Motion detection is a fundamental neural computation performed by many sensory systems. In the fly, local motion computation is thought to occur within the first two layers of the visual system, the lamina and medulla. We constructed specific genetic driver lines for each of the 12 neuron classes in the lamina. We then depolarized and hyperpolarized each neuron type and quantified fly behavioral responses to a diverse set of motion stimuli. We found that only a small number of lamina output neurons are essential for motion detection, while most neurons serve to sculpt and enhance these feedforward pathways. Two classes of feedback neurons (C2 and C3), and lamina output neurons (L2 and L4), are required for normal detection of directional motion stimuli. Our results reveal a prominent role for feedback and lateral interactions in motion processing and demonstrate that motion-dependent behaviors rely on contributions from nearly all lamina neuron classes.
Although familiar to each of us, the sensation of inhabiting a body is ineffable. Traditional senses like vision and hearing monitor the external environment, allowing humans to have shared sensory experiences. But proprioception, the sensation of body position and movement, is fundamentally personal and typically absent from conscious perception. Nonetheless, this 'sixth sense' remains critical to human experience, a fact that is most apparent when one considers those who have lost it. Take, for example, the case of Ian Waterman who, at the age of 19, suffered a rare autoimmune response to a flu infection that attacked the sensory neurons from his neck down. This infection deprived him of the sense of position, movement and touch in his body. With this loss of feedback came a complete inability to coordinate his movements. While he could compel his muscles to contract, he lost the ability to orchestrate these actions into purposeful behaviors, in essence leaving him immobile, unable to stand, walk, or use his body to interact with the world. Only after years of dedicated training was he able to re-learn to move his body entirely under visual control.
Summary Animals rely on an internal sense of body position and movement to effectively control motor behavior. This sense of proprioception is mediated by diverse populations of mechanosensory neurons distributed throughout the body. Here, we investigate neural coding of leg proprioception in Drosophila, using in vivo two-photon calcium imaging of proprioceptive sensory neurons during controlled movements of the fly tibia. We found that the axons of leg proprioceptors are organized into distinct functional projections that contain topographic representations of specific kinematic features. Using subclass-specific genetic driver lines, we show that one group of axons encodes tibia position (flexion/extension), another encodes movement direction, and a third encodes bidirectional movement and vibration frequency. Overall, our findings reveal how proprioceptive stimuli from a single leg joint are encoded by a diverse population of sensory neurons, and provide a framework for understanding how proprioceptive feedback signals are used by motor circuits to coordinate the body.
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