Circuits - Computation - Models: Fly Motion Vision

Fly Motion Vision

<div style="text-align: justify;"><strong>Optic flow guided course control</strong>. Optic flow is generated by the fly's own movements. Visual stimuli excite the retina (in red). Photoreceptor signals are processed by a sequence of neuropile layers each built in a retinotopic columnar fashion. At the level of the lobula plate, the optic flow is neutrally represented by a 2D array of local motion-sensitive neurons. Their output signals become integrated by large-field lobula plate tangential cells.</div> Zoom Image
Optic flow guided course control. Optic flow is generated by the fly's own movements. Visual stimuli excite the retina (in red). Photoreceptor signals are processed by a sequence of neuropile layers each built in a retinotopic columnar fashion. At the level of the lobula plate, the optic flow is neutrally represented by a 2D array of local motion-sensitive neurons. Their output signals become integrated by large-field lobula plate tangential cells.
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Whenever a seeing organism moves through its environment, the images of the environment shift across its eyes. The resulting distribution of motion vectors on the retina is called ‘optic flow’. Optic flow is a rich source of information about the animal’s own movement and is therefore used extensively for visual course control. This is particularly pronounced in fast flying animals such as flies which are highly specialized for motion vision. We are interested in how motion information from the changing retinal images is computed in the fly visual system, and how this information is decoded for flight control. In general, this processing is done in two steps: First, local motion vectors are calculated from local changes in retinal brightness. From the resulting vector fields (the ‘neural optic flow’), important course control parameters are extracted in a second step.

The fly visual system consists of four successive visual neuropile layers each built from repetitive columns arranged in a retinotopic way: the lamina, the medulla, the lobula and the lobula plate. Fly photoreceptors R1-6 synapse, either directly or indirectly, onto 5 different lamina neurons. From this group, lamina neurons L1 and L2 form the inputs to separate and independent channels for the analysis of motion (Joesch et al., 2010; Eichner et al., 2011): L1 feeds into a circuit specialized to detect motion of brightness increments (ON-channel), L2 feeds into a circuit specialized to detect motion of brightness decrements (OFF-channel). T4 and T5 cells form the output of each channel, respectively. There are four T4 and four T5 cells per column, tuned to the four cardinal directions: front-to-back, back-to-front, upwards and downwards. According to their preferred direction, T4 and T5 cells terminate in four different layers of the lobula plate where they converge onto the large dendrites of the tangential cells (Maisak et al., 2013).

The lobula plate tangential cells can be identified individually due to their invariant anatomy and, due to their size, are accessible to whole-cell patch clamp recordings. They have large receptive fields and respond to visual motion in a directionally selective way: they depolarize when the pattern moves along their preferred direction, and hyperpolarize for pattern motion along their null direction. Tangential cells can be roughly grouped in cells of the horizontal system (HS-cells) and cells of the vertical system (VS-cells). There are three HS-cells (the northern HSN, the equatorial HSE and the southern HSS-cell) (Schnell et al., 2010) and 6 VS-cells (VS1-VS6) (Joesch et al., 2008) together covering almost completely the visual space surrounding the animal. The different members of each family occupy different regions within the lobula plate and, due to the retinotopic organization, have different but often overlapping receptive fields. HS- and VS-cells are thought to be the major output elements of the lobula-plate and, in blow flies, directly project onto descending neurons which finally control motor neurons for locomotion or head movements (Wertz et al., 2009).

References

Eichner, H., Joesch, M., Schnell, B., Reiff, D. F. & Borst, A. Internal structure of the fly elementary motion detector. Neuron 70, 1155–1164 (2011).

Joesch, M., Schnell, B., Raghu, S. V., Reiff, D. F. & Borst, A. ON and OFF pathways in Drosophila motion vision. Nature 468, 300–304 (2010).

Joesch, M., Plett, J., Borst, A. & Reiff, D. F. Response properties of motion-sensitive visual interneurons in the lobula plate of Drosophila melanogaster. Curr. Biol. 18, 368–374 (2008).

Maisak, M. S. et al. A directional tuning map of Drosophila elementary motion detectors. Nature 500, 212–216 (2013).

Schnell, B. et al. Processing of horizontal optic flow in three visual interneurons of the Drosophila brain. J. Neurophysiol. 103, 1646–1657 (2010).

Wertz, A., Gaub, B., Plett, J., Haag, J. & Borst, A. Robust coding of ego-motion in descending neurons of the fly. J. Neurosci. 29, 14993–15000 (2009).

 
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