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Comparative Study
. 2010 Sep 1;588(Pt 17):3243-53.
doi: 10.1113/jphysiol.2010.192716. Epub 2010 Jul 12.

Synaptic inputs and timing underlying the velocity tuning of direction-selective ganglion cells in rabbit retina

Benjamin Sivyer  1 , Michiel van Wyk, David I Vaney, W Rowland Taylor
Affiliations
Comparative Study

Synaptic inputs and timing underlying the velocity tuning of direction-selective ganglion cells in rabbit retina

Benjamin Sivyer et al. J Physiol. .

Abstract

There are two types of direction-selective ganglion cells (DSGCs) identified in the rabbit retina, which can be readily distinguished both morphologically and physiologically. The well characterized ON-OFF DSGCs respond to a broad range of image velocities whereas the less common ON DSGCs are tuned to slower image velocities. This study examined how the synaptic inputs shape the velocity tuning of DSGCs in an isolated preparation of the rabbit retina. The receptive-field properties were mapped by extracellular spike recordings and compared with the light-evoked excitatory and inhibitory synaptic conductances that were measured under voltage-clamp. The synaptic mechanisms underlying the generation of direction selectivity appear to be similar in both cell types in that preferred-direction image motion elicits a greater excitatory input and null-direction image motion elicits a greater inhibitory input. To examine the temporal tuning of the DSGCs, the cells were stimulated with either a grating drifted over the receptive-field centre at a range of velocities or with a light spot flickered at different temporal frequencies. Whereas the excitatory and inhibitory inputs to the ON-OFF DSGCs are relatively constant over a wide range of temporal frequencies, the ON DSGCs receive less excitation and more inhibition at higher temporal frequencies. Moreover, transient inhibition precedes sustained excitation in the ON DSGCs, leading to slowly activating, sustained spike responses. Consequently, at higher temporal frequencies, weaker excitation combines with fast-rising inhibition resulting in lower spike output.

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Figures

Figure 1
Figure 1. Directional tuning of DSGCs
A, dendritic morphology of an ON DSGC revealed by dye filling with Neurobiotin; the terminal dendrites often branch at right angles from the parent dendrite, producing a space-filling lattice. Scale bar = 100 μm. B, current-clamp recordings from an ON DSGC in response to a light bar moved in 12 directions through the receptive field; the polar plot shows the mean number of spikes for each direction of image motion (squares), together with a von Mises fit of the data (continuous line).
Figure 2
Figure 2. Mean directional tuning functions for ON and ON–OFF DSGCs
Mean directional tuning functions for 17 ON DSGCs (A) and 55 ON–OFF DSGCs (B), showing both the total spike counts to a light bar moved in 12 directions through the receptive field (left panels) and the maximum firing rate (right panels). The continuous line shows the von Mises fit for each data set.
Figure 3
Figure 3. Conductance analysis of voltage-clamped currents in ON DSGCs
A and B, extracellular spike responses of an ON DSGC to a light bar moving in the preferred direction (A) and the opposite null direction (B). C and D, current recordings at holding potentials from −90 to −10 mV in response to a light bar moving in the preferred direction (C) and the null direction (D). E and F, sample I–V plots at the time points marked with a black square in C and D; the continuous line shows the linear fit to the I–V relation. G and H, change in the whole-cell zero-current potential (ΔVr), calculated by interpolation of the whole-cell I–V plots; ΔVr was depolarized during preferred-direction motion (G) and hyperpolarized during null-direction motion (H). I and J, excitatory (Ge, black) and inhibitory (Gi, grey) synaptic conductance calculated for the voltage-clamped responses to preferred-direction motion (I) and null-direction motion (J); Ge was greater in the preferred direction whereas Gi was greater in the null direction.
Figure 4
Figure 4. Directionality of synaptic inputs to ON DSGCs
The integrated excitatory conductance (GE) and the integrated inhibitory conductance (GI) in the preferred direction plotted against those in the null direction; in most cells, GE was greater in the preferred direction while GI was greater in the null direction.
Figure 5
Figure 5. Step responses and intrinsic membrane properties of DSGCs
A and B, extracellular spike recordings of individual DSGCs (upper panels) and mean spike-frequency histograms (±s.e.m.) of 20 ON DSGCs and 11 ON–OFF DSGCs (lower panels) to a light spot flashed in the receptive-field centre for 2 s; the ON DSGCs show sustained firing throughout the flash whereas the ON–OFF DSGCs fire transiently at the onset and termination of the flash. C and D, current-clamp recordings from an ON DSGC (C) and an ON–OFF DSGC (D) in response to the same stimulus as A and B. E, steady current injection into an ON DSGC produces sustained firing that shows only mild accommodation.
Figure 6
Figure 6. Excitatory and inhibitory conductances evoked by step illumination in ON and ON–OFF DSGCs
Excitatory conductance (Ge) and inhibitory conductance (Gi) evoked by step illumination in an ON DSGC (A and C) and an ON–OFF DSGC (B and D). Ge remains elevated throughout illumination in the ON DSGC but rises transiently at the onset and termination of the flash in the ON–OFF DSGC.
Figure 7
Figure 7. Temporal response properties of DSGCs to moving gratings and stationary flickering spots
A and B, mean spike-frequency histograms (±s.e.m.) for ON DSGCs (n= 11) and ON–OFF DSGCs (n= 15) in response to gratings moved in the preferred direction at different velocities. C and D, spike counts in response to moving gratings (filled circles) and stationary flickering spots (open squares) matched for temporal frequency; the spike counts are vertically scaled to account for differences in the absolute number of spikes generated by moving and stationary temporal stimuli.
Figure 8
Figure 8. Temporal response properties of synaptic inputs to DSGCs
A and B, mean excitatory conductance (Ge, black, ±s.e.m.) and mean inhibitory conductance (Gi, grey, ±s.e.m.) in 7 ON DSGCs (A) and 6 ON–OFF DSGCs (B) in response to gratings moved at different velocities through the receptive field. C and D, integral excitatory conductance (GE, black, ±s.e.m.) and integral inhibitory conductance (GI, grey, ±s.e.m.) for the same data sets as A and B.
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