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Different receptive fields in axons and dendrites underlie robust coding in motion-sensitive neurons

Nature Neuroscience volume 12, pages 327–332 (2009)Cite this article

Abstract

In the visual system of the blowfly Calliphora vicina, neurons of the vertical system (VS cells) integrate wide-field motion information from a retinotopic array of local motion detectors. In vivo calcium imaging reveals two distinct and separate receptive fields in these cells: a narrow dendritic receptive field corresponding to feedforward input from the local motion detectors and a broad axon terminal receptive field that additionally incorporates input from neighboring cells mediated by lateral axo-axonal gap junctions. We show that the axon terminal responses are linear interpolations of the dendritic responses, resulting in a robust population coding of optic flow parameters as predicted by previous modeling studies. Compartmental modeling shows that spatially separating the axonal gap junctions from the conductive load of the dendritic synapses increases the coupling strength of the gap junctions, making this interpolation possible.

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Figure 1: Broadening of VS cells' receptive fields within single cells.
Figure 2: Voltage clamping of dendritic input.
Figure 3: Interpolation of dendritic responses in the axon terminal.
Figure 4: Axon terminal coupling of model VS cells results in more robust population coding than dendritic coupling.

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Acknowledgements

We thank Y. Choe for useful comments on an early version of the manuscript, D. Spavieri Jr. for helpful discussions and R. Gleich for technical assistance. This study was supported by the Max Planck Society and by the Bernstein Center for Computational Neuroscience. Y.M.E. was partially supported by a Minerva Foundation fellowship from the Max Planck Society.

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Authors and Affiliations

  1. Department of Systems and Computational Neurobiology, Max Planck Institute of Neurobiology, Am Klopferspitz 18, Martinsried, 82152, Germany

    Yishai M Elyada, Juergen Haag & Alexander Borst

  2. Bernstein Center for Computational Neuroscience Munich, Marchioninistrasse 23, Munich, 81377, Germany

    Juergen Haag & Alexander Borst

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  1. Yishai M Elyada
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Contributions

Y.M.E., J.H. and A.B. collectively designed the experiments; Y.M.E. performed the experiments and simulations and evaluated the data; and Y.M.E., J.H. and A.B. collectively wrote the manuscript.

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Correspondence to Alexander Borst.

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Supplementary Figures 1–6, Supplementary Table 1 and Supplementary Methods (PDF 597 kb)

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Elyada, Y., Haag, J. & Borst, A. Different receptive fields in axons and dendrites underlie robust coding in motion-sensitive neurons. Nat Neurosci 12, 327–332 (2009). https://doi.org/10.1038/nn.2269

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