A common strategy by which developing neurons locate their synaptic partners is through projections to circuit-specific neuropil sublayers. Once established, sublayers serve as a substrate for selective synapse formation, but how sublayers arise during neurodevelopment remains unknown. Here, we identify the earliest events that initiate formation of the direction-selective circuit in the inner plexiform layer of mouse retina. We demonstrate that radially migrating newborn starburst amacrine cells establish homotypic contacts on arrival at the inner retina. These contacts, mediated by the cell-surface protein MEGF10, trigger neuropil innervation resulting in generation of two sublayers comprising starburst-cell dendrites. This dendritic scaffold then recruits projections from circuit partners. Abolishing MEGF10-mediated contacts profoundly delays and ultimately disrupts sublayer formation, leading to broader direction tuning and weaker direction-selectivity in retinal ganglion cells. Our findings reveal a mechanism by which differentiating neurons transition from migratory to mature morphology, and highlight this mechanism’s importance in forming circuit-specific sublayers.

The output of the retina is organized into many detector grids, called ‘mosaics’ that signal different features of visual scenes to the brain 1 – 4 . Each mosaic comprises a single retinal ganglion cell (RGC) type, whose receptive fields (RFs) tile space. Many mosaics arise as pairs, signaling increments (ON) and decrements (OFF), respectively, of a particular visual feature 5 . Using a model of efficient coding 6 , we determine how such mosaic pairs should be arranged to optimize the encoding of natural scenes. We find that information is maximized when these mosaic pairs are anti-aligned, meaning the RF centers between mosaics are more distant than expected by chance. We test this prediction across multiple RF mosaics acquired with large-scale measurements of RGC light responses from rat and primate. We find that ON and OFF RGC pairs with similar feature selectivity exhibit anti-aligned RF mosaics, consistent with theory. ON and OFF types that encode distinct features exhibit independent mosaics. These results extend efficient coding theory (ECT) beyond individual cells to predict how populations of diverse RGC types are spatially arranged.

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Motion estimation is crucial for aerial animals such as the fly, which perform fast and complex maneuvers while flying through a 3-D environment. Motion-sensitive neurons in the lobula plate, a part of the visual brain, of the fly have been studied extensively for their specialized role in motion encoding. However, the visual stimuli used in such studies are typically highly simplified, often move in restricted ways, and do not represent the complexities of optic flow generated during actual flight. Here, we use combined rotations about different axes to study how H1, a wide-field motion-sensitive neuron, encodes preferred yaw motion in the presence of stimuli not aligned with its preferred direction. Our approach is an extension of "white noise" methods, providing a framework that is readily adaptable to quantitative studies into the coding of mixed dynamic stimuli in other systems. We find that the presence of a roll or pitch ("distractor") stimulus reduces information transmitted by H1 about yaw, with the amount of this reduction depending on the variance of the distractor. Spike generation is influenced by features of both yaw and the distractor, where the degree of influence is determined by their relative strengths. Certain distractor features may induce bidirectional responses, which are indicative of an imbalance between global excitation and inhibition resulting from complex optic flow. Further, the response is shaped by the dynamics of the combined stimulus. Our results provide intuition for plausible strategies involved in efficient coding of preferred motion from complex stimuli having multiple motion components.