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Dennis M. Dacey, Joanna D. Crook, Michael B. Manookin, Orin S. Packer; Absence Of Synaptic Inhibition Associated With S-cone On Excitatory Input To The Small Bistratified, Blue-yellow Opponent Ganglion Cell Of The Macaque Monkey Retina. Invest. Ophthalmol. Vis. Sci. 2011;52(14):4571.
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© ARVO (1962-2015); The Authors (2016-present)
The primate small bistratified ganglion cell receives input from ON and OFF bipolar cells that contact short (S) vs long (L) and middle (M) wavelength sensitive cones respectively, establishing ON vs OFF pathway synaptic excitation as the basis for 'blue-yellow' color opponency (Crook et al., 2010, ARVO, 5178). However, the role of synaptic inhibition in the blue-yellow circuitry is not understood. Our purpose therefore was to determine the origin and the dynamics of inhibition associated with S-ON vs L+M-OFF pathways.
We recorded in whole-cell voltage clamp from small bistratified cells in an in vitro wholemount of the macaque retina. Synaptic currents were evoked by either S-cone or L+M-cone selective stimuli in a variety of spatio-temporal configurations. Inhibitory conductances were extracted from current-voltage plots at each time point in the stimulus by modeling the total stimulus-evoked synaptic current as a linear sum of excitatory and inhibitory currents with reversal potentials at zero and -67 mV respectively. The contribution of inhibition to the S- and L+M-evoked currents was also measured after bath application of GABAergic and glycinergic receptor antagonists (TPMPA, GABAzine and strychnine).
Both S and L+M cone-selective stimuli evoked large excitatory conductances (18.0±1.3 vs 11.1±0.3 nS; mean±SEM; n = 21 cells). However, NO synaptic inhibition was associated with either the ON (0.12±0.15nS) or the OFF phase (0.07±0.04nS) of S cone stimulus modulation. By contrast, L+M cone stimuli evoked distinct feedforward-OFF phase (5.30±0.90nS) and crossover-ON phase inhibition (7.50±1.10nS). L+M cone feedforward and crossover inhibition were abolished by block of GABAergic and glycinergic transmission respectively. By contrast, blocking synaptic inhibition had no effect on the synaptic currents evoked by selective S cone modulation.
We have discovered a dramatic S vs L+M cone asymmetry in the inhibitory input to the small bistratified ganglion cell. We predict that the previously observed inhibitory synapses on the inner-ON dendritic tier (Percival et al., J Comp Neurol, 517:655, 2009) must be driven not by the S-ON bipolar but by a diffuse L+M ON bipolar cell to thereby elicit L+M crossover inhibition. The absence of S cone-associated inhibition at the opponent locus may underlie unusual features of the human S-cone pathway such as susceptibility to response saturation (eg., Stromeyer et al., Vis Res; 19:1025, 1979).
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