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Synaptic dynamics mediate sensitivity to motion independent of stimulus details

Nature Neuroscience volume 7, pages 380–388 (2004)Cite this article

Abstract

Humans and other animals generally perceive motion independently of the cues that define the moving object. To understand the underlying mechanisms of this generalization of stimulus attributes, we have examined the cellular properties of avian wide-field tectal neurons that are sensitive to a variety of moving stimuli but not to static stationary stimuli. This in vitro study showed phasic signal transfer at the retinotectal synapse and binary dendritic responses to synaptic inputs that interact in a mutually exclusive manner in the postsynaptic tectal neuron. A model of the tectal circuitry predicts that these two cellular properties mediate sensitivity to a wide range of dynamic spatiotemporal stimuli, including moving stimuli, but not to static stationary stimuli in a tectal neuron. The computation that is independent of stimulus detail is initiated by tectal neurons and is completed by rotundal neurons that integrate outputs from multiple tectal neurons in a directionally selective manner.

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Figure 1: SGC-I morphology, location of stimulus electrodes and response to synaptic stimulation.
Figure 2: Response of SGC-I neurons to synaptic and direct stimulation of dendritic endings.
Figure 3: Structure of the SGC-I model and the visual stimuli.
Figure 4: Response of the model SGC-I cell to a static stationary (a–d) or moving (e–h) luminance-defined bar stimulus (Fig. 3c).
Figure 5: Response of the SGC-I model to a static stationary (a–d) and uncorrelated second-order motion (e–h) random-dot pattern (Fig. 3d).
Figure 6: Parameter dependence of the SGC-I model response to stationary stimuli and first- and second-order motion.

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Acknowledgements

The authors thank H.J. Karten and D. Kleinfeld for support during the collection of preliminary data, A. Mahani for comments and W.B. Kristan, H. Wagner, G. DeAngelis, M. Ariel, P. Lukasiewicz, J. Sanes and A. Carlsson for critical reading of the manuscript. The work was supported by grants from Deutsche Forschungsgemeinschaft to H.L. and Whitehall Foundation and McDonnell Center for Higher Brain Function to R.W.

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Authors and Affiliations

  1. Institute of Biology II, Rheinisch-Westfälische Technische Hochschule Aachen, Aachen, 52074, Germany

    Harald Luksch

  2. Department of Physics, CB 1105, Washington University, St. Louis, 63130, Missouri, USA

    Reza Khanbabaie & Ralf Wessel

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Correspondence to Ralf Wessel.

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Luksch, H., Khanbabaie, R. & Wessel, R. Synaptic dynamics mediate sensitivity to motion independent of stimulus details. Nat Neurosci 7, 380–388 (2004). https://doi.org/10.1038/nn1204

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