Journal Article

Space–time wiring specificity supports direction selectivity in the retina

Seung, H. Sebastian, Denk, Winfried, Behabadi, Bardia F., Richardson, Mark, Turaga, Srinivas C., Greene, Matthew J., Lee, Kisuk, Robinson, Amy, Purcaro, Michael, Campos, Michael, Kim, Jinseop S., Zlateski, Aleksandar, Balkam, Matthew

2014

Overview

How does the mammalian retina detect motion? This classic problem in visual neuroscience has remained unsolved for 50 years. In search of clues, here we reconstruct Off-type starburst amacrine cells (SACs) and bipolar cells (BCs) in serial electron microscopic images with help from EyeWire, an online community of ‘citizen neuroscientists’. On the basis of quantitative analyses of contact area and branch depth in the retina, we find evidence that one BC type prefers to wire with a SAC dendrite near the SAC soma, whereas another BC type prefers to wire far from the soma. The near type is known to lag the far type in time of visual response. A mathematical model shows how such ‘space–time wiring specificity’ could endow SAC dendrites with receptive fields that are oriented in space–time and therefore respond selectively to stimuli that move in the outward direction from the soma. Motion detection by the retina is thought to rely largely on the biophysics of starburst amacrine cell dendrites; here machine learning is used with gamified crowdsourcing to draw the wiring diagram involving amacrine and bipolar cells to identify a plausible circuit mechanism for direction selectivity; the model suggests similarities between mammalian and insect vision. The retina's sense of direction Motion detection by the mammalian retina has been thought to rely largely on the intrinsic biophysics of the dendrites of starburst amacrine cells (SACs). Now Sebastian Seung and colleagues have combined new machine-learning techniques with crowd sourcing via the EyeWire brain-mapping game to redraw the wiring diagram for amacrine cells and bipolar cells. Their results show that direction selectivity is established at the presynaptic level — in the spatiotemporal inputs to the amacrine cells — identifying neural circuits rather than intrinsic properties of SACs as the key to direction selectivity. This new model brings the mouse retina closer in certain respects to the Reichardt motion detector characteristic of insect vision.

• Publisher: Nature Publishing Group UK,Nature Publishing Group
• Subject: 14 / 14/28 / 631/378/2613/1786 / Accuracy / Amacrine Cells - cytology / Amacrine Cells - physiology / Amacrine Cells - ultrastructure / Animals / Artificial Intelligence / Brain Mapping / Brain research / Brain stimulation / Crowdsourcing / Dendrites / Dendrites - metabolism / Humanities and Social Sciences / Mice / Models, Neurological / Motion / multidisciplinary / Neural circuitry / Neural Pathways - physiology / Neurology / Neurons / Physiological aspects / Presynaptic Terminals - metabolism / Retina / Retina - cytology / Retina - physiology / Retinal Bipolar Cells - cytology / Retinal Bipolar Cells - physiology / Retinal Bipolar Cells - ultrastructure / Science / Spatio-Temporal Analysis