Cell types and cell circuits in human and non-human primate retina.

A central goal in the study of any sensory system is to predict neural responses to complex inputs, especially those encountered during natural stimulation. Nowhere is the transformation from stimulus to response better understood than the vertebrate retina. Nevertheless, descriptions of retinal computation are largely based on stimulation using artificial visual stimuli, and it is unclear how these descriptions map onto the encoding of natural stimuli. We demonstrate that nonlinear spatial integration, a common feature of retinal ganglion cell (RGC) processing, shapes neural responses to natural visual stimuli in primate Off parasol RGCs, whereas On parasol RGCs exhibit surprisingly linear spatial integration. Despite this asymmetry, both cell types show strong nonlinear integration when presented with artificial stimuli. We show that nonlinear integration of natural stimuli is a consequence of rectified excitatory synaptic input and that accounting for nonlinear spatial integration substantially improves models that predict RGC responses to natural images.

Synaptic rectification controls nonlinear spatial integration of natural visual inputs

A Color Vision Circuit for Non-Image-Forming Vision in the Primate Retina

Human retinal model systems: Strengths, weaknesses, and future directions.

In primates, broad thorny retinal ganglion cells are highly sensitive to small, moving stimuli. They have tortuous, fine dendrites with many short, spine-like branches that occupy three contiguous strata in the middle of the inner plexiform layer. The neural circuits that generate their responses to moving stimuli are not well-understood, and that was the goal of this study. A connectome from central macaque retina was generated by serial block-face scanning electron microscopy, a broad thorny cell was reconstructed, and its synaptic inputs were analyzed. It received fewer than 2% of its inputs from both ON and OFF types of bipolar cells; the vast majority of its inputs were from amacrine cells. The presynaptic amacrine cells were reconstructed, and seven types were identified based on their characteristic morphology. Two types of narrow-field cells, knotty bistratified type 1 and wavy multistratified type 2, were identified. Two types of medium-field amacrine cells, ON starburst and spiny, were also presynaptic to the broad thorny cell. Three types of wide-field amacrine cells, wiry type 2, stellate wavy and semilunar type 2, also made synapses onto the broad thorny cell. Physiological experiments using a macaque retinal preparation in vitro confirmed that broad thorny cells received robust excitatory input from both the ON and the OFF pathways. Given the paucity of bipolar cell inputs, it is likely that amacrine cells provided much of the excitatory input, in addition to inhibitory input. This article is protected by copyright. All rights reserved.

Synaptic inputs to broad thorny 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.

Rebecca J. Girresch

Papers

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

Synaptic inputs to broad thorny ganglion cells in macaque retina.