Hierarchical Fluctuation Shapes a Dynamic Flow Linked to States of Consciousness

Abstract

Consciousness emerges from the spatiotemporal dynamics of neural activity. However, how such an extraordinary phenomenon is supported by neural flexibility and regional specialization across the cerebral cortex remains elusive. Here, using several functional magnetic resonance imaging (fMRI) paradigms (e.g., anesthesia, sleep, and drowsiness), we show a consciousness-related signature characterized by shifting spontaneous fluctuations along a unimodal-transmodal cortical organizational axis. The signature is simple and sensitive to altered states of consciousness in single individuals, exhibiting abnormal elevation under psychedelics as well as in individuals with psychosis. Under task-free conditions, this hierarchical dynamic reflects ongoing brain state changes in global integration and connectome diversity. Applying quasi-periodic pattern detection during different vigilance states, we found that hierarchical heterogeneity also manifested as spatiotemporally propagation waves related to arousal. A similar pattern was observed in neural activity measured with cortex-wide electrocorticography (ECoG) in macaques. Last, we observed that the spatial distribution of the principle cortical gradient not only preferentially recapitulated the genetic transcription levels of the histaminergic system but also that of the functional connectome mapping of the tuberomammillary nucleus (TMN), which promotes wakefulness. Combining behavioral, neuroimaging, electrophysiological, and transcriptomic evidence, we suggest that global state of consciousness is supported by efficient hierarchical processing that can be constrained along a low-dimensional macroscale gradient.

Local Orchestration of Global Functional Patterns Supporting Loss and Restoration of Consciousness in the Primate Brain

“…However, there is now increasingly compelling evidence for a role of distributed, large-scale patterns of cortical organisation supporting cognitive function, dysfunction, (Margulies et al, 2016;Huntenburg, Bazin and Margulies, 2018;Fulcher et al, 2019;Paquola et al, 2019;Bethlehem et al, 2020;Cross et al, 2021) and consciousness (Dehaene and Naccache, 2001;Dehaene and Changeux, 2011;Atasoy et al, 2017;Atasoy, Deco, et al, 2018). Recent work has demonstrated that multiple pathological and pharmacological perturbations of consciousness induce consistent reorganisation of the brain's functional architecture along functional and anatomical axes of cortical organisation (Huang, Mashour and Hudetz, 2023;Li et al, 2023;Luppi, Hansen, et al, 2023). This distributed approach goes beyond viewing the brain in terms of brain regions and fixed networks, emphasising the role of dynamics and functional organisation.…”

Neural geometrodynamics, complexity, and plasticity: a psychedelics perspective

“…This has been suggested to be intimately linked to non-equilibrium dynamics in thermodynamic-inspired frameworks where the level of hierarchy is related to the amount of brain signal irreversibility as well as entropy production [41][42][43]. Indeed it has been demonstrated that the principal functional gradient collapses under the influence of various psychedelics [44][45][46].…”

Deciphering complex brain spatiotemporal dynamics shaping diverse human behavior

“…The human brain, as the one of the most morphologically and functionally intricate biological structures, operates as a complex, adaptive, dynamic system [17][18][19][20] governed by intricate cross-scale spatiotemporal mechanisms 7,21 . This system demands continuous adaptability and responsiveness to external stimuli or engaging in internal cognitive processes like mind-wandering 22,23 .…”

“…This system demands continuous adaptability and responsiveness to external stimuli or engaging in internal cognitive processes like mind-wandering 22,23 . Previous research indicates that certain temporal statistical features can illuminate intrinsic system-level properties, potentially facilitating comparisons among diverse neural systems 21,[24][25][26][27][28] . For instance, a straightforward metric, 'temporal autocorrelation', identifies the intrinsic timescale of a system's information integrating 29 , thereby sketching its hierarchical organization from sensory to associative areas 30 .…”

“…Alternatively, systems of varying complexity, characterized by the richness and diversity of their information processing, can exhibit differences in the predictability or compressibility of their spatiotemporal signals, as captured by entropy-based measurements 26,27 . Moreover, systems manifest varied global configurations such as task processing, differing consciousness levels, or abnormal states; these global states, associated with changes in neural dimensionality and flexibility, can be inferred from the amplitude fluctuations of spatiotemporal signals 21,31 . Thus, these spatiotemporal dynamic characteristics can aid in outlining a system's essence, contributing to our understanding of why different systems display varied behaviors.…”