Article

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

Smith-Kettlewell Eye Research Institute, San Francisco, CA 94115, USA.
Visual Neuroscience (Impact Factor: 1.68). 01/1997; 14(1):39-54. DOI: 10.1017/S0952523800008749
Source: PubMed

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.

0 Bookmarks
 · 
36 Views
  • Source
    [Show abstract] [Hide abstract]
    ABSTRACT: We investigated the morphology, distribution and synaptic connectivity of cholinergic neurons in the mouse retina by immunocytochemistry, using antisera against choline acetyltransferase (ChAT). ChAT-immunoreactive amacrine cells fall into two groups according to the localization of their somas in the retina: one is situated in the inner nuclear layer (INL), near the border of the inner plexiform layer (IPL), and the other is displaced in the ganglion cell layer (GCL). The dendrites of amacrine cells from the INL ramify in sublamina a and that of the displaced amacrine cells ramify in sublamina b of the IPL. Double labeling with an antisera against ChAT and r-aminobutyric acid (GABA) demonstrated that these labeled cells formed a subpopulation of GABAergic amacrine cells. The synaptic connectivity of ChAT-immunoreactive amacrine cells was identified in the IPL by electron microscopy. The most frequent synaptic input of ChAT-labeled amacrine cells was from bipolar cells in both sublaminae a and b of the IPL, followed by labeled amacrine cells and unlabeled amacrine cells. Their primary output targets were onto ganglion cells in both sublaminae a and b and output onto ganglion cells was more frequently observed in sublamina b of the IPL. Our results suggest that cholinergic amacrine cells in the mouse retina are very similar to their counter parts in other mammals, and they can attribute a major role in the pathway feeding into directionally selective ganglion cells.
    01/2004; 34(4).
  • Source
    [Show abstract] [Hide abstract]
    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.
    Experimental Eye Research 05/2014; DOI:10.1016/j.exer.2014.02.021 · 3.02 Impact Factor
  • Source
    [Show abstract] [Hide abstract]
    ABSTRACT: Although many effects of gamma-aminobutyric acid (GABA) on retinal function have been attributed to GABA(A) and GABA(C) receptors, specific retinal functions have also been shown to be mediated by GABA(B) receptors, including facilitation of light-evoked acetylcholine release from the rabbit retina (Neal and Cunningham [1995] J. Physiol. 482:363-372). To explain the results of a rich set of experiments, Neal and Cunningham proposed a model for this facilitation. In this model, GABA(B) receptor-mediated inhibition of glycinergic cells would reduce their own inhibition of cholinergic cells. In turn, muscarinic input from the latter to the glycinergic cells would complete a negative-feedback circuitry. In this study, we have used immunohistochemical techniques to test elements of this model. We report that glycinergic amacrine cells are GABA(B) receptor negative. In contrast, our data reveal the localization of GABA(B) receptors on cholinergic/GABAergic starburst amacrine cells. High-resolution localization of GABA(B) receptors on starburst amacrine cells shows that they are discretely localized to a limited population of its varicosities, the majority of likely synaptic-release sites being devoid of detectable levels of GABA(B) receptors. Finally, we identify a glycinergic cell that is a potential muscarinic receptor-bearing target of GABA(B)-modulated acetylcholine release. This target is the DAPI-3 cell. We propose, based on these data, a modification of the Neal and Cunningham model in which GABA(B) receptors are on starburst, not glycinergic amacrine cells.
    The Journal of Comparative Neurology 12/2005; 493(3):448-459. DOI:10.1002/cne.20766 · 3.51 Impact Factor