A Neuron in the Visual System That Provides Feedback About Limb Movement

Abstract

Sensory stimuli can arise from the environment and also, predictably, from an organism’s own movements. The ability to distinguish between self-generated and external sensory stimuli is essential for normal behavior, but the neural circuits that anticipate and cancel responses to self-motion are not well understood in most organisms and modalities. This study focuses on a previously uncharacterized group of neurons in the Drosophila visual system known as LT52 cells. LT52 cells receive the majority of their input from the optic lobes and provide strong inhibitory input to a specialized circuit in the central brain that mediates the visual pursuit of moving objects. To our surprise, we found that LT52 neurons are strongly activated when flies groomed their heads – even in the absence of an external visual stimulus. By comparing activity in genetically blind and control flies, we determined that this activity is partially driven by a non-visual signal. We found that the non-visual component of the response is specifically related to the movement of the ipsilateral foreleg, suggesting that it arises from internal self-motion signals, specifically proprioceptive feedback and/or copies of ipsilateral motor commands. In terms of visual tuning, we found that LT52 neurons respond best to large, fast-moving stimuli with vertically extended edges and have a strong directional preference for motion in the front-to-back direction. We show that these tuning properties overlap with the visual stimulus generated by the fly’s leg as it sweeps back and forth across the eye during head grooming, suggesting that LT52 activity during head grooming is also partly driven by visual reafference. The visual tuning of LT52 complements the tuning of its postsynaptic targets, which are small object motion detectors that respond to slower, more ethologically-relevant speeds. Taken together, our results suggest that LT52 neurons serve to inhibit the postsynaptic population’s response to large, fast-moving stimuli that the downstream circuit might otherwise confuse for the movement of a visual target. The movement of the fly’s own leg represents a special kind of visual “distractor” whose appearance can be predicted by a combination of visual reafference and internal self-motion signals input to LT52.