Visuomotor Transformation in the Fly Gaze Stabilization System

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Abstract
For sensory signals to control an animal's behavior, they must first be transformed into a format appropriate for use by its motor systems. This fundamental problem is faced by all animals, including humans. Beyond simple reflexes, little is known about how such sensorimotor transformations take place. Here we describe how the outputs of a well-characterized population of fly visual interneurons, lobula plate tangential cells (LPTCs), are used by the animal's gaze-stabilizing neck motor system. The LPTCs respond to visual input arising from both self-rotations and translations of the fly. The neck motor system however is involved in gaze stabilization and thus mainly controls compensatory head rotations. We investigated how the neck motor system is able to selectively extract rotation information from the mixed responses of the LPTCs. We recorded extracellularly from fly neck motor neurons (NMNs) and mapped the directional preferences across their extended visual receptive fields. Our results suggest that—like the tangential cells—NMNs are tuned to panoramic retinal image shifts, or optic flow fields, which occur when the fly rotates about particular body axes. In many cases, tangential cells and motor neurons appear to be tuned to similar axes of rotation, resulting in a correlation between the coordinate systems the two neural populations employ. However, in contrast to the primarily monocular receptive fields of the tangential cells, most NMNs are sensitive to visual motion presented to either eye. This results in the NMNs being more selective for rotation than the LPTCs. Thus, the neck motor system increases its rotation selectivity by a comparatively simple mechanism: the integration of binocular visual motion information. Many behavioral tasks rely on sensory information. This information, however, needs to be transformed into a format that is compatible with the requirements of motor systems. In this study we characterize the neural basis of such a sensorimotor transformation in a model system. Flies, like humans, stabilize their gaze to keep their eyes level, even when the body is rotating. An identified population of fly brain neurons called lobula plate tangential cells (LPTCs) contributes to this task. These cells analyze the wide-field retinal image shifts generated when the fly is moving relative to its environment. We have characterized the visual receptive fields of motor neurons that use the information encoded by LPTCs to control gaze-stabilizing head movements. Our results suggest that the motor neurons use their LPTC inputs in a comparatively simple and direct way: they combine inputs from both sides of the brain to increase the motor neurons' selectivity for rotations. Such a mechanism enables a specific, fast, and surprisingly simple sensorimotor transformation in which visual information contributes to gaze stabilization.