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Inhibition dominates sensory responses in the awake cortex

A Corrigendum to this article was published on 10 July 2013

This article has been updated

Abstract

The activity of the cerebral cortex is thought to depend on the precise relationship between synaptic excitation and inhibition1,2,3,4. In the visual cortex, in particular, intracellular measurements have related response selectivity to coordinated increases in excitation and inhibition5,6,7,8,9. These measurements, however, have all been made during anaesthesia, which strongly influences cortical state10 and therefore sensory processing7,11,12,13,14,15. The synaptic activity that is evoked by visual stimulation during wakefulness is unknown. Here we measured visually evoked responses—and the underlying synaptic conductances—in the visual cortex of anaesthetized and awake mice. Under anaesthesia, responses could be elicited from a large region of visual space16 and were prolonged. During wakefulness, responses were more spatially selective and much briefer. Whole-cell patch-clamp recordings of synaptic conductances5,17 showed a difference in synaptic inhibition between the two conditions. Under anaesthesia, inhibition tracked excitation in amplitude and spatial selectivity. By contrast, during wakefulness, inhibition was much stronger than excitation and had extremely broad spatial selectivity. We conclude that during wakefulness, cortical responses to visual stimulation are dominated by synaptic inhibition, restricting the spatial spread and temporal persistence of neural activity. These results provide a direct glimpse of synaptic mechanisms that control sensory responses in the awake cortex.

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Figure 1: Spontaneous and evoked activity in the anaesthetized and awake visual cortex (V1).
Figure 2: Anaesthetized responses are long lasting regardless of cortical state.
Figure 3: Responses are spatiotemporally restricted during waking.
Figure 4: Visually evoked conductance is dominated by inhibition in awake V1.

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Acknowledgements

We thank T. Sato, A. Saleem and A. Ayaz for help with procedures; S. L. Smith, C. Schmidt-Hieber and K. Powell for advice on recordings, and A. Roth, M. Scanziani and D. McCormick for comments. We are grateful to the National Science Foundation, the European Research Council, the Wellcome Trust, the Medical Research Council and the Gatsby Charitable Foundation for financial support. M.C. holds the GlaxoSmithKline/Fight for Sight Chair in Visual Neuroscience.

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B.H. performed the experiments. B.H. and M.C. performed the analyses. B.H., M.H. and M.C. designed the study and wrote the paper.

Corresponding author

Correspondence to Bilal Haider.

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The authors declare no competing financial interests.

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This file contains Supplementary Figures 1-11. Supplementary Figure 8 was corrected on 10 July 2013; see corrigendum linked to original manuscript for details. (PDF 936 kb)

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Haider, B., Häusser, M. & Carandini, M. Inhibition dominates sensory responses in the awake cortex. Nature 493, 97–100 (2013). https://doi.org/10.1038/nature11665

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