Sequential Nonlinear Filtering of Local Motion Cues by Global Motion Circuits

• Published in: Neuron (Cambridge, Mass.) Vol. 100; no. 1; pp. 229 - 243.e3
• Main Authors: Barnhart, Erin L., Wang, Irving E., Wei, Huayi, Desplan, Claude, Clandinin, Thomas R.
• Format: Journal Article
• Language: English
• Published: United States Elsevier Inc 10.10.2018; Elsevier Limited
• Subjects: Animals; Brain - physiology; Calcium imaging; Calcium Signaling - physiology; Circuits; Cues; Dendrites; Dendrites - physiology; dendritic computation; Drosophila melanogaster; feature selectivity; in vivo calcium imaging; Information processing; Insects; Motion detection; Motion Perception - physiology; motion vision; Neurons; Neurons - physiology; Optic flow; Photoreceptors; Retina; Software; Velocity; Visual Pathways - physiology; in vivo calcium imaging; motion vision; feature selectivity; dendritic computation
• ISSN: 0896-6273; 1097-4199
• DOI: 10.1016/j.neuron.2018.08.022

Many animals guide their movements using optic flow, the displacement of stationary objects across the retina caused by self-motion. How do animals selectively synthesize a global motion pattern from its local motion components? To what extent does this feature selectivity rely on circuit mechanisms versus dendritic processing? Here we used in vivo calcium imaging to identify pre- and postsynaptic mechanisms for processing local motion signals in global motion detection circuits in Drosophila. Lobula plate tangential cells (LPTCs) detect global motion by pooling input from local motion detectors, T4/T5 neurons. We show that T4/T5 neurons suppress responses to adjacent local motion signals whereas LPTC dendrites selectively amplify spatiotemporal sequences of local motion signals consistent with preferred global patterns. We propose that sequential nonlinear suppression and amplification operations allow optic flow circuitry to simultaneously prevent saturating responses to local signals while creating selectivity for global motion patterns critical to behavior. •Global motion circuits in Drosophila exhibit nonlinear summation of local signals•Neurons that detect local motion suppress spatially adjacent signals•Dendrites that pool local motion inputs align with a preferred direction of motion•Oriented dendrites amplify responses to specific spatiotemporal input sequences Barnhart et al. show that sequential nonlinear summation of local motion cues shapes feature selectivity in the Drosophila visual system. In global motion circuits, adjacent local signals are suppressed presynaptically, whereas specific spatiotemporal sequences of local signals are amplified postsynaptically.