Abstract
Neocortical GABAergic neurons have diverse molecular, structural and electrophysiological features, but the functional correlates of this diversity are largely unknown. We found unique membrane potential dynamics of somatostatin-expressing (SOM) neurons in layer 2/3 of the primary somatosensory barrel cortex of awake behaving mice. SOM neurons were spontaneously active during periods of quiet wakefulness. However, SOM neurons hyperpolarized and reduced action potential firing in response to both passive and active whisker sensing, in contrast with all other recorded types of nearby neurons, which were excited by sensory input. Optogenetic inhibition of SOM neurons increased burst firing in nearby excitatory neurons. We hypothesize that the spontaneous activity of SOM neurons during quiet wakefulness provides a tonic inhibition to the distal dendrites of excitatory pyramidal neurons. Conversely, the inhibition of SOM cells during active cortical processing likely enhances distal dendritic excitability, which may be important for top-down computations and sensorimotor integration.
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04 March 2012
In the version of this article initially published online, the legend for Supplementary Movie 1 was missing. The error has been corrected for the HTML version of this article.
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Acknowledgements
We thank L. Looger (Howard Hughes Medical Institute, Janelia Farm) for GCaMP3 and K. Deisseroth (Stanford University) for eNpHR3.0. This work was funded by grants from the Swiss National Science Foundation (C.C.H.P.), Human Frontiers in Science Program (C.C.H.P.), SystemsX.ch (C.C.H.P.) and Deutsche Forschungsgemeinschaft (Sta 431/8-1, 10-1 to J.F.S.), and a joint Deutsche Forschungsgemeinschaft/Swiss National Science Foundation grant Bacofun (C.C.H.P. and J.F.S.).
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L.J.G. carried out all of the membrane potential recordings and analyzed the data. Y.K. carried out all of the GCaMP3 imaging experiments and analyzed the data. H.T. and Z.J.H. provided unpublished genetically engineered mice. J.F.S. carried out all of the immunohistochemistry and analyzed the data. C.C.H.P. contributed to the design of experiments, supervised the project and wrote the manuscript. All of the authors commented on the manuscript.
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Supplementary Figures 1–9 (PDF 6653 kb)
Supplementary Movie 1
GCaMP3 was expressed in excitatory neurons of the barrel cortex of an Emx1-Cre mouse using an AAV-FLEX vector. Fluorescence of layer 1 dendrites in the awake head-restrained mouse was imaged using a two-photon microscope. Whisker movements were filmed simultaneously with the calcium imaging. When the mouse moves its whiskers, the dendrites in layer 1 increase fluorescence. (MOV 12306 kb)
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Gentet, L., Kremer, Y., Taniguchi, H. et al. Unique functional properties of somatostatin-expressing GABAergic neurons in mouse barrel cortex. Nat Neurosci 15, 607–612 (2012). https://doi.org/10.1038/nn.3051
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DOI: https://doi.org/10.1038/nn.3051