Synaptic influences on rat ganglion-cell photoreceptors

J Physiol. 2007 Jul 1;582(Pt 1):279-96. doi: 10.1113/jphysiol.2007.133751. Epub 2007 May 17.

Abstract

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.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Amacrine Cells / metabolism
  • Amacrine Cells / physiology*
  • Amacrine Cells / radiation effects
  • Animals
  • Circadian Rhythm
  • Darkness
  • Excitatory Postsynaptic Potentials
  • Glutamic Acid / metabolism
  • Glycine / metabolism
  • In Vitro Techniques
  • Inhibitory Postsynaptic Potentials
  • Kinetics
  • Light
  • Male
  • 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
  • gamma-Aminobutyric Acid / metabolism

Substances

  • Rod Opsins
  • melanopsin
  • Glutamic Acid
  • gamma-Aminobutyric Acid
  • Glycine