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Orientation selectivity in rabbit retinal ganglion cells is mediated by presynaptic inhibition.

ABSTRACT: Cells sensitive to the orientation of edges are ubiquitous in visual systems, and have been described in the vertebrate retina, yet the synaptic mechanisms that generate orientation selectivity in the retina are largely unknown. Here, we analyze the synaptic mechanisms that generate selective responses to vertically and horizontally oriented stimuli in rabbit retinal ganglion cells. The data indicate that the excitatory and inhibitory inputs to orientation-selective ganglion cells are rendered orientation selective within the presynaptic circuitry. In accordance with previous extracellular recordings, presynaptic GABAergic inhibition is critical to generate orientation selectivity, and we show that it includes lateral inhibition of glutamatergic bipolar cells and serial inhibitory connections between GABAergic and glycinergic amacrine cells. Despite very similar spiking properties, vertically and horizontally selective ganglion cells (VS-GCs and HS-GCs, respectively) show marked differences in their underlying synaptic mechanisms. Both cell types receive glutamatergic inputs via non-NMDA (AMPA/kainate) and NMDA receptors, while VS-GCs receive additional excitation mediated by glycinergic disinhibition. A striking difference between these cells is that during nonpreferred simulation, excitation is suppressed and direct glycinergic inhibition is increased in HS-GCs, whereas for VS-GCs, both excitatory and inhibitory inputs are suppressed. Thus, orientation selectivity is generated presynaptically both by modulation of bipolar cell output and by serial inhibitory connections between amacrine cells. Minimal circuit models are proposed that account for these observations.

SUBMITTER: Venkataramani S

PROVIDER: S-EPMC3135107 | biostudies-other | 2010 Nov

REPOSITORIES: biostudies-other

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Orientation selectivity in rabbit retinal ganglion cells is mediated by presynaptic inhibition.

Venkataramani Sowmya S Taylor W Rowland WR

The Journal of neuroscience : the official journal of the Society for Neuroscience 20101101 46

Cells sensitive to the orientation of edges are ubiquitous in visual systems, and have been described in the vertebrate retina, yet the synaptic mechanisms that generate orientation selectivity in the retina are largely unknown. Here, we analyze the synaptic mechanisms that generate selective responses to vertically and horizontally oriented stimuli in rabbit retinal ganglion cells. The data indicate that the excitatory and inhibitory inputs to orientation-selective ganglion cells are rendered o ...[more]

PMID: 21084622

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Project description:BackgroundMany neurons in the central nervous system, including retinal ganglion cells (RGCs), possess asymmetric dendritic arbors oriented toward their presynaptic partners. How such dendritic arbors become biased during development in vivo is not well understood. Dendritic arbors may become oriented by directed outgrowth or by reorganization of an initially unbiased arbor. To distinguish between these possibilities, we imaged the dynamic behavior of zebrafish RGC dendrites during development in vivo. We then addressed how cell positioning within the retina, altered in heart-and-soul (has) mutants, affects RGC dendritic orientation.ResultsIn vivo multiphoton time-lapse analysis revealed that RGC dendrites initially exhibit exploratory behavior in multiple directions but progressively become apically oriented. The lifetimes of basal and apical dendrites were generally comparable before and during the period when arbors became biased. However, with maturation, the addition and extension rates of basal dendrites were slower than those of the apical dendrites. Oriented dendritic arbors were also found in misplaced RGCs of the has retina but there was no preferred orientation amongst the population. However, has RGCs always projected dendrites toward nearby neuropil where amacrine and bipolar cell neurites also terminated. Chimera analysis showed that the abnormal dendritic organization of RGCs in the mutant was non-cell autonomous.ConclusionsOur observations show that RGC dendritic arbors acquire an apical orientation by selective and gradual restriction of dendrite addition to the apical side of the cell body, rather than by preferential dendrite stabilization or elimination. A biased arbor emerges at a stage when many of the dendritic processes still appear exploratory. The generation of an oriented RGC dendritic arbor is likely to be determined by cell-extrinsic cues. Such cues are unlikely to be localized to the basal lamina of the inner retina, but rather may be provided by cells presynaptic to the RGCs.

Dataset Information

Orientation selectivity in rabbit retinal ganglion cells is mediated by presynaptic inhibition.

Publications

Orientation selectivity in rabbit retinal ganglion cells is mediated by presynaptic inhibition.

Similar Datasets

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