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Independent control of reciprocal and lateral inhibition at the axon terminal of retinal bipolar cells

Authors


M. Tachibana: Department of Psychology, Graduate School of Humanities and Sociology, The University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-0033, Japan. Email: tchbn2ms@l.u-tokyo.ac.jp

Key points

  • • Two different forms of feedback inhibition, reciprocal and lateral inhibition, are ubiquitously observed throughout the nervous system.
  • • In the retina, the axon terminal of bipolar cells receives reciprocal and lateral GABAergic inhibitory inputs from amacrine cells, but how a variety of visual inputs activate each inhibition remains largely unexplored.
  • • Here we show that each inhibition is independently controlled by different types of bipolar cell outputs; reciprocal inhibition is driven by strong output from each bipolar cell, whereas lateral inhibition is driven by outputs from multiple bipolar cells even when each output is weak.
  • • Composition of transmitter receptors and localization of Na+ channels were different between two inhibitory pathways, suggesting that different amacrine cells may mediate each inhibition.
  • • The dual feedback inhibition can cooperatively reduce bipolar cell outputs in response to various visual inputs without deteriorating the quality of visual signals, thereby contributing to efficient signal transmission in the visual pathway.

Abstract  Bipolar cells (BCs), the second order neurons in the vertebrate retina, receive two types of GABAergic feedback inhibition at their axon terminal: reciprocal and lateral inhibition. It has been suggested that two types of inhibition may be mediated by different pathways. However, how each inhibition is controlled by excitatory BC output remains to be clarified. Here, we applied single/dual whole cell recording techniques to the axon terminal of electrically coupled BCs in slice preparation of the goldfish retina, and found that each inhibition was regulated independently. Activation voltage of each inhibition was different: strong output from a single BC activated reciprocal inhibition, but could not activate lateral inhibition. Outputs from multiple BCs were essential for activation of lateral inhibition. Pharmacological examinations revealed that composition of transmitter receptors and localization of Na+ channels were different between two inhibitory pathways, suggesting that different amacrine cells may mediate each inhibition. Depending on visual inputs, each inhibition could be driven independently. Model simulation showed that reciprocal and lateral inhibition cooperatively reduced BC outputs as well as background noise, thereby preserving high signal-to-noise ratio. Therefore, we conclude that excitatory BC output is efficiently regulated by the dual operating mechanisms of feedback inhibition without deteriorating the quality of visual signals.

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