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Supralinear increase of recurrent inhibition during sparse activity in the somatosensory cortex

Nature Neuroscience volume 10, pages 743–753 (2007)Cite this article

A Corrigendum to this article was published on 01 August 2007

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Abstract

The balance between excitation and inhibition in the cortex is crucial in determining sensory processing. Because the amount of excitation varies, maintaining this balance is a dynamic process; yet the underlying mechanisms are poorly understood. We show here that the activity of even a single layer 2/3 pyramidal cell in the somatosensory cortex of the rat generates widespread inhibition that increases disproportionately with the number of active pyramidal neurons. This supralinear increase of inhibition results from the incremental recruitment of somatostatin-expressing inhibitory interneurons located in layers 2/3 and 5. The recruitment of these interneurons increases tenfold when they are excited by two pyramidal cells. A simple model demonstrates that the distribution of excitatory input amplitudes onto inhibitory neurons influences the sensitivity and dynamic range of the recurrent circuit. These data show that through a highly sensitive recurrent inhibitory circuit, cortical excitability can be modulated by one pyramidal cell.

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Figure 1: Unitary recurrent inhibitory circuits.
Figure 2: Supralinear increase of inhibition.
Figure 3: Intra- and translaminar recurrent inhibitory circuits.
Figure 4: Spike timing of somatostatin-positive interneurons determines the time course of recurrent inhibition.
Figure 5: Increase in the recruitment of somatostatin-expressing interneurons.
Figure 6: Model describing range and sensitivity of recurrent inhibition.

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  • 11 July 2007

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Notes

  1. *NOTE: In the version of this article initially published, the authors neglected to cite a related paper that was published during the review process. At the end of the Introduction, the following sentences should have been included: “During the revision of this manuscript, another group reported the presence of a recurrent inhibitory circuit with similar properties to the one described here in layer 5 of the somatosensory cortex42. Together, these findings suggest common principles of operation of elementary circuits across cortical layers.” In the reference list, the following reference should have been included: “42. Silberberg, G. & Markram, H. Disynaptic inhibition between neocortical pyramidal cells mediated by Martinotti cells. Neuron 53, 735-746 (2007).” The error has been corrected in the HTML and PDF versions of the article.

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Acknowledgements

We are very grateful to F. Pouille for contributing to some of the experiments included in this study. We thank J. Isaacson, E. Flister and the members of the Scanziani lab for comments on the manuscript and their continuous support. This work was funded by the US National Institutes of Health (MH71401 and MH70058). L.L.G. was supported by a predoctoral National Research Service Award grant (1-F31NS056529-01).

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Author notes

  1. Christoph Kapfer

    Present address: Current address: Max Planck Institute of Neurobiology, Am Klopferspitz 18, 82152 Martinsried, Germany.,

  2. Lindsey L Glickfeld and Bassam V Atallah: These authors contributed equally to this work.

Authors and Affiliations

  1. Division of Biology, Neuroscience Graduate Program and Neurobiology Section, University of California San Diego, 9500 Gilman Drive, La Jolla, California, 92093-0634, USA

    Christoph Kapfer, Lindsey L Glickfeld, Bassam V Atallah & Massimo Scanziani

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Correspondence to Massimo Scanziani.

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Supplementary information

Supplementary Fig. 1

Monosynaptic excitation between layer 2/3 pyramidal cells. (PDF 132 kb)

Supplementary Fig. 2

Model for SOM interneuron activation with three action potentials. (PDF 245 kb)

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Kapfer, C., Glickfeld, L., Atallah, B. et al. Supralinear increase of recurrent inhibition during sparse activity in the somatosensory cortex. Nat Neurosci 10, 743–753 (2007). https://doi.org/10.1038/nn1909

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