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Centre–surround inhibition among olfactory bulb glomeruli

Nature volume 426, pages 623–629 (2003)Cite this article

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Abstract

Centre–surround inhibition—the suppression of activity of neighbouring cells by a central group of neurons—is a fundamental mechanism that increases contrast in patterned sensory processing. The initial stage of neural processing in olfaction occurs in olfactory bulb glomeruli, but evidence for functional interactions between glomeruli is fragmentary. Here we show that the so-called ‘short axon’ cells, contrary to their name, send interglomerular axons over long distances to form excitatory synapses with inhibitory periglomerular neurons up to 20–30 glomeruli away. Interglomerular excitation of these periglomerular cells potently inhibits mitral cells and forms an on-centre, off-surround circuit. This interglomerular centre–surround inhibitory network, along with the well-established mitral–granule–mitral inhibitory circuit, forms a serial, two-stage inhibitory circuit that could enhance spatiotemporal responses to odours.

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Figure 1: Extensive interglomerular connections shown by DiI and microbead tracing.
Figure 2: Interglomerular connections derive from non-GABAergic ‘short axon’ cells.
Figure 3: Functional imaging shows extensive interglomerular excitation.
Figure 4: Interglomerular connections excite juxtaglomerular cells.
Figure 5: Interglomerular connections inhibit mitral cell responses to olfactory nerve input.
Figure 6: Centre–surround inhibitory networks in the olfactory bulb.

Change history

  • 27 March 2018

    This article was initially published with an incorrect DOI that did not match the registered version at Crossref. The DOI has been corrected in the article.

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Acknowledgements

The authors thank F. L. Margolis for expert assistance in ZnSO4 epithelium lesions and A. Keller for valuable comments on the manuscript. This work was supported by the National Institute on Deafness and Other Communication Disorders.

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Author notes

  1. P. M. Heyward

    Present address: Department of Physiology, Otago School of Medical Sciences, University of Otago, Dunedin, 9001, New Zealand

  2. J. L. Aungst, P. M. Heyward and A. C. Puche: These authors contributed equally to this work

Authors and Affiliations

  1. Department of Anatomy and Neurobiology, Program in Neuroscience, The University of Maryland School of Medicine, Room 222, 685 West Baltimore Street, Maryland, 21201, Baltimore, USA

    J. L. Aungst, P. M. Heyward, A. C. Puche, S. V. Karnup, A. Hayar & M. T. Shipley

  2. Department of Gene Technology and Developmental Neurobiology, Institute of Experimental Medicine, Budapest, Hungary

    G. Szabo

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Aungst, J., Heyward, P., Puche, A. et al. Centre–surround inhibition among olfactory bulb glomeruli. Nature 426, 623–629 (2003). https://doi.org/10.1038/nature02185

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