Global Jitter Motion of the Retinal Image Dynamically Alters the Receptive Field Properties of Retinal Ganglion Cells

Abstract

Fixational eye movements induce aperiodic motion of the retinal image. However, it is not yet fully understood how fixational eye movements affect retinal information processing. Here we show that global jitter motion, simulating the image motion during fixation, alters the spatiotemporal receptive field properties of retinal ganglion cells. Using multi-electrode and whole-cell recording techniques, we investigated light-evoked responses from ganglion cells in the isolated goldfish retina. Ganglion cells were classified into six groups based on the filtering property of light stimulus, the membrane properties, and the cell morphology. The spatiotemporal receptive field profiles of retinal ganglion cells were estimated by the reverse correlation method, where the dense noise stimulus was applied on the dark or random-dot background. We found that the jitter motion of the random-dot background elongated the receptive filed along the rostral-caudal axis and temporally sensitized in a specific group of ganglion cells: Fast-transient ganglion cells. At the newly emerged regions of the receptive field local light stimulation evoked excitatory postsynaptic currents with large amplitude and fast kinetics without changing the properties of inhibitory postsynaptic currents. Pharmacological experiments suggested two presynaptic mechanisms underlying the receptive field alteration: (i) electrical coupling between bipolar cells, which expands the receptive field in all directions; (ii) GABAergic presynaptic inhibition from amacrine cells, which reduces the dorsal and ventral regions of the expanded receptive field, resulting in elongation along the rostral-caudal axis. Our study demonstrates that the receptive field of Fast-transient ganglion cells is not static but dynamically altered depending on the visual inputs. The receptive field elongation during fixational eye movements may contribute to prompt firing to a target in the succeeding saccade.