Non-monotonic contrast behavior in directionally selective ganglion cells and evidence for its dependence on their GABAergic input

Abstract

We serendipitously discovered that the preferred-direction responses of ON-OFF directionally selective (DS) ganglion cells in the rabbit retina fall as a function of contrast when the contrast of a moving bar exceeds about 100%. Null-direction responses did not fall for contrasts up to 400%. Because the non-monotonic (rise-then-fall) behavior as a function of contrast occurred only for preferred-direction responses, it must depend on the mechanism of directional selectivity. It became thus of interest to investigate how this non-monotonicity depends on the major synapses involved in directional selectivity. Blockades of nicotinic acetylcholine (ACh) and NMDA glutamate receptors reduced responses without eliminating preferred-response non-monotonicity. Blocking GABAergic inhibition, however, did eliminate non-monotonicity. These results pose a difficult puzzle, since in the accompanying paper (Grzywacz et al., 1998), we showed that residual responses under combined nicotinic and NMDA blockades are not statistically significantly directionally selective. How is it possible that null-direction GABAergic inhibition affects non-nicotinic-non-NMDA residual responses without generating directional selectivity? This may happen if there exists an asymmetric GABAergic input to distal dendrites of the DS cell while the excitatory, non-nicotinic-non-NMDA input is to proximal dendrites. In support of this hypothesis, bath-applied GABA reduces responses to exogenous ACh under synaptic block, providing for the first time in the rabbit's retina, direct evidence of GABA receptors on DS cells.

Separability of stimulus parameter encoding by on-off directionally selective rabbit retinal ganglion cells

“…We note that, contrary to the results reported by Merwine et al (1998) for contrast, we did not observe a fall in response magnitude at high luminance levels. This, however, may be explained by the possibility that the luminance levels that we tested were not high enough to elicit this effect.…”

“…Generally, as the luminance increased, the mean number of spikes also increased, but in a highly nonlinear fashion: at the low luminance levels it exhibited a rapid rise followed by a plateau indicating saturation at the high luminance levels. Contrary to the results reported by Merwine et al (1998) for contrast, we did not observe a fall in response at high luminance levels, possibly because the luminance levels that we tested were not high enough to elicit this effect. As in the case of speed, we found that the luminance tuning curves were similar in shape independent of direction, although they differed in maximum and minimum values.…”

“…On-Off DS RGCs have also been shown to be broadly tuned for contrast, maintaining directional selectivity over the entire range of contrasts to which they respond, even at contrasts of a few percent . Contrast tuning curves for the preferred and null directions determined in that study were found to be nonmonotonic in the same rise-then-fall fashion as speed tuning curves, consistent with an earlier study in which spike count rather than mean firing rate was the response measure (Merwine et al 1998).…”

“…The responses of On-Off DS RGCs for the preferred and null directions have been shown to depend nonmonotonically on the stimulus contrast: they increase at low contrasts and, after reaching a peak, decrease at high contrasts, both when the mean firing rate and the mean spike count (Merwine et al 1998) are considered. Here, we investigated a closely related cell characteristic, namely luminance tuning curves, employing more directions than just the preferred and null ones.…”

Computation of motion direction in the vertebrate retina

“…A hallmark of retinal DS cells is their surprising robustness: They easily outperform their counterparts in the primary visual cortex (V1) in many respects: ON-OFF DS cells detect the direction of motion within their receptive field centre more reliably, largely independent of contrast [56] and velocity [37, 65,88] and even for small movements of a few micrometres [38]. Direction discrimination is roughly constant over a velocity range of more than two orders of magnitude (reviewed in [37]).…”