what the moment demands.