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Multiplicative computation in a visual neuron sensitive to looming

Nature volume 420, pages 320–324 (2002)Cite this article

Abstract

Multiplicative operations are important in sensory processing1,2,3,4,5, but their biophysical implementation remains largely unknown5,6,7,8,9,10. We investigated an identified neuron (the lobula giant movement detector, LGMD, of locusts) whose output firing rate in response to looming visual stimuli has been described by two models, one of which involves a multiplication. In this model, the LGMD multiplies postsynaptically two inputs (one excitatory, one inhibitory) that converge onto its dendritic tree11,12; in the other model, inhibition is presynaptic to the LGMD13,14. By using selective activation and inactivation of pre- and postsynaptic inhibition, we show that postsynaptic inhibition has a predominant role, suggesting that multiplication is implemented within the neuron itself. Our pharmacological experiments and measurements of firing rate versus membrane potential also reveal that sodium channels act both to advance the response of the LGMD in time and to map membrane potential to firing rate in a nearly exponential manner. These results are consistent with an implementation of multiplication based on dendritic subtraction of two converging inputs encoded logarithmically, followed by exponentiation through active membrane conductances.

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Figure 1: Properties of a neuronal circuit involved in locust escape behaviour and obstacle avoidance.
Figure 2: Effect of activating lateral or feedforward inhibition on peak firing time (magenta lines).
Figure 3: Effect of picrotoxin (PCTX) on the LGMD's responses to approaching stimuli.
Figure 4: Transformation between membrane potential (Vm) and firing rate at the spike initiation zone.

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Acknowledgements

We thank C. Mo for technical assistance with the experiments presented in Fig. 2, S. Potter for help with two-photon confocal microscopy, and J. Maunsell for comments. This work was supported by the Sloan Foundation, the National Institute of Mental Health (F.G., C.K.), the National Institute for Deafness and Communication Disorders (G.L.), the McKnight Foundation (G.L.) and the Center for Neuromorphic Engineering as part of the NSF Engineering Research Center programme. H.G.K. was supported by a travel grant of the Deutsche Forschungsgemeinschaft. F.G. is an Alfred P. Sloan research fellow.

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Authors and Affiliations

  1. Division of Biology, California Institute of Technology, California, 91125, Pasadena, USA

    Fabrizio Gabbiani, Holger G. Krapp, Christof Koch & Gilles Laurent

  2. Division of Neuroscience, Baylor College of Medicine, One Baylor Plaza, Texas, 77030, Houston, USA

    Fabrizio Gabbiani

  3. Department of Zoology, University of Cambridge, Downing Street, CB2 3EJ, Cambridge, UK

    Holger G. Krapp

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  1. Fabrizio Gabbiani
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Correspondence to Fabrizio Gabbiani.

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Gabbiani, F., Krapp, H., Koch, C. et al. Multiplicative computation in a visual neuron sensitive to looming. Nature 420, 320–324 (2002). https://doi.org/10.1038/nature01190

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