Spike Burst Coding of Translatory Optic Flow and Depth from Motion in the Fly Visual System

• Published in: Current biology 2017-11, Vol.27 (21), p.3225-3236.e3
• Main Authors: Longden, Kit D., Wicklein, Martina, Hardcastle, Ben J., Huston, Stephen J., Krapp, Holger G.
• Format: Article
• Language: English
• Subjects: Animals; depth from motion; Diptera - physiology; Flight, Animal - physiology; fly visual system; Interneurons - physiology; Motion Perception - physiology; Optic Flow - physiology; Photic Stimulation; spike bursting; translatory optic flow; Visual Pathways - physiology
• ISSN: 0960-9822; 1879-0445
• DOI: 10.1016/j.cub.2017.09.044

Many animals use the visual motion generated by traveling straight—the translatory optic flow—to successfully navigate obstacles: near objects appear larger and to move more quickly than distant objects. Flies are expert at navigating cluttered environments, and while their visual processing of rotatory optic flow is understood in exquisite detail, how they process translatory optic flow remains a mystery. We present novel cell types that have local motion receptive fields matched to translation self-motion, the vertical translation (VT) cells. One of these, the VT1 cell, encodes self-motion in the forward-sideslip direction and fires action potentials in spike bursts as well as single spikes. We show that the spike burst coding is size and speed-tuned and is selectively modulated by motion parallax—the relative motion experienced during translation. These properties are spatially organized, so that the cell is most excited by clutter rather than isolated objects. When the fly is presented with a simulation of flying past an elevated object, the spike burst activity is modulated by the height of the object, and the rate of single spikes is unaffected. When the moving object alone is experienced, the cell is weakly driven. Meanwhile, the VT2–3 cells have motion receptive fields matched to the lift axis. In conjunction with previously described horizontal cells, the VT cells have properties well suited to the visual navigation of clutter and to encode the fly’s movements along near cardinal axes of thrust, lift, and forward sideslip. •VT1 is a novel cell encoding sideslip translatory optic flow with spike bursts•Spike burst rate is modulated by size, temporal frequency, and motion parallax•These properties enable spike bursting to be modulated by multiple depth planes•VT2–3 are complementary novel cells with receptive fields matching lift translation Longden et al. report novel optic flow-processing neurons in the fly with motion receptive fields matched to translatory optic flow. One of these cells, VT1, encodes properties of the moving visual scene in spike bursts, such that depth from motion modulates the rate of spike bursts and not the rate of single action potentials.