Neural Dynamics in Primate Cortex During Exposure to Subanesthetic Concentrations of Nitrous Oxide
Open Access
- 16 June 2021
- journal article
- research article
- Published by Society for Neuroscience in eneuro
Abstract
Nitrous oxide (N2O) is a hypnotic gas with anti-depressant and psychedelic properties at subanesthetic concentrations. Despite longstanding clinical use, there is insufficient understanding of its effect on neural dynamics and cortical processing, which is important for mechanistic understanding of its therapeutic effects. We administered subanesthetic (70%), inhaled N2O and studied dynamic changes of spiking rate, spectral content, and somatosensory information representation in primary motor cortex (M1) in two male Rhesus macaques implanted with Utah microelectrode arrays in the hand area of M1. The average, sorted multi-unit spiking rate in M1 increased from 8.1±0.99 to 10.6±1.3 Hz in Monkey W (p < 0.001) and from 5.6±0.87 to 7.0 ± 1.1 Hz in Monkey N (p = 0.003). Power spectral densities increased in beta and gamma band power. To evaluate somatosensory content in M1 as a surrogate of information transfer, fingers were lightly brushed and classified using a naïve Bayes classifier. In both monkeys, the proportion of correctly classified fingers dropped from 0.50±0.06 before N2O to 0.34±0.03 during N2O (p = 0.018), although some fingers continued to be correctly classified (p = 0.005). The decrease in correct classifications corresponded to decreased modulation depth for the population (p = 0.005) and fewer modulated units (p = 0.046). However, the increased single-unit firing rate was not correlated with its modulation depth (R2 < 0.001, p = 0.93). These data suggest that N2O degrades information transfer, although no clear relationship was found between neuronal tuning and N2O-induced changes in firing rate. Significance Statement There are few intra-cortical studies characterizing the influence of nitrous oxide (N2O) on neuronal behavior in the primate brain. Herein we demonstrate increased spiking rate in primary motor cortex (M1) as well as increased beta/gamma power during administration of subanesthetic N2O. In a previously validated model of primary somatosensory to M1 information transfer, we also show a degradation of somatosensory representation. The degraded representation, as assessed by modulation depth, was not correlated with neuronal firing rate changes.This publication has 42 references indexed in Scilit:
- Rapid fragmentation of neuronal networks at the onset of propofol-induced unconsciousnessProceedings of the National Academy of Sciences of the United States of America, 2012
- Neuronal assembly dynamics in the beta1 frequency range permits short-term memoryProceedings of the National Academy of Sciences of the United States of America, 2011
- Neural Correlates of High-Gamma Oscillations (60–200 Hz) in Macaque Local Field Potentials and Their Potential Implications in ElectrocorticographyJournal of Neuroscience, 2008
- NMDA Receptor Hypofunction Produces Opposite Effects on Prefrontal Cortex Interneurons and Pyramidal NeuronsJournal of Neuroscience, 2007
- A beta2-frequency (20–30 Hz) oscillation in nonsynaptic networks of somatosensory cortexProceedings of the National Academy of Sciences of the United States of America, 2006
- Cortico‐cortical mediation of short‐latency (lemniscal) sensory input to the motor cortex in deeply pentobitone anaesthetized catsActa Physiologica Scandinavica, 1995
- Effects of nitrous oxide on global and regional cortical blood flow.Stroke, 1990
- Effects of nitrous oxide on the somatosensory evoked response in catsJournal of Anesthesia, 1990
- The Effects of Ketamine on Cerebral Circulation and Metabolism in ManAnesthesiology, 1972
- A Neurophysiologic Study of Ketamine Anesthesia in the CatAnesthesiology, 1971