Functional hierarchies in brain dynamics characterized by signal reversibility in ferret cortex

PLoS Comput Biol. 2024 Jan 19;20(1):e1011818. doi: 10.1371/journal.pcbi.1011818. eCollection 2024 Jan.

Abstract

Brain signal irreversibility has been shown to be a promising approach to study neural dynamics. Nevertheless, the relation with cortical hierarchy and the influence of different electrophysiological features is not completely understood. In this study, we recorded local field potentials (LFPs) during spontaneous behavior, including awake and sleep periods, using custom micro-electrocorticographic (μECoG) arrays implanted in ferrets. In contrast to humans, ferrets remain less time in each state across the sleep-wake cycle. We deployed a diverse set of metrics in order to measure the levels of complexity of the different behavioral states. In particular, brain irreversibility, which is a signature of non-equilibrium dynamics, captured by the arrow of time of the signal, revealed the hierarchical organization of the ferret's cortex. We found different signatures of irreversibility and functional hierarchy of large-scale dynamics in three different brain states (active awake, quiet awake, and deep sleep), showing a lower level of irreversibility in the deep sleep stage, compared to the other. Irreversibility also allowed us to disentangle the influence of different cortical areas and frequency bands in this process, showing a predominance of the parietal cortex and the theta band. Furthermore, when inspecting the embedded dynamic through a Hidden Markov Model, the deep sleep stage was revealed to have a lower switching rate and lower entropy production. These results suggest functional hierarchies in organization that can be revealed through thermodynamic features and information theory metrics.

MeSH terms

  • Animals
  • Brain Mapping / methods
  • Brain* / physiology
  • Ferrets*
  • Humans
  • Sleep / physiology
  • Wakefulness / physiology

Grants and funding

S.I is supported by the EU project euSNN (MSCA-ITN-ETN H2020-860563). G.D. received funding from the Horizon EU ERC Synergy Grant Project ID: 101071900; Spanish national research project (ref. PID2019-105772GB-I00/AEI/10.13039/501100011033) funded by the Spanish Ministry of Science, Innovation and Universities (MCIU); A.K.E. received funding from the DFG (SFB936-178316478-A2) and from the European Union (project cICMs, ERC-2022-AdG-101097402). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Views and opinions expressed in this paper are those of the authors only and do not necessarily reflect those of the European Union or the European Research Council. Neither the European Union nor the granting authority can be held responsible for them.