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M. B. Manookin, J. D. Crook, D. M. Dacey; Synaptic Origins of Excitatory and Inhibitory Conductances in Midget and Parasol Ganglion Cells of the Macaque Monkey Retina. Invest. Ophthalmol. Vis. Sci. 2010;51(13):1867.
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© ARVO (1962-2015); The Authors (2016-present)
The midget and parasol ganglion cells provide the major input to the parvo- and magnocellular LGN, show ON- and OFF-center-surround organization and play fundamental roles in achromatic spatial vision. Midget cells have sustained light responses, linear contrast gain and may set the limit on spatial resolution. Parasol cells show transient responses, non-linear contrast gain and may contribute strongly to motion processing. Our goal is to determine the role played by synaptic excitation and inhibition in the signaling properties of the two distinct visual pathways.
We recorded in whole-cell voltage-clamp from macaque retina in vitro at holding potentials between ~-90 to +50 mV. Stimuli were centered spots, annuli and drifting gratings. Stimulus contrast was sine wave modulated at 2 Hz (mean luminance, ~10^5-10^6 R*/cone/sec). Excitatory and inhibitory conductances were derived from light evoked currents using established methods (e.g., Taylor and Vaney, J Neurosci 22:7712 2002).
Both ON- and OFF-center parasol cells showed prominent crossover inhibition, blocked by a glycine-receptor antagonist (strychnine); and feedforward inhibition, blocked by GABA(A/C)-receptor antagonists (GABAzine and TPMPA). However, there were distinct ON/OFF asymmetries in this circuitry: crossover inhibition was spatially restricted to the ON parasol center but extended into the surround for OFF cells. In addition, inhibitory block in ON parasol cells unmasked a prominent OFF excitation. By contrast, midget cells lacked glycinergic crossover inhibition but blocking GABA receptors uncovered feedforward inhibition suppressed by strychnine. Parasol and midget cells also differed in their excitatory synaptic organization. In parasols, excitation was mediated by a linear AMPA-receptor conductance, with a small contribution from NMDA receptors near Vrest (10-15% at -62 mV). In midget cells however, NMDA receptors provided 60-80% of the excitatory conductance at -62 mV (reversibly blocked with D-AP5).
There are major differences in inhibitory circuitry and glutamate receptor expression in parasol and midget cells. We hypothesize that the lack/presence of glycinergic crossover inhibition and NMDA receptor expression contributes to the linear vs non-linear visual physiology of the two pathways.
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