Information theoretic evidence for layer- and frequency-specific changes in cortical information processing under anesthesia

PLoS Comput Biol. 2023 Jan 26;19(1):e1010380. doi: 10.1371/journal.pcbi.1010380. eCollection 2023 Jan.

Abstract

Nature relies on highly distributed computation for the processing of information in nervous systems across the entire animal kingdom. Such distributed computation can be more easily understood if decomposed into the three elementary components of information processing, i.e. storage, transfer and modification, and rigorous information theoretic measures for these components exist. However, the distributed computation is often also linked to neural dynamics exhibiting distinct rhythms. Thus, it would be beneficial to associate the above components of information processing with distinct rhythmic processes where possible. Here we focus on the storage of information in neural dynamics and introduce a novel spectrally-resolved measure of active information storage (AIS). Drawing on intracortical recordings of neural activity in ferrets under anesthesia before and after loss of consciousness (LOC) we show that anesthesia- related modulation of AIS is highly specific to different frequency bands and that these frequency-specific effects differ across cortical layers and brain regions. We found that in the high/low gamma band the effects of anesthesia result in AIS modulation only in the supergranular layers, while in the alpha/beta band the strongest decrease in AIS can be seen at infragranular layers. Finally, we show that the increase of spectral power at multiple frequencies, in particular at alpha and delta bands in frontal areas, that is often observed during LOC ('anteriorization') also impacts local information processing-but in a frequency specific way: Increases in isoflurane concentration induced a decrease in AIS in the alpha frequencies, while they increased AIS in the delta frequency range < 2Hz. Thus, the analysis of spectrally-resolved AIS provides valuable additional insights into changes in cortical information processing under anaesthesia.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Anesthesia*
  • Animals
  • Brain / physiology
  • Electroencephalography
  • Ferrets
  • Isoflurane* / pharmacology
  • Unconsciousness

Substances

  • Isoflurane

Associated data

  • Dryad/10.5061/dryad.z8w9ghxgp

Grants and funding

E.P. is currently employed by the Leibniz Institute for Resilience Research funded by the Leibniz Gemeinschaft. M. W. is employed at the Campus Institute for Dynamics of Biological Networks funded by the VolkswagenStiftung. O.T. is currently employed by the Leibniz Institute for Resilience Research and University Medical Center of the Johannes Gutenberg University Mainz and received funding by the German Research Foundation (DFG CRC 1193, subproject C04), the Ministry of Science of the state of Rhineland-Palatinate (LIR/DRZ program), and the European Union’s Horizon 2020 research and innovation program (grant agreements No. 777084) in the context of this research. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.