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Non-classical receptive field mediates switch in a sensory neuron's frequency tuning

Nature volume 423, pages 77–81 (2003)Cite this article

A Corrigendum to this article was published on 26 June 2003

Abstract

Animals have developed stereotyped communication calls to which specific sensory neurons are well tuned1,2. These communication calls must be discriminated from environmental signals such as those produced by prey. Sensory systems might have evolved neural circuitry to encode both categories. In weakly electric fish, prey and communication signals differ in their spatial extent and frequency content3,4. Here we show that stimuli of different spatial extents mimicking prey and communication signals cause a switch in the frequency tuning and spike-timing precision of electrosensory pyramidal neurons, resulting in the selective and optimal encoding of both stimulus categories. As in other sensory systems5, pyramidal neurons respond only to stimuli located within a restricted region of space known as the classical receptive field (CRF)6. In some systems, stimulation outside the CRF but within a non-classical receptive field (nCRF) can modulate the neural response to CRF stimulation even though nCRF stimulation alone fails to elicit responses7,8. We show that pyramidal neurons possess a nCRF and that it can modulate the response to CRF stimuli to induce this neurobiological switch in frequency tuning.

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Figure 1: ELL pyramidal neurons display differential frequency tuning to local and global stimulation geometries.
Figure 2: Spike timing reliability and precision under local and global stimulation geometries.
Figure 3: The nCRF mediates pyramidal neuron frequency tuning.

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Acknowledgements

We thank A.-M. Oswald, J. Lewis and B. Lindner for their reading the manuscript. This research was supported by NSERC (M.J.C., B.D., A.L.), CIHR (L.M., A.L.) and NIH (J.B.).

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Authors and Affiliations

  1. Physics Department, University of Ottawa, Ottawa, Ontario, K1N 6N5, Canada

    Maurice J. Chacron, Brent Doiron & André Longtin

  2. Department of Cellular and Molecular Medicine, University of Ottawa, Ottawa, Ontario, K1H 8M5, Canada

    Maurice J. Chacron, Brent Doiron & Leonard Maler

  3. Department of Zoology, University of Oklahoma, Oklahoma, Norman, 73019, USA

    Joseph Bastian

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  1. Maurice J. Chacron
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Correspondence to Maurice J. Chacron.

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Chacron, M., Doiron, B., Maler, L. et al. Non-classical receptive field mediates switch in a sensory neuron's frequency tuning. Nature 423, 77–81 (2003). https://doi.org/10.1038/nature01590

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