Is the input to a GABAergic synapse the sole asymmetry in turtle's retinal directional selectivity?

Abstract

We examined the effects of picrotoxin and pentylenetetrazol (PTZ) on the responses to motions of ON-OFF directionally selective (DS) ganglion cells of the turtle's retina. These drugs are antagonists of the inhibitory neurotransmitter GABA. For continuous motions, picrotoxin markedly reduced the overall directionality of the cells. In 21% of the cells, directional selectivity was lost regardless of speed and contrast. However, other cells maintained their preferred direction despite saturating concentrations of picrotoxin. And in most cells, loss, maintenance, or even reversal of preferred and null directions could occur as speed and contrast were modulated. In 50% of the cells, reversal of preferred and null directions occurred at some condition of visual stimuli. However, picrotoxin did not tend to alter the preferred-null axis for directional selectivity. For apparent motions, picrotoxin made motion facilitation, which normally occurs exclusively in preferred-direction responses, to become erratic and often occur during null-direction motions. Finally, PTZ had effects similar to picrotoxin but with less potency. The results in this paper indicated that models of directional selectivity based solely on a GABAergic implementation of Barlow and Levick's asymmetric-inhibition model do not apply to the turtle retina. Alternative models may comprise multiple directional mechanisms and/or a symmetric inhibitory one, but not asymmetric facilitation.

Visual Stimulation Reverses the Directional Preference of Direction-Selective Retinal Ganglion Cells

“…In all cases, this application abolished the DS response and increased the response to stimuli in all directions (n=4, Figure 3A, B). These findings distinguish reversal described here from paradoxical reversal of the PD and ND that has been reported in the presence of GABA blockers (Ackert et al, 2009; Grzywacz et al, 1997; Smith et al, 1996; Trenholm et al, 2011). …”

Parallel Mechanisms Encode Direction in the Retina

“…Even in previous studies where directionally selective responses were detectable under saturating concentrations of inhibitory blockers, they were relatively mild (Smith et al, 1996; Grzywacz et al, 1997). Because we had performed our initial experiments at relatively slow stimulus speeds, we next tested the effects of varying speed on DSI, in an attempt to reconcile our findings with previous work.…”

“…In contrast to inhibitory circuit mechanisms, previous studies in a variety of species have reported that DS responses persisted when GABA A receptors were blocked (Bülthoff and Bülthoff, 1987; Egelhaaf et al, 1990; Öğmen, 1991; Smith et al, 1996; Grzywacz et al, 1997; Ackert et al, 2009). Much less is known about mechanisms that could generate directional selectivity in the retina independent of inhibitory circuits.…”

GABA blockade unmasks an OFF response in ON direction selective ganglion cells in the mammalian retina

“…These results suggest that the directional OFF response has the capability to influence optokinetic signals, at least when the ON response component is blocked. Studies of rabbit and turtle retinas indicate that after application of PTX, up to 50% of ON–OFF DS ganglion cells still show direction selective responses, but often with reverse preference (Smith et al 1996; Grzywacz et al 1997). PTX‐induced reversals in the directional preference of neurons have also been reported in invertebrate eyes (Bülthoff & Bülthoff, 1987; Öğmen, 1991).…”