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

Smith-Kettlewell Eye Research Institute, San Francisco, CA 94115, USA.
Visual Neuroscience (Impact Factor: 2.21). 01/1997; 14(1):39-54. DOI: 10.1017/S0952523800008749
Source: PubMed


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.

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    • "10 ; O ' Malley et al . , 1992 ; Strang et al . , 2007 ) . ACh and GABA are co - secreted from the SACs ( Kosaka et al . , 1988 ; Lee et al . , 2010 ; Masland , 2005 ; O ' Malley et al . , 1992 ; Vaney and Young , 1988 ) . The DS RGCs lose their direction - selectivity when the SACs are eliminated through immunotoxin mediated cell targeting ( Grzywacz et al . , 1997 ; Yoshida et al . , 2001 ) . These results therefore indicate that the SACs play a critical role in direction - selectivity ."
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    ABSTRACT: Direction-selective retinal ganglion cells (DS RGCs) respond strongly to a stimulus that moves in their preferred direction, but respond weakly or do not respond to a stimulus that moves in the opposite or null direction. DS RGCs are sensitive to acetylcholine, and starburst amacrine cells (SACs) make cholinergic synapses on DS RGCs. We studied the distributions of nicotinic acetylcholine receptor (nAChR) α7 and ß2 subunits on the dendritic arbors of DS RGCs to search for anisotropies that contribute to the directional preferences of DS RGCs. The DS RGCs from the retinas of postnatal mice (postnatal day P5, P10, and P15) were injected with Lucifer yellow, and injected cells were identified by their dendritic morphology. The dendrites of the DS RGCs were labeled with antibodies for either the nAChR α7 or ß2 subunit as well as postsynaptic density protein-95 (PSD-95), visualized by confocal microscopy, and reconstructed from high-resolution confocal images. The distribution of nAChR subunits on the dendritic arbors in both the ON and OFF layers of the RGCs revealed an asymmetrical pattern on early postnatal day P5. However, the distributions of nAChR subunits on the dendritic arbors were not asymmetric on P10 and P15. Our results therefore provide anatomical and developmental evidence suggesting that the nAChR α7 and ß2 subunits may involve in the early direction-selectivity formation of DS RGCs in the mouse retina.
    Full-text · Article · May 2014 · Experimental Eye Research
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    • "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). "
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    ABSTRACT: Direction selectivity in the retina is mediated by direction-selective ganglion cells. These cells are part of a circuit in which they are asymmetrically wired to inhibitory neurons. Thus, they respond strongly to an image moving in the preferred direction and weakly to an image moving in the opposite (null) direction. Here, we demonstrate that adaptation with short visual stimulation of a direction-selective ganglion cell using drifting gratings can reverse this cell's directional preference by 180°. This reversal is robust, long lasting, and independent of the animal's age. Our findings indicate that, even within circuits that are hardwired, the computation of direction can be altered by dynamic circuit mechanisms that are guided by visual stimulation. VIDEO ABSTRACT:
    Full-text · Article · Nov 2012 · Neuron
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    • "When blocking the excitatory input from the SACs, DS-RGCs still evoke a direction selectivity response [23, 31]. On the other hand, DS-RGCs lose their ability when SACs are completely eliminated by using immunotoxin-mediated cell targeting method [21]. Direction selectivity also persisted after laser ablation of SACs [23]. "
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    ABSTRACT: The detection of image motion is important to vision. Direction-selective retinal ganglion cells (DS-RGCs) respond strongly to stimuli moving in one direction of motion and are strongly inhibited by stimuli moving in the opposite direction. In this article, we investigated the distributions of kainate glutamate receptor subtypes KA1 and KA2 on the dendritic arbors of DS-RGCs in developing (5, 10) days postnatal (PN) and adult mouse retina to search for anisotropies. The distribution of kainate receptor subtypes on the DS-RGCs was determined using antibody immunocytochemistry. To identify their characteristic morphology, DS-RGCs were injected with Lucifer yellow. The triple-labeled images of dendrites, kinesin II, and receptors were visualized by confocal microscopy and were reconstructed from high-resolution confocal images. We found no evidence of asymmetry in any of the kainate receptor subunits examined on the dendritic arbors of both the On and Off layers of DS-RGCs in all periods of developing and adult stage that would predict direction selectivity.
    Full-text · Article · Feb 2012 · ACTA HISTOCHEMICA ET CYTOCHEMICA
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