Synaptic influences on rat ganglion-cell photoreceptors

• Published in: The Journal of physiology Vol. 582; no. 1; pp. 279 - 296
• Main Authors: Wong, Kwoon Y., Dunn, Felice A., Graham, Dustin M., Berson, David M.
• Format: Journal Article
• Language: English
• Published: Oxford, UK The Physiological Society 01-07-2007; Blackwell Publishing Ltd; Blackwell Science Inc
• Subjects: Amacrine Cells - metabolism; Amacrine Cells - physiology; Amacrine Cells - radiation effects; Animals; Circadian Rhythm; Darkness; Excitatory Postsynaptic Potentials; gamma-Aminobutyric Acid - metabolism; Glutamic Acid - metabolism; Glycine - metabolism; In Vitro Techniques; Inhibitory Postsynaptic Potentials; Kinetics; Light; Male; Neuroscience; Patch-Clamp Techniques; Photic Stimulation; Rats; Rats, Sprague-Dawley; Retinal Bipolar Cells - metabolism; Retinal Bipolar Cells - physiology; Retinal Bipolar Cells - radiation effects; Retinal Ganglion Cells - metabolism; Retinal Ganglion Cells - physiology; Retinal Ganglion Cells - radiation effects; Rod Opsins - metabolism; Sensory Thresholds; Synaptic Transmission - radiation effects; Visual Pathways - cytology; Visual Pathways - metabolism; Visual Pathways - physiology; Visual Pathways - radiation effects
• ISSN: 0022-3751; 1469-7793
• DOI: 10.1113/jphysiol.2007.133751

The intrinsically photosensitive retinal ganglion cells (ipRGCs) provide a conduit through which rods and cones can access
brain circuits mediating circadian entrainment, pupillary constriction and other non-image-forming visual functions. We characterized
synaptic inputs to ipRGCs in rats using whole-cell and multielectrode array recording techniques. In constant darkness all
ipRGCs received spontaneous excitatory and inhibitory synaptic inputs. Light stimulation evoked in all ipRGCs both synaptically
driven (‘extrinsic’) and autonomous melanopsin-based (‘intrinsic’) responses. The extrinsic light responses were depolarizing,
about 5 log units more sensitive than the intrinsic light response, and transient near threshold but sustained to brighter
light. Pharmacological data showed that ON bipolar cells and amacrine cells make the most prominent direct contributions to
these extrinsic light responses, whereas OFF bipolar cells make a very weak contribution. The spatial extent of the synaptically
driven light responses was comparable to that of the intrinsic photoresponse, suggesting that synaptic contacts are made onto
the entire dendritic field of the ipRGCs. These synaptic influences increase the sensitivity of ipRGCs to light, and also
extend their temporal bandpass to higher frequencies. These extrinsic ipRGC light responses can explain some of the previously
reported properties of circadian photoentrainment and other non-image-forming visual behaviours.