Populations of local direction–selective cells encode global motion patterns generated by self-motion

Abstract

Self-motion generates visual patterns on the eye that are important for navigation. These optic flow patterns are encoded by the population of local direction–selective cells in the mouse retina, whereas in flies, local direction–selective T4/T5 cells are thought to be uniformly tuned. How complex global motion patterns can be computed downstream is unclear. We show that the population of T4/T5 cells in Drosophila encodes global motion patterns. Whereas the mouse retina encodes four types of optic flow, the fly visual system encodes six. This matches the larger number of degrees of freedom and the increased complexity of translational and rotational motion patterns during flight. The four uniformly tuned T4/T5 subtypes described previously represent a local subset of the population. Thus, a population code for global motion patterns appears to be a general coding principle of visual systems that matches local motion responses to modes of the animal’s movement.

Eye structure shapes neuron function inDrosophilamotion vision

“…1F), rather than a purely rotational one, as expected for H2 (blowflies 23 ). This shift in the local PD of H2 implies that T4 neurons are not globally tuned to cardinal motion directions, a prediction that agrees well with a recent imaging study of T4/T5 axons 24 . But what causes T4 cells to change their directional preference across the eye?…”

“…3E). Since we identified the T4 subtypes based on lobula plate layer innervation, the striking within-subtype similarity of the PDs, does not support further divisions based on morphology 19,24,26 . Our analysis has thus revealed that T4 neurons share a universal sampling strategy-throughout the eye they innervate a unit hexagon of columns, while establishing a preferred direction by aligning their dendrites mostly in one direction, parallel to either the horizontal or vertical axes of the hexagonal grid.…”

“…Based on our anatomical analysis of the dendritic orientation of T4 neurons, identified by their targeted lobula plate layer, we find no evidence for additional subtypes of T4 neurons. However, recent transcriptomic studies 26 provide evidence for additional subtype diversity, and functional studies 24 suggest that local PDs may be regionally modified through as-yet-undescribed connectivity differences, an important question for future EM studies. Finally, our analysis of global optic flow patterns (Fig.…”

Neuronal circuits integrating visual motion information in Drosophila melanogaster

“…Clarifying the role of these Y cells will require establishing whether they are excitatory or inhibitory (inhibition via glutamate is a strong possibility, as T4/T5 axons express GluCla , a glutamate-gated chloride channel, 66 yet are not strong targets of the bilayer LPi neurons; Figure 4; Data S1). These recurrent connections could provide a possible mechanistic explanation for the functionally identified subtypes of T4/T5; 36 however, this recent study found subtypes in layers 1 and 2, whereas Y11 and Y12 collect outputs and provide inputs to layers 1, 3, and 4. Both neurons combine a vertical motion signal with front-to-back motion, but we did not find complementary neurons for the oblique motion directions integrating Lop2/back-to-front motion.…”

“…However, recent work has shown that the population of T4/T5 cells encodes a global pattern that is not consistent with these cardinal directions throughout the eye. 36 Anatomical and physiological data suggest a correlation between an LPTC's visual motion responses and its lobula plate layer pattern, 29,37 although each neuron's selectivity for visual motion patterns can be influenced by network connections. 38,39 Many details of the lobula plate circuitry have not been thoroughly investigated, with the noteworthy exception of two bilayer lobula plate-intrinsic (LPi) cells: LPi3-4 receives input in Lop3 and provides output to Lop4, whereas LPi4-3 sends signals from Lop4 to Lop3.…”