Synaptic inputs and timing underlying the velocity tuning of direction‐selective ganglion cells in rabbit retina

• Published in: The Journal of physiology Vol. 588; no. 17; pp. 3243 - 3253
• Main Authors: Sivyer, Benjamin, Van Wyk, Michiel, Vaney, David I., Taylor, W. Rowland
• Format: Journal Article
• Language: English
• Published: Oxford, UK Blackwell Publishing Ltd 01-09-2010; Wiley Subscription Services, Inc; Blackwell Science Inc
• Subjects: Animals; Circadian rhythm; Female; Light effects; Male; Neuroscience; Photic Stimulation - methods; Rabbits; Retina; Retina - cytology; Retina - physiology; Retinal ganglion cells; Retinal Ganglion Cells - cytology; Retinal Ganglion Cells - physiology; Synapses - physiology; Synaptic Transmission - physiology; Time Factors; Velocity
• ISSN: 0022-3751; 1469-7793
• DOI: 10.1113/jphysiol.2010.192716

There are two types of direction‐selective ganglion cells (DSGCs) identified in the rabbit retina, which can be readily distinguished both morphologically and physiologically. The well characterized ON–OFF DSGCs respond to a broad range of image velocities whereas the less common ON DSGCs are tuned to slower image velocities. This study examined how the synaptic inputs shape the velocity tuning of DSGCs in an isolated preparation of the rabbit retina. The receptive‐field properties were mapped by extracellular spike recordings and compared with the light‐evoked excitatory and inhibitory synaptic conductances that were measured under voltage‐clamp. The synaptic mechanisms underlying the generation of direction selectivity appear to be similar in both cell types in that preferred‐direction image motion elicits a greater excitatory input and null‐direction image motion elicits a greater inhibitory input. To examine the temporal tuning of the DSGCs, the cells were stimulated with either a grating drifted over the receptive‐field centre at a range of velocities or with a light spot flickered at different temporal frequencies. Whereas the excitatory and inhibitory inputs to the ON–OFF DSGCs are relatively constant over a wide range of temporal frequencies, the ON DSGCs receive less excitation and more inhibition at higher temporal frequencies. Moreover, transient inhibition precedes sustained excitation in the ON DSGCs, leading to slowly activating, sustained spike responses. Consequently, at higher temporal frequencies, weaker excitation combines with fast‐rising inhibition resulting in lower spike output.
Retinal ganglion cells are the neurons that transmit visual information from the eye to the brain. Some of these retinal ganglion cells are direction‐selective ganglion cells (DSGCs), which respond best to images moving in a particular direction, called the preferred direction, and are silent for motion in the opposite direction. In the retina, two types of DSGCs that project to different brain nuclei are thought to serve different functions, and differ markedly in their preferences for the speed of image motion (speed tuning); the more common ON–OFF DSGCs respond well to a wide range of image speeds whereas the less common ON DSGCs respond well to relatively slow image speeds. We show that differences in the magnitude and timing of the synaptic input signals to these two types of DSGCs can account for their different preferences for the speed of image motion. Knowledge of how speed tuning is generated in DSGCs increases our understanding of how image motion is encoded and processed in the visual system.