Receptive Fields in Primate Retina Are Coordinated to Sample Visual Space More Uniformly

In the visual system, large ensembles of neurons collectively sample visual space with receptive fields (RFs). A puzzling problem is how neural ensembles provide a uniform, high-resolution visual representation in spite of irregularities in the RFs of individual cells. This problem was approached by simultaneously mapping the RFs of hundreds of primate retinal ganglion cells. As observed in previous studies, RFs exhibited irregular shapes that deviated from standard Gaussian models. Surprisingly, these irregularities were coordinated at a fine spatial scale: RFs interlocked with their neighbors, filling in gaps and avoiding large variations in overlap. RF shapes were coordinated with high spatial precision: the observed uniformity was degraded by angular perturbations as small as 15°, and the observed populations sampled visual space with more than 50% of the theoretical ideal uniformity. These results show that the primate retina encodes light with an exquisitely coordinated array of RF shapes, illustrating a higher degree of functional precision in the neural circuitry than previously appreciated. : All visual information reaching the brain is transmitted by retinal ganglion cells, each of which is sensitive to a small region of space known as its receptive field. Each of the 20 or so distinct ganglion cell types is thought to transmit a complete visual image to the brain, because the receptive fields of each type form a regular lattice covering visual space. However, within each regular lattice, individual receptive fields have jagged, asymmetric shapes, which could produce “blind spots” and excessive overlap, degrading the visual image. To understand how the visual system overcomes this problem, we used a multielectrode array to record from hundreds of ganglion cells in isolated patches of peripheral primate retina. Surprisingly, we found that irregularly shaped receptive fields fit together like puzzle pieces, with high spatial precision, producing a more homogeneous coverage of visual space than would be possible otherwise. This finding reveals that the representation of visual space by neural ensembles in the retina is functionally coordinated and tuned, presumably by developmental interactions or ongoing visual activity, producing a more precise sensory signal. Receptive fields in primate retina have irregular shapes, but they interlock like puzzle pieces to provide highly uniform coverage of visual space.