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Synaptic physiology of direction selectivity in the retina - PubMed

  • ️Tue Jan 01 2008

Review

Synaptic physiology of direction selectivity in the retina

Z Jimmy Zhou et al. J Physiol. 2008.

Abstract

Detection of the direction of image movement is accomplished first in the retina by an elegant neuronal circuit, which integrates multiple levels of spatially asymmetric synaptic interactions among subsets of bipolar, amacrine and ganglion cells. Central to these interactions is the asymmetric GABAergic inhibition exerted by the starburst amacrine cell (SAC), a cholinergic and GABAergic interneuron with a radially symmetric dendritic tree. SACs make reciprocal GABAergic synapses on each other to create a direct inhibitory receptive field surround, which suppresses the response of each SAC to centripetal image movement. Each radially projecting branch of a SAC responds to image movement with a centrifugal bias and, through directionally asymmetric synaptic connections with the dendrites of direction-selective ganglion cells (DSGCs), exerts a spatially offset inhibition that vetoes the response of DSGCs to image movement in a specific (null) direction. Recent physiological studies have greatly advanced our understanding of the mechanism of direction selectivity and also revealed a new level of complexity that remains to be understood.

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Figures

Figure 1
Figure 1. A current model of direction selectivity in DSGCs based on asymmetric wiring between SACs and DSGCs

The processes of starburst cells (‘s’, blue) that point in the null direction provide inhibition to DS cell dendrites (‘DS’, grey). Starburst processes respond best to movement away from the cell body, which makes the inhibitory input delivered to DS cells larger for movement in the null direction (bottom panel) than for movement in the preferred direction (top panel). An additional inhibition acts presynaptically to reduce excitation for null direction movement. Although this presynaptic inhibition is depicted as coming from starburst cells, the existence of another type of cell cannot be ruled out. The excitatory input to DS cells probably comes from bipolar cells (‘b’, red) and may also have a cholinergic component from other starburst cells. For movement in the null direction, the inhibitory input reaches each subregion of the DS cell ahead of the stimulus edge and therefore before excitation. For movement in the preferred direction, inhibition lags behind excitation. Reproduced from Fried et al. 2002, Nature 420, 411–414; reprinted by permission from Macmillan Publishers Ltd.

Figure 2
Figure 2. Directional suppression of calcium responses in SAC distal dendrites and of inhibitory inputs to DSGCs by two-flash apparent motion

A, photomicrograph of a SAC under whole-cell current clamp with a pipette filled with Oregon Green 488 BAPTA-1. The rectangle (marked CTL) indicates the area in which a control light is flashed both to elicit a light response and to measure the Ca2+ response from the dendrites. Simulated centripetal motion is generated by flashing another light in the surround area (CP) 200 ms prior to the onset of the control (CTL) flash. Scale bar: 50 μm. B, the average fluorescence response of eight varicosities in area CTL to a CTL flash (blue trace) is strongly suppressed by a preceding CP flash that simulates a centripetal motion (red trace). Fo indicates the basal fluorescence intensity immediately prior to the light response. C, inhibitory synaptic inputs to a DSGC in response to flashed bars (100 × 300 μm). Simulated preferred-direction motion greatly suppresses the inhibitory input to the DSGC, showing a similarity to the suppression of the calcium response in SAC dendrites by CP motion. Adapted from from Lee & Zhou (2006), Neuron 51, 787–799 and from Fried et al. (2005), Neuron 46, 117–127, with permission from Elsevier.

Figure 3
Figure 3. A synaptic model of direction selectivity at the distal processes of SACs

The concentric centre–surround receptive field of a SAC (SCA0) is shaped largely by a centre excitatory input from bipolar cells (BC) and a surround inhibitory input from neighbouring SACs. Centripetal (CP) light movement evokes a leading GABAergic input (blue arrow) to the distal zone from the surround SACs (represented by SAC1), whereas centrifugal (CF) light movement evokes predominantly an excitatory input (red arrow) to the distal zone from the centre. Adapted from Lee & Zhou (2006, Neuron 51,787–799 with permission from Elsevier.

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