Distinct expressions of contrast gain control in parallel synaptic pathways converging on a retinal ganglion cell

J Physiol. 2008 Nov 15;586(22):5487-502. doi: 10.1113/jphysiol.2008.156224. Epub 2008 Oct 2.


Visual neurons adapt to increases in stimulus contrast by reducing their response sensitivity and decreasing their integration time, a collective process known as 'contrast gain control.' In retinal ganglion cells, gain control arises at two stages: an intrinsic mechanism related to spike generation, and a synaptic mechanism in retinal pathways. Here, we tested whether gain control is expressed similarly by three synaptic pathways that converge on an OFF alpha/Y-type ganglion cell: excitatory inputs driven by OFF cone bipolar cells; inhibitory inputs driven by ON cone bipolar cells; and inhibitory inputs driven by rod bipolar cells. We made whole-cell recordings of membrane current in guinea pig ganglion cells in vitro. At high contrast, OFF bipolar cell-mediated excitatory input reduced gain and shortened integration time. Inhibitory input was measured by clamping voltage near 0 mV or by recording in the presence of ionotropic glutamate receptor (iGluR) antagonists to isolate the following circuit: cone --> ON cone bipolar cell --> AII amacrine cell --> OFF ganglion cell. At high contrast, this input reduced gain with no effect on integration time. Mean luminance was reduced 1000-fold to recruit the rod bipolar pathway: rod --> rod bipolar cell --> AII cell --> OFF ganglion cell. The spiking response, measured with loose-patch recording, adapted despite essentially no gain control in synaptic currents. Thus, cone bipolar-driven pathways adapt differently, with kinetic effects confined to the excitatory OFF pathway. The ON bipolar-mediated inhibition reduced gain at high contrast by a mechanism that did not require an iGluR. Under rod bipolar-driven conditions, ganglion cell firing showed gain control that was explained primarily by an intrinsic property.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Contrast Sensitivity / physiology*
  • Electrophysiology
  • Guinea Pigs
  • Models, Neurological
  • Nonlinear Dynamics
  • Photic Stimulation
  • Retinal Ganglion Cells / physiology*
  • Synapses / physiology
  • Visual Pathways / physiology