Wide-field amacrine cell inputs to ON parasol ganglion cells in macaque retina.

Parasol cells are one of the major types of primate retinal ganglion cells. The goal of this study was to describe the synaptic inputs that shape the light responses of the ON type of parasol cells, which are excited by increments in light intensity. A connectome from central macaque retina was generated by serial blockface scanning electron microscopy. Six neighboring ON parasol cells were reconstructed, and their synaptic inputs were analyzed. On average, they received 21% of their input from bipolar cells, excitatory local circuit neurons receiving input from cones. The majority of their input was from amacrine cells, local circuit neurons of the inner retina that are typically inhibitory. Their contributions to the neural circuit providing input to parasol cells are not well-understood, and the focus of this study was on the presynaptic wide-field amacrine cells, which provided 17% of the input to ON parasol cells. These are GABAergic amacrine cells with long, relatively straight dendrites, and sometimes also axons, that run in a single, narrow stratum of the inner plexiform layer. The presynaptic wide-field amacrine cells were reconstructed, and two types were identified based on their characteristic morphology. One presynaptic amacrine cell was identified as semilunar type 2, a polyaxonal cell that is electrically coupled to ON parasol cells. A second amacrine was identified as wiry type 2, a type known to be sensitive to motion. These inputs likely make ON parasol cells more sensitive to stimuli that are rapidly changing outside their classical receptive fields.

Neural Mechanisms Mediating Motion Sensitivity in Parasol Ganglion Cells of the Primate Retina.

Considerable theoretical and experimental effort has been dedicated to understanding how neural circuits detect visual motion. In primates, much is known about the cortical circuits that contribute to motion processing, but the role of the retina in this fundamental neural computation is poorly understood. Here, we used a combination of extracellular and whole-cell recording to test for motion sensitivity in the two main classes of output neurons in the primate retina-midget (parvocellular-projecting) and parasol (magnocellular-projecting) ganglion cells. We report that parasol, but not midget, ganglion cells are motion sensitive. This motion sensitivity is present in synaptic excitation and disinhibition from presynaptic bipolar cells and amacrine cells, respectively. Moreover, electrical coupling between neighboring bipolar cells and the nonlinear nature of synaptic release contribute to the observed motion sensitivity. Our findings indicate that motion computations arise far earlier in the primate visual stream than previously thought.