Desflurane Anesthesia Alters Cortical Layer–specific Hierarchical Interactions in Rat Cerebral Cortex

BACKGROUND: Neurocognitive investigations suggest that conscious sensory perception depends on recurrent neuronal interactions among sensory, parietal, and frontal cortical regions, which are suppressed by general anesthetics. The purpose of this work was to investigate if local interactions in sensory cortex are also altered by anesthetics. The authors hypothesized that desflurane would reduce recurrent neuronal interactions in cortical layer-specific manner consistent with the anatomical disposition of feedforward and feedback pathways. METHODS: Single-unit neuronal activity was measured in freely moving adult male rats (268 units; 10 animals) using microelectrode arrays chronically implanted in primary and secondary visual cortex. Layer-specific directional interactions were estimated by mutual information and transfer entropy of multineuron spike patterns within and between cortical layers three and five. The effect of incrementally increasing and decreasing steady-state concentrations of desflurane (0 to 8% to 0%) was tested for statistically significant quadratic trend across the successive anesthetic states. RESULTS: Desflurane produced robust, state-dependent reduction (P = 0.001) of neuronal interactions between primary and secondary visual areas and between layers three and five, as indicated by mutual information (37 and 41% decrease at 8% desflurane from wakeful baseline at [mean +/- SD] 0.52 +/- 0.51 and 0.53 +/- 0.51 a.u., respectively) and transfer entropy (77 and 78% decrease at 8% desflurane from wakeful baseline at 1.86 +/- 1.56 a.u. and 1.87 +/- 1.67 a.u., respectively). In addition, a preferential suppression of feedback between secondary and primary visual cortex was suggested by the reduction of directional index of transfer entropy overall (P = 0.001; 89% decrease at 8% desflurane from 0.11 +/- 0.18 a.u. at baseline) and specifically, in layer five (P = 0.001; 108% decrease at 8% desflurane from 0.12 +/- 0.19 a.u. at baseline). CONCLUSIONS: Desflurane anesthesia reduces neuronal interactions in visual cortex with a preferential effect on feedback. The findings suggest that neuronal disconnection occurs locally, among hierarchical sensory regions, which may contribute to global functional disconnection underlying anesthetic-induced unconsciousness. : WHAT WE ALREADY KNOW ABOUT THIS TOPIC: Recurrent neuronal interactions between sensory and association cortices are thought to underlie conscious experienceAnesthetics-induced loss of consciousness is accompanied by a breakdown of functional connectivity between these brain regionsThe effects of anesthetics on neuronal connectivity in within local neuronal circuits have not been previously reported WHAT THIS ARTICLE TELLS US THAT IS NEW: In vivo intracortical electrophysiologic recordings from the visual cortices of male rats reveal that desflurane disrupts cortical layer-specific neuronal interactions in local brain circuitsThese observations suggest that neuronal connectivity changes in local cortical circuits may contribute to large-scale cortical functional disintegration as a mechanism of anesthetic-induced unconsciousness.