Abstract
Purpose: :
Cone photoreceptors have fast response kinetics and a high level of intrinsic dark noise compared to rods. We investigated how the retinal circuitry filters the cone signals to understand the limits set by cone noise and response kinetics on the encoding of temporal information in the primate retina.
Methods: :
Responses from cones, cone bipolars, horizontal cells and ganglion cells were recorded by whole-cell and cell-attached patch clamp configurations in the slice and flat mount preparations of primate (Macaca fascicularis, M. nemestrina, M. mulatta & Papio anubis) retinae. Flashes (10 ms) and white noise stimuli were presented in the presence of steady background lights in the intensity range 0 - 10 000 R*/L-cone/s (640 nm wide-field LED spot). Rod mediated signals were suppressed by dim background light (510 nm, ca. 30 R*/rod/s) or by blocking the rod pathway pharmacologically. Synaptic filters between pre- and postsynaptic neurons and for the entire retina were calculated based on measured responses to flashes and/or white noise stimuli. Dynamic clamp recordings on retinal ganglion cells were carried out to test directly the effects of different noise components in the input currents on spike generation.
Results: :
Firstly, synaptic filtering substantially speeds the kinetics of light responses in the neurons downstream of cones (bipolar cells, horizontal cells and ganglion cells. Secondly, signal transmission across the retina removes a significant fraction of the high-frequency noise originating in cone phototransduction.
Conclusions: :
Signal transmission across the cone circuitry improves the signal-to-noise ratio of photopic vision by removing high-frequency noise and the temporal precision of ganglion cell responses by speeding up the cone responses. Our results suggest that filtering in the cone circuitry represents a tradeoff between effective noise removal and the preservation of high-frequency signal components needed for rapid vision.
Keywords: retinal connections, networks, circuitry • photoreceptors: visual performance • retina: proximal (bipolar, amacrine, and ganglion cells)