Breakdown of local information processing may underlie isoflurane anesthesia effects

TL;DR

This study suggests that isoflurane anesthesia impairs local cortical information processing, leading to decreased source entropy and reduced interareal information transfer, challenging the view that decoupling alone causes loss of consciousness.

Contribution

It demonstrates that local information processing deficits, rather than interareal decoupling, primarily underlie anesthesia effects on brain connectivity.

Findings

Strong decrease in source entropy in V1 and PFC under isoflurane

Reduced bidirectional information transfer between V1 and PFC

Greater decrease in source entropy in PFC compared to V1

Abstract

The disruption of coupling between brain areas has been suggested as the mechanism underlying loss of consciousness in anesthesia. This hypothesis has been tested previously by measuring the information transfer between brain areas, and by taking reduced information transfer as a proxy for decoupling. Yet, information transfer is a function of the amount of information available in the information source-such that transfer decreases even for unchanged coupling when less source information is available. Therefore, we asked whether impaired local information processing leads to a loss of information transfer. An important prediction of this alternative hypothesis is that changes in locally available information (signal entropy) should be at least as pronounced as changes in information transfer. We tested this prediction by recording local field potentials in two ferrets after administration of isoflurane in concentrations of 0.0 %, 0.5 %, and 1.0 %. We found strong decreases in the source entropy under isoflurane in area V1 and the prefrontal cortex (PFC)-as predicted by our alternative hypothesis. The decrease in source entropy was stronger in PFC. Information transfer between V1 and PFC was reduced bidirectionally, but with a stronger decrease from PFC to V1. This links the stronger decrease in information transfer to the stronger decrease in source entropy, suggesting reduced source entropy reduces information transfer. This conclusion fits the observation that the synaptic targets of isoflurane are located in local cortical circuits rather than on the synapses formed by interareal axonal projections. Thus, changes in information transfer under isoflurane seem to be a consequence of changes in local processing more than of decoupling between brain areas. We suggest that source entropy changes must be considered whenever interpreting changes in information transfer as decoupling.