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Inhibitory feedback required for network oscillatory responses to communication but not prey stimuli

Nature volume 421, pages 539–543 (2003)Cite this article

Abstract

Stimulus-induced oscillations occur in visual1,2, olfactory3,4,5,6 and somatosensory7 systems. Several experimental2,3,5 and theoretical8,9,10,11,12,13 studies have shown how such oscillations can be generated by inhibitory connections between neurons. But the effects of realistic spatiotemporal sensory input on oscillatory network dynamics and the overall functional roles of such oscillations in sensory processing are poorly understood. Weakly electric fish must detect electric field modulations produced by both prey (spatially localized)14 and communication (spatially diffuse)15 signals. Here we show, through in vivo recordings, that sensory pyramidal neurons in these animals produce an oscillatory response to communication-like stimuli, but not to prey-like stimuli. On the basis of well-characterized circuitry16, we construct a network model of pyramidal neurons that predicts that diffuse delayed inhibitory feedback is required to achieve oscillatory behaviour only in response to communication-like stimuli. This prediction is experimentally verified by reversible blockade of feedback inhibition that removes oscillatory behaviour in the presence of communication-like stimuli. Our results show that a sensory system can use inhibitory feedback as a mechanism to ‘toggle’ between oscillatory and non-oscillatory firing states, each associated with a naturalistic stimulus.

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Figure 1: ELL pyramidal neurons show differential responses to local (prey-like) and global (communication-like) stimuli (n = 15).
Figure 2: ELL neural network simulations involving global inhibitory feedback show differential responses to local and global stimuli.
Figure 3: Simulated asynchronous firing and synchronized oscillations during one presentation of a local or global stimulus, respectively.
Figure 4: Blockade of the inhibitory component of the StF pathway.

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Acknowledgements

We thank J. Lewis, C. Laing, R. W. Turner and M. Higley for reading the manuscript. Funding was provided by the National Science and Engineering Research Council (B.D., M.J.C., A.L.), the Canadian Institutes of Health Research (A.L., L.M.) and the National Institutes of Health (J.B.).

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Authors and Affiliations

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

    Brent Doiron, Maurice J. Chacron & André Longtin

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

    Brent Doiron, Maurice J. Chacron & Leonard Maler

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

    Joseph Bastian

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Correspondence to Brent Doiron.

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Doiron, B., Chacron, M., Maler, L. et al. Inhibitory feedback required for network oscillatory responses to communication but not prey stimuli. Nature 421, 539–543 (2003). https://doi.org/10.1038/nature01360

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