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Spike frequency adaptation mediates looming stimulus selectivity in a collision-detecting neuron

Nature Neuroscience volume 12, pages 318–326 (2009)Cite this article

Abstract

How active membrane conductance dynamics tunes neurons for specific time-varying stimuli remains poorly understood. We studied the biophysical mechanisms by which spike frequency adaptation shapes visual stimulus selectivity in an identified visual interneuron of the locust. The lobula giant movement detector (LGMD) responds preferentially to objects approaching on a collision course with the locust. Using calcium imaging, pharmacology and modeling, we show that spike frequency adaptation in the LGMD is mediated by a Ca2+-dependent potassium conductance closely resembling those associated with 'small-conductance' (SK) channels. Intracellular block of this conductance minimally affected the LGMD's response to approaching stimuli, but substantially increased its response to translating ones. Thus, spike frequency adaptation contributes to the neuron's tuning by selectively decreasing its responses to nonpreferred stimuli. Our results identify a new mechanism by which spike frequency adaptation may tune visual neurons to behaviorally relevant stimuli.

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Figure 1: LGMD morphology and response to looming versus translating stimuli.
Figure 2: Spike frequency adaptation in the LGMD results from an SK-like KCa conductance.
Figure 3: Intracellular block of spike frequency adaptation (SFA) in vivo enhances the responses to translating motion.
Figure 4: Block of spike frequency adaptation has little effect on the time-course of looming response.
Figure 5: Calcium entry is confined to a region of the LGMD close to the spike initiation zone during depolarizing current injection.
Figure 6: LGMD compartmental model reproduces in vivo current injection and visual stimulation results, both before and after block of spike frequency adaptation by simulated BAPTA iontophoresis.

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Acknowledgements

We would like to thank K. Josic and H. Krapp for comments. This work was supported by grants from the US National Institute of Mental Health. The use of the QNX 6 OS was made possible by QNX Software Systems' Educational Program.

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Authors and Affiliations

  1. Department of Neuroscience, Baylor College of Medicine, One Baylor Plaza, Houston, 77030, Texas, USA

    Simon Peron & Fabrizio Gabbiani

  2. Department of Computational and Applied Mathematics, Rice University, 6100 Main Street MS 134, Houston, 77005, Texas, USA

    Fabrizio Gabbiani

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  1. Simon Peron
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S.P. performed the experiments and simulations; S.P. and F.G. wrote the manuscript; F.G. supervised the project.

Corresponding author

Correspondence to Fabrizio Gabbiani.

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Supplementary Figures 1–7, Supplementary Methods and Supplementary Pharmacology (PDF 2130 kb)

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Peron, S., Gabbiani, F. Spike frequency adaptation mediates looming stimulus selectivity in a collision-detecting neuron. Nat Neurosci 12, 318–326 (2009). https://doi.org/10.1038/nn.2259

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