Abstract
How neurons become sensitive to the direction of visual motion represents a classic example of neural computation. Two alternative mechanisms have been discussed in the literature so far: preferred direction enhancement, by which responses are amplified when stimuli move along the preferred direction of the cell, and null direction suppression, where one signal inhibits the response to the subsequent one when stimuli move along the opposite, i.e. null direction. Along the processing chain in the Drosophila optic lobe, directional responses first appear in T4 and T5 cells. Visually stimulating sequences of individual columns in the optic lobe with a telescope while recording from single T4 neurons, we find both mechanisms at work implemented in different sub-regions of the receptive field. This finding explains the high degree of directional selectivity found already in the fly's primary motion-sensing neurons and marks an important step in our understanding of elementary motion detection.
Highlights
Flies see the world through a hexagonal array of facets each equipped with its own small lens focusing the light onto 8 photoreceptors
We used a driver line specific for those T4 and T5 cells sending their axons into layer 3 of the lobula plate that are sensitive to upward motion
When we simulated the responses of the model to grating motion into different directions, we found the full model T4 cell to be more sharply tuned to its preferred direction than the one without preferred direction enhancement or the one without null direction suppression (Figure 5d)
Summary
Flies see the world through a hexagonal array of facets each equipped with its own small lens focusing the light onto 8 photoreceptors. Visual motion information is extracted in parallel pathways encoding light increments (ON) and decrements (OFF) (Joesch et al, 2010; Eichner et al, 2011; Joesch et al, 2013) Both pathways bifurcate in the lamina and lead, via a set of specific medulla interneurons, onto the dendrites of T4 and T5 cells, respectively (Takemura et al, 2013; Shinomiya et al, 2014). Both T4 and T5 cells exist in 4 subgroups tuned to one of the four cardinal directions of motion and project into four layers of the lobula plate (Maisak et al, 2013) (Figure 1b). Since none of the neurons upstream from T4 and T5 respond to visual motion in a direction-selective way (Behnia et al, 2014; Strother et al, 2014; Meier et al, 2014; Ammer et al, 2015; Serbe et al, 2016), T4 and T5 cells are the first neurons in the processing chain where directional information is represented explicitly (Maisak et al, 2013; Fisher et al, 2015)
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