The Emergence of Directional Selectivity in the Visual Motion Pathway of Drosophila

• Published in: Neuron (Cambridge, Mass.) Mass.), 2017-04, Vol.94 (1), p.168-182.e10
• Main Authors: Strother, James A., Wu, Shiuan-Tze, Wong, Allan M., Nern, Aljoscha, Rogers, Edward M., Le, Jasmine Q., Rubin, Gerald M., Reiser, Michael B.
• Format: Article
• Language: English
• Subjects: Action Potentials - physiology; Animals; Calcium - metabolism; Calcium imaging; Dendrites; Dendrites - physiology; directional selectivity; Drosophila; Gene Expression Profiling; Insects; Medulla oblongata; Medulla Oblongata - cytology; Medulla Oblongata - physiology; Models, Neurological; Motion detection; Motion Perception - physiology; motion vision; Navigation behavior; Neural Circuit; Neurons; Neurons - physiology; Photoactivation; Retina; Selectivity; Studies; Synapses; T4 neurons; Visual Pathways - physiology; Visual perception
• ISSN: 0896-6273; 1097-4199
• DOI: 10.1016/j.neuron.2017.03.010

The perception of visual motion is critical for animal navigation, and flies are a prominent model system for exploring this neural computation. In Drosophila, the T4 cells of the medulla are directionally selective and necessary for ON motion behavioral responses. To examine the emergence of directional selectivity, we developed genetic driver lines for the neuron types with the most synapses onto T4 cells. Using calcium imaging, we found that these neuron types are not directionally selective and that selectivity arises in the T4 dendrites. By silencing each input neuron type, we identified which neurons are necessary for T4 directional selectivity and ON motion behavioral responses. We then determined the sign of the connections between these neurons and T4 cells using neuronal photoactivation. Our results indicate a computational architecture for motion detection that is a hybrid of classic theoretical models. •Each major T4 input encodes different features of ON and OFF visual stimuli•Directional selectivity for ON motion emerges in the dendrites of T4 cells•Mi1 and Tm3 cells excite T4s while Mi4 and Mi9 cells inhibit T4s•T4 cells compute motion using elements from two classic motion detection models Strother et al. dissect the responses of directionally selective visual neurons in Drosophila, by systematically recording, silencing, and activating each of the major input cells. Their results suggest motion detection is implemented using a hybrid of two classic theoretical models.