Vision influences behavior, but ongoing behavior also modulates vision in animals ranging from insects to primates. The function and biophysical mechanisms of most such modulations remain unresolved. Here, we combine behavioral genetics, electrophysiology, and high-speed videography to advance a function for behavioral modulations of visual processing in Drosophila. We argue that a set of motion-sensitive visual neurons regulate gaze-stabilizing head movements. We describe how, during flight turns, Drosophila perform a set of head movements that require silencing their gaze-stability reflexes along the primary rotation axis of the turn. Consistent with this behavioral requirement, we find pervasive motor-related inputs to the visual neurons, which quantitatively silence their predicted visual responses to rotations around the relevant axis while preserving sensitivity around other axes. This work proposes a function for a behavioral modulation of visual processing and illustrates how the brain can remove one sensory signal from a circuit carrying multiple related signals.

Visual object fixation and figure-ground discrimination in Drosophila are robust behaviors requiring sophisticated computation by the visual system, yet the neural substrates remain unknown. Recent experiments in walking flies revealed object fixation behavior mediated by circuitry independent from the motion-sensitive T4-T5 cells required for wide-field motion responses. In tethered flight experiments under closed-loop conditions, we found similar results for one feedback gain, whereas intact T4-T5 cells were necessary for robust object fixation at a higher feedback gain and in figure-ground discrimination tasks. We implemented dynamical models (available at http://strawlab.org/asymmetric-motion/) based on neurons downstream of T4-T5 cells—one a simple phenomenological model and another, physiologically more realistic model—and found that both predict key features of stripe fixation and figure-ground discrimination and are consistent with a classical formulation. Fundamental to both models is motion asymmetry in the responses of model neurons, whereby front-to-back motion elicits stronger responses than back-to-front motion. When a bilateral pair of such model neurons, based on well-understood horizontal system cells, downstream of T4-T5, is coupled to turning behavior, asymmetry leads to object fixation and figure-ground discrimination in the presence of noise. Furthermore, the models also predict fixation in front of a moving background, a behavior previously suggested to require an additional pathway. Thus, the models predict several aspects of object responses on the basis of neurons that are also thought to serve a key role in background stabilization.

Highlights d Optic-flow processing neurons are suppressed during loomevoked flight turns d This suppression cuts signaling of head-movement-induced visual motion during turns d The cells are not suppressed during optomotor responses to rotational visual motion d Suppression thus occurs during course-changing, but not course-stabilizing, turns