Visual motion sensitivity in descending neurons in the hoverfly

Abstract

Many animals use motion vision information to control dynamic behaviors. For example, flying insects must decide whether to pursue a prey or not, to avoid a predator, to maintain their current flight trajectory, or to land. The neural mechanisms underlying the computation of visual motion have been particularly well investigated in the fly optic lobes. However, the descending neurons, which connect the optic lobes with the motor command centers of the ventral nerve cord, remain less studied. To address this deficiency, we describe motion vision sensitive descending neurons in the hoverfly Eristalis tenax. We describe how the neurons can be identified based on their receptive field properties, and how they respond to moving targets, looming stimuli and to widefield optic flow. We discuss their similarities with previously published visual neurons, in the optic lobes and ventral nerve cord, and suggest that they can be classified as target-selective, looming sensitive and optic flow sensitive, based on these similarities. Our results highlight the importance of using several visual stimuli as the neurons can rarely be identified based on only one response characteristic. In addition, they provide an understanding of the neurophysiology of visual neurons that are likely to affect behavior.

Facilitation of neural responses to targets moving against optic flow

“…1a, b, blue line indicates target motion). As shown previously 14,29 , TSDNs typically have no spontaneous activity (Fig. 1b).…”

“…We recorded extracellularly from target selective descending neurons (TSDNs) in male Eristalis hoverflies. TSDNs respond selectively to the motion of small targets 14,29 , as shown in the example where a round, black target traverses a white background (Extended Data Movie 1, 2, Fig. 1a, b, blue line indicates target motion).…”

“…We used a 3D optic flow stimulus built of many targets that move coherently 29 to simulate the types of retinal flow fields experienced during self-generated optic flow. Against this optic flow, the target can only be identified by its independent trajectory.…”

“…We generated optic flow using the coherent motion of thousands of “targets” within a simulated 3D space surrounding the hoverfly, and projecting the can 1200 targets anterior of the fly onto a 2D visual monitor 29 . We showed that this 3D optic flow stimulus modulates the TSDN response to target motion.…”

“…To redress this deficiency, we quantified the responses of Eristalis TSDNs to targets moving against 6 types of optic flow, three translations and three rotations. By calibrating for the hoverfly’s position relative to the visual monitor, the simulated optic flow 29 mimics the self-generated optic flow seen during motion through a 3D world. For this purpose, we used an optic flow stimulus consisting of many targets moving coherently.…”