Abstract

Neural responses in the cerebral cortex change dramatically between the ‘synchronized’ state during sleep and ‘desynchronized’ state during wakefulness. Our understanding of cortical state emerges largely from experiments performed in sensory areas of head-fixed or tethered rodents due to technical limitations of recording from larger freely-moving animals for several hours. Here, we report a system integrating wireless electrophysiology, wireless eye tracking, and real-time video analysis to examine the dynamics of population activity in a high-level, executive area – dorsolateral prefrontal cortex (dlPFC) of unrestrained monkey. This technology allows us to identify cortical substates during quiet and active wakefulness, and transitions in population activity during rest. We further show that narrow-spiking neurons exhibit stronger synchronized fluctuations in population activity than broad-spiking neurons regardless of state. Our results show that cortical state is controlled by behavioral demands and arousal by asymmetrically modulating the slow response fluctuations of local excitatory and inhibitory cell populations.

Highlights

  • Neural responses in the cerebral cortex change dramatically between the ‘synchronized’ state during sleep and ‘desynchronized’ state during wakefulness

  • Despite the prevalence of these ideas, previous investigations of cortical state dynamics at single cell resolution have been performed in rodent sensory cortex while technical limitations have prevented the analysis of dynamic cortical states in larger animals freely moving in their environment for many hours

  • We performed wireless recordings using a 96-channel multielectrode array implanted in the dorsolateral prefrontal cortex of two freelymoving monkeys (Fig. 1a and Supplementary Fig. 1; sessions lasted 195 min on average)

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Summary

Results

Integrated wireless system to examine brain states in monkey. We developed an integrated system for large-scale electrophysiology, eye tracking, and behavioral state classification in freely-moving macaque monkey. Narrow-spiking units have been reported to fire for a brief phase of the cortical slow oscillation, which could further increase low-frequency synchrony[30,31] To determine if both subpopulations are modulated differently by quiet and active wakefulness, we normalized the PSI values in these states to their rest values. Consistent with past work[27,28], narrow-spiking neurons comprised 16% of the overall population and had significantly higher firing rates than broad-spiking cells (Wilcoxon rank-sum test, p < 0.01; mean rates 5.63 sp/s and 4.02 sp/s, respectively; Fig. 4b) Firing rates of both subpopulations were influenced by behavioral state, with highest firing rates occurring in the active state and lowest in rest (Fig. 4c; p < 0.001, Friedman test; p < 0.001, Wilcoxon signed-rank test with Bonferroni correction for pairwise comparisons). The dynamic shift towards inhibition observed during rest implies an active role of inhibitory

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