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Internal brain state regulates membrane potential synchrony in barrel cortex of behaving mice

Abstract

Internal brain states form key determinants for sensory perception, sensorimotor coordination and learning1,2. A prominent reflection of different brain states in the mammalian central nervous system is the presence of distinct patterns of cortical synchrony, as revealed by extracellular recordings of the electroencephalogram, local field potential and action potentials. Such temporal correlations of cortical activity are thought to be fundamental mechanisms of neuronal computation3,4,5,6,7,8,9,10,11. However, it is unknown how cortical synchrony is reflected in the intracellular membrane potential (Vm) dynamics of behaving animals. Here we show, using dual whole-cell recordings from layer 2/3 primary somatosensory barrel cortex in behaving mice, that the Vm of nearby neurons is highly correlated during quiet wakefulness. However, when the mouse is whisking, an internally generated state change reduces the Vm correlation, resulting in a desynchronized local field potential and electroencephalogram. Action potential activity was sparse during both quiet wakefulness and active whisking. Single action potentials were driven by a large, brief and specific excitatory input that was not present in the Vm of neighbouring cells. Action potential initiation occurs with a higher signal-to-noise ratio during active whisking than during quiet periods. Therefore, we show that an internal brain state dynamically regulates cortical membrane potential synchrony during behaviour and defines different modes of cortical processing.

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Figure 1: Internal brain state determines membrane potential dynamics.
Figure 2: EEG, LFP and V m are highly correlated during quiet wakefulness but not during active whisking.
Figure 3: Subthreshold membrane potential synchrony in layer 2/3 barrel cortex depends on the internal brain state.
Figure 4: Action potentials result from large, brief and specific input during both quiet wakefulness and whisking.

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Acknowledgements

We thank D. Hill and D. Kleinfeld for help with coherence analyses. We thank S. Crochet, L. Gentet, I. Ferezou and S. Lefort for discussions and critical reading of the manuscript. This work was funded by a Long Term Fellowship from the Human Frontier Science Program and a grant from the Swiss National Science Foundation.

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Correspondence to Carl C. H. Petersen.

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Supplementary Information 1

The file contains Supplementary Figures 1-8 with Legends and the legend to Supplementary Movie 1. (PDF 1752 kb)

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Poulet, J., Petersen, C. Internal brain state regulates membrane potential synchrony in barrel cortex of behaving mice. Nature 454, 881–885 (2008). https://doi.org/10.1038/nature07150

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