Bi-directional Control of Walking Behavior by Horizontal Optic Flow Sensors

• Published in: Current biology 2018-12, Vol.28 (24), p.4037-4045.e5
• Main Authors: Busch, Christian, Borst, Alexander, Mauss, Alex S.
• Format: Article
• Language: English
• Subjects: Drosophila; horizontal system cells; null direction hyperpolarization; optic flow; optogenetics; optomotor response; preferred direction depolarization; steering; tethered walking
• ISSN: 0960-9822; 1879-0445
• DOI: 10.1016/j.cub.2018.11.010

Moving animals experience constant sensory feedback, such as panoramic image shifts on the retina, termed optic flow. Underlying neuronal signals are thought to be important for exploratory behavior by signaling unintended course deviations and by providing spatial information about the environment [1, 2]. Particularly in insects, the encoding of self-motion-related optic flow is well understood [1–5]. However, a gap remains in understanding how the associated neuronal activity controls locomotor trajectories. In flies, visual projection neurons belonging to two groups encode panoramic horizontal motion: horizontal system (HS) cells respond with depolarization to front-to-back motion and hyperpolarization to the opposite direction [6, 7], and other neurons have the mirror-symmetrical response profile [6, 8, 9]. With primarily monocular sensitivity, the neurons’ responses are ambiguous for different rotational and translational self-movement components. Such ambiguities can be greatly reduced by combining signals from both eyes [10–12] to determine turning and movement speed [13–16]. Here, we explore the underlying functional logic by optogenetic HS cell manipulation in tethered walking Drosophila. We show that de- and hyperpolarization evoke opposite turning behavior, indicating that both direction-selective signals are transmitted to descending pathways for course control. Further experiments reveal a negative effect of bilaterally symmetric de- and hyperpolarization on walking velocity. Our results are therefore consistent with a functional architecture in which the HS cells’ membrane potential influences walking behavior bi-directionally via two decelerating pathways. [Display omitted] •Horizontal optic flow detectors (HS cells) affect turning in walking flies•De- and hyperpolarization evoke opposite turning•Both signals negatively influence walking speed•HS cells thus mediate bi-directional turning via asymmetric deceleration Busch et al. study the behavioral effects of manipulating optic flow-sensing HS cells in tethered walking Drosophila. Both de- and hyperpolarization elicit turning syndirectional with the mimicked visual motion. Therefore, two steering signals are encoded in the HS cell-response sign, likely mediating the fly’s tendency to follow a rotating pattern.