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

Abstract

We examined contrast, direction of motion, and concentration dependencies of the effects of GABAergic and cholinergic antagonists, and anticholinesterases on responses to movement of On—Off directionally selective (DS) ganglion cells of the rabbit's retina. The drugs tested were curare and hexamethonium bromide (cholinergic antagonists), physostigmine (anticholinesterase), and picrotoxin (GABAergic antagonist). They all reduced the cells' directional selectivity, while maintaining their preferred-null axis. However, cholinergic antagonists did not block directional selectivity completely even at saturating concentrations. The failure to eliminate directional selectivity was probably not due to an incomplete blockade of cholinergic receptors. In a extension of a Masland and Ames (1976) experiment, saturating concentrations of antagonists blocked the effects of exogenous acetylcholine or nicotine applied during synaptic blockade. Consequently, a noncholinergic pathway may be sufficient to account for at least some directional selectivity. This putative pathway interacts with the cholinergic pathway before spike generation, since physostigmine eliminated directional selectivity at contrasts lower than those saturating responses. This elimination apparently resulted from cholinergic-induced saturation, since reduction of contrast restored directional selectivity. Under picrotoxin, directional selectivity was lost in 33% of the cells regardless of contrast. However, 47% maintained their preferred direction despite saturating concentrations of picrotoxin, and 20% reversed the preferred and null directions. Therefore, models based solely on a GABAergic implementation of Barlow and Levick's asymmetric-inhibition model or solely on a cholinergic implementation of asymmetric-excitation models are not complete models of directional selectivity in the rabbit. We propose an alternate model for this retinal property.

Starburst cholinergic amacrine cells in the tree shrew retina

“…For quite some time, they have been assumed to play an important role in the pathway leading to directionally selective ganglion cells, and several models on their contribution to directional selectivity have been proposed (see, e.g., Masland and Tauchi, 1986;Borg-Graham and Grzywacz, 1992). Most recently, the importance of starburst cells for the implementation of directional selectivity in the rabbit retinal ganglion cells has been questioned (Grzywacz et al, 1997;He and Masland, 1997), and the functional roles of this distinct amacrine cell type remain enigmatic.…”

“…We assume the same ON/OFF dichotomy in tree shrew. Rabbit starburst cells costratify and synapse with directionally selective ganglion cells (Vaney et al, 1989;Famiglietti, 1992; for recent discussions of the functional effects, see Yang and Masland, 1992;Grzywacz et al, 1997;Kittila and Massey, 1997). The tree shrew also possesses directionally selective ganglion cells (van Dongen et al, 1976), but their morphology is not known, and it remains to be shown that they connect to the starburst cells.…”

Diverse Synaptic Mechanisms Generate Direction Selectivity in the Rabbit Retina

“…These amacrine cells contain both acetylcholine and GABA and thus could contribute to both the excitatory and inhibitory mechanisms (Vaney et al, 1989;Borg-Graham and Grzywacz, 1992;Grzywacz et al, 1997). The role of starburst cells within the direction-selective circuit is controversial, however, with one report claiming that they are critical (Yoshida et al, 2001) and another claiming that they are not essential (He and Masland, 1997).…”

The dendritic architecture of the cholinergic plexus in the rabbit retina: Selective labeling by glycine accumulation in the presence of sarcosine

“…He and Masland (1997) obtained clear evidence that the On-Off DS cells receive symmetrical input from surrounding cholinergic cells by using a laser to selectively ablate Cb amacrine cells located on either the preferred side of the ganglion cell or the opposite null side (see also Vaney et al, 2000). In contrast, Grzywacz et al (1997Grzywacz et al ( , 1998 have interpreted their own electrophysiological results as indicating that the On-Off DS cells receive strong input from cholinergic cells located on the preferred side and weak input from cholinergic cells located on the null side. In support of this conclusion, the authors cite abstracts of a morphological study showing that "the amount of dendritic material in proximity to DS ganglion cells' dendrites is larger for preferred-side cholinergic cells than for nullside ones" (Amthor and Grzywacz, 1995;Grzywacz et al, 1995).…”