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Neural mechanism underlying complex receptive field properties of motion-sensitive interneurons

Abstract

In many species, neurons responding to visual motion at higher processing stages are often specifically tuned to particular flow fields; however, the neural circuitry that leads to this selectivity is not yet understood. Here we have studied this problem in 'vertical system' (VS) cells of the blowfly lobula plate. These neurons possess distinctive local preferred directions in different parts of their receptive field. Dual recordings from pairs of VS cells show that they are electrically coupled. This coupling is responsible for the elongated horizontal extent of their receptive fields. VS cells with a lateral receptive field have additional connections to a VS cell with a frontal receptive field and to the horizontal system, tuning these cells to rotational flow fields. In summary, the receptive field of these cells consists of two components: one that they receive from local motion detectors on their dendrite, and one that they import from other large-field neurons.

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Figure 1: Response characteristics of VS cells.
Figure 2: VS cells are electrically coupled.
Figure 3: Connectivity between VS cells.
Figure 4: EPSP analysis in VS7/8.
Figure 5: Two-photon imaging of VS cells.

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Acknowledgements

We are grateful to R. Gleich for excellent technical assistance. This work was supported by the Max-Planck-Society.

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Correspondence to Juergen Haag.

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The authors declare no competing financial interests.

Supplementary information

Supplementary Fig. 1

Possible wiring scheme for the VS7/8-cell. (a) Schematic drawing of the receptive field of VS7/8. It shows three features: I a broad vertical sensitivity for downward motion, II an upward sensitivity in the frontal part of the receptive field and III a horizontal sensitivity in the dorsal visual field. (b) Underlying network: VS7/8 is connected to its neighboring VS-cell (VS6 and VS9) through electrical synapses, resulting in a broad vertical sensitivity for downward motion (I). It receives inhibitory input from VS1 which itself is excited by downward motion in the frontal visual field. This causes the upward sensitivity found in VS7/8 (II). In addition VS7/8 is electrically coupled to a spiking neuron (X) that is responsible for the EPSPs measured in VS7/8. The spiking neuron receives excitatory input from HSN. This connection results in the horizontal sensitivity of VS7/8 in the dorsal part of the receptive field (III). (JPG 17 kb)

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Haag, J., Borst, A. Neural mechanism underlying complex receptive field properties of motion-sensitive interneurons. Nat Neurosci 7, 628–634 (2004). https://doi.org/10.1038/nn1245

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