Receptive field coordination across mosaics of diverse retinal ganglion cell types in the mammalian retina

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Throughout the brain, neural circuits are composed of diverse cell types. In the retina, cell types are spatially organized into mosaics, in which the receptive fields of each type approximately tile space. This organization ensures that the computations performed by each cell type occur uniformly across the visual field, with no gaps or gluts in processing. This exquisite coordination within each cell type to uniformly cover space raises the question, ‘is there coordination across cell types?’ In general, this coordination could manifest as either a tendency toward alignment, or anti-alignment, between two mosaics of receptive fields. Our central hypothesis is that mosaics of receptive fields are intricately coordinated across retinal cell types and that this coordination reflects fundamental organizing principles for how the retina processes natural scenes. We demonstrate with preliminary data that across four retinal ganglion cell (RGC) types in the rat retina, mosaics of receptive fields are intricately coordinated. Specifically, mosaics of ON and OFF RGC types that signal similar visual features are consistently anti-aligned. Meanwhile, mosaics of OFF and OFF types that signal distinct features are also anti-aligned while mosaics of ON and ON types are aligned. Finally, we show that across ON and OFF types that signal distinct visual features the mosaics are statistically independent in their spatial arrangement. The objectives of this proposal are to build upon these observations to (1) understand the mechanisms that underlie inter-mosaic coordination (Aim 1), (2) determine how and when this coordination develops (Aim 2), and (3) to determine the significance of inter-mosaic coordination of visual as well as how extensively mosaics are coordinated across additional RGC types (Aim 3). This proposed research is significant because it will uncover an entirely new phenomenon in the vertebrate retina: inter-mosaic coordination across diverse cell types with diverse receptive field properties. It will also reveal either new developmental mechanisms, or new roles for previously established mechanisms in coordinating mosaics across RGC types. It will also make novel predictions for how downstream neurons could pool over retinal inputs to produce orientation and direction tuned responses. Finally, this work is significant because it extends the theoretical basis (e.g. ‘efficient coding theory’) of how we understand the organization of retinal processing. The proposed research is innovative because it applies a recently developed analytical framework to large-scale population measurements of RGC receptive fields with the goal of understanding the contributions of cell position and synaptic specificity to inter-mosaic coordination. Furthermore, the work is conceptually innovative because it shows receptive field mosaics are coordinated and identifies the benefits of coordination to vision. The expected outcome of this research is a novel set of mechanisms and developmental process that yield functional coordination across distinct cell types in the retina. We anticipate these discoveries as being fundamental and impactful to understanding the retina and sensory processing