Current Biology
Volume 28, Issue 24, 17 December 2018, Pages 4037-4045.e5
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Bi-directional Control of Walking Behavior by Horizontal Optic Flow Sensors

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Highlights

  • 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

Summary

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, 2, 3, 4, 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, 11, 12] to determine turning and movement speed [13, 14, 15, 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.

Keywords

optic flow
optomotor response
Drosophila
horizontal system cells
optogenetics
preferred direction depolarization
null direction hyperpolarization
steering
tethered walking

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