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

Author

Listed:
  • Brent Doiron

    (University of Ottawa
    University of Ottawa)

  • Maurice J. Chacron

    (University of Ottawa
    University of Ottawa)

  • Leonard Maler

    (University of Ottawa)

  • André Longtin

    (University of Ottawa)

  • Joseph Bastian

    (University of Oklahoma)

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.

Suggested Citation

  • Brent Doiron & Maurice J. Chacron & Leonard Maler & André Longtin & Joseph Bastian, 2003. "Inhibitory feedback required for network oscillatory responses to communication but not prey stimuli," Nature, Nature, vol. 421(6922), pages 539-543, January.
  • Handle: RePEc:nat:nature:v:421:y:2003:i:6922:d:10.1038_nature01360
    DOI: 10.1038/nature01360
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    Cited by:

    1. Ling Li & Shasha Li & Wenhai Wang & Jielian Zhang & Yiming Sun & Qunrui Deng & Tao Zheng & Jianting Lu & Wei Gao & Mengmeng Yang & Hanyu Wang & Yuan Pan & Xueting Liu & Yani Yang & Jingbo Li & Nengjie, 2024. "Adaptative machine vision with microsecond-level accurate perception beyond human retina," Nature Communications, Nature, vol. 15(1), pages 1-11, December.

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