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Nonlinear, binocular interactions underlying flow field selectivity of a motion-sensitive neuron

Abstract

Neurons in many species have large receptive fields that are selective for specific optic flow fields. Here, we studied the neural mechanisms underlying flow field selectivity in lobula plate tangential cells (LPTCs) of the blowfly. Among these cells, the H2 cell responds preferentially to visual stimuli approximating rotational optic flow. Through double recordings from H2 and many other LPTCs, we characterized a bidirectional commissural pathway that allows visual information to be shared between the hemispheres. This pathway is mediated by axo-axonal electrical coupling of H2 and the horizontal system equatorial (HSE) cell located in the opposite hemisphere. Using single-cell ablations, we found that this pathway is sufficient to allow H2 to amplify and attenuate dendritic input during binocular visual stimuli. This is accomplished through a modulation of H2's membrane potential by input from the contralateral HSE cell, which scales the firing rate of H2 during visual stimulation but is not sufficient to induce action potentials.

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Figure 1: Network connections.
Figure 2: Flow field selectivity of H2.
Figure 3: Double intracellular recording of H2 and HSE cells in opposite hemispheres.
Figure 4: Connectivity between H2 and the different HS and CH cells located in the opposite lobula plate.
Figure 5: H2 EPSP comparison.
Figure 6: Double ablations of ipsilateral CH cells.
Figure 7: Block of HS and CH cells in the opposite hemisphere.
Figure 8: Simulations of experiments shown in Figure 7.

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Acknowledgements

We would like to thank R.H. Masland for carefully reading an earlier version of this manuscript.

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K.F. and J.H. performed the experiments and analyzed the data. K.F. carried out the computer simulations. K.F., J.H. and A.B. jointly planned the experiments, discussed the results and wrote the manuscript.

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Correspondence to Karl Farrow.

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Farrow, K., Haag, J. & Borst, A. Nonlinear, binocular interactions underlying flow field selectivity of a motion-sensitive neuron. Nat Neurosci 9, 1312–1320 (2006). https://doi.org/10.1038/nn1769

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