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Activity-dependent gating of lateral inhibition in the mouse olfactory bulb

Nature Neuroscience volume 11, pages 80–87 (2008)Cite this article

Abstract

Lateral inhibition is a circuit motif found throughout the nervous system that often generates contrast enhancement and center-surround receptive fields. We investigated the functional properties of the circuits mediating lateral inhibition between olfactory bulb principal neurons (mitral cells) in vitro. We found that the lateral inhibition received by mitral cells is gated by postsynaptic firing, such that a minimum threshold of postsynaptic activity is required before effective lateral inhibition is recruited. This dynamic regulation allows the strength of lateral inhibition to be enhanced between cells with correlated activity. Simulations show that this regulation of lateral inhibition causes decorrelation of mitral cell activity that is evoked by similar stimuli, even when stimuli have no clear spatial structure. These results show that this previously unknown mechanism for specifying lateral inhibitory connections allows functional inhibitory connectivity to be dynamically remapped to relevant populations of neurons.

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Figure 1: Activity-dependent gating of lateral inhibition.
Figure 2: Activity-dependent gating of lateral inhibition in mitral cell pairs.
Figure 3: Summary results of activity-dependent lateral inhibition.
Figure 4: Lateral inhibition evoked by direct stimulation of granule cells.
Figure 5: Overlapping and cooperative activation of granule cells following mitral cell stimulation.
Figure 6: Activity-dependent lateral inhibition enhances contrast and decorrelates similar patterns of activity.

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Acknowledgements

Thanks to A.T. Schaefer and members of the Urban laboratory for helpful comments and discussion. This work was supported by the grants from the National Institute of Deafness and Other Communication Disorders (F30 DC008274, A.A.; R01 DC005798, N.U.) and by a fellowship from the National Science Foundation Integrative Graduate Education and Research Traineeship program (NSF DGE-9987588, A.A.).

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Authors and Affiliations

  1. Center for Neuroscience, University of Pittsburgh, A210 Langley Hall, Pittsburgh, 15260, Pennsylvania, USA

    Armen C Arevian & Nathaniel N Urban

  2. Center for the Neural Basis of Cognition, 4400 Fifth Avenue, Pittsburgh, 15213, Pennsylvania, USA

    Armen C Arevian, Vikrant Kapoor & Nathaniel N Urban

  3. Department of Biology, Carnegie Mellon University, 4400 Fifth Avenue, Pittsburgh, 15213, Pennsylvania, USA

    Vikrant Kapoor & Nathaniel N Urban

Authors
  1. Armen C Arevian
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  3. Nathaniel N Urban
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Contributions

A.A. and N.U. designed all experiments (including computational) except for those in Figure 5, which were designed by V.K. and N.U. A.A. conducted and analyzed all experiments except for those in Figure 5, which were conducted and analyzed by V.K. A.A. and N.U. wrote the manuscript.

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Correspondence to Nathaniel N Urban.

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Arevian, A., Kapoor, V. & Urban, N. Activity-dependent gating of lateral inhibition in the mouse olfactory bulb. Nat Neurosci 11, 80–87 (2008). https://doi.org/10.1038/nn2030

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