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. 2011 Nov 1;519(16):3128-38.
doi: 10.1002/cne.22720.

A novel type of complex ganglion cell in rabbit retina

Benjamin Sivyer  1 , Sowmya Venkataramani, W Rowland Taylor, David I Vaney
Affiliations

A novel type of complex ganglion cell in rabbit retina

Benjamin Sivyer et al. J Comp Neurol. .

Abstract

The 15-20 physiological types of retinal ganglion cells (RGCs) can be grouped according to whether they fire to increased illumination in the receptive-field center (ON cells), decreased illumination (OFF cells), or both (ON-OFF cells). The diversity of RGCs has been best described in the rabbit retina, which has three types of ON-OFF RGCs with complex receptive-field properties: the ON-OFF direction-selective ganglion cells (DSGCs), the local edge detectors, and the uniformity detectors. Here we describe a novel type of bistratified ON-OFF RGC that has not been described in either physiological or morphological studies of rabbit RGCs. These cells stratify in the ON and OFF sublaminae of the inner plexiform layer, branching at about 30% and 60% depth, between the ON and OFF arbors of the bistratified DSGCs. Similar to the ON-OFF DSGCs, these cells respond with transient firing to both bright and dark spots flashed in the receptive field but, unlike the DSGCs, they show no directional preference for moving stimuli. We have termed these cells "transient ON-OFF" RGCs. Area-response measurements show that both the ON and the OFF spike responses have an antagonistic receptive-field organization, but with different spatial extents. Voltage-clamp recordings reveal transient excitatory inputs at light ON and light OFF; this excitation is strongly suppressed by surround stimulation, which also elicits direct inhibitory inputs to the cells at light ON and light OFF. Thus the receptive-field organization is mediated both within the presynaptic circuitry and by direct feed-forward inhibition.

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Figures

Figure 1
Figure 1
Microscopic targeting of transient ON-OFF RGCs. Gradient-contrast optics micrograph of the RGC layer in the visual streak of the isolated rabbit retina. The arrow marks a small, round soma that is typical of transient ON-OFF RGCs. Displaced starburst amacrine cells are also numerous in the RGC layer but have slightly smaller somas that are almost filled by the nucleus (asterisks). The arrowhead marks a more elongated soma that is typical of a local edge detector RGC. Scale bar = 20 µm.
Figure 2
Figure 2
Extracellular spike responses to flashed stimuli. A: The visual stimulus was a 200-µm-diameter dark spot (shown) or light spot (not shown) of 50% contrast, flashed for 2 seconds in the center of the receptive field; the background illumination was in the photopic range. B: Spike raster plots from a transient ON-OFF RGC in response to 15 presentations of a bright spot (top) and a dark spot (bottom): the cell fires transiently at both light ON and light OFF. C: Spike recording from a local edge detector in response to a dark spot flashed for 6 seconds: the cell gives sustained responses at both light ON and light OFF.
Figure 3
Figure 3
Transient ON-OFF RGCs are not direction-selective. Polar plot of the spike responses to a dark bar moved through the receptive field in 12 directions spaced at 30° intervals; the first group of spikes to the leading edge is the OFF response (solid circles), and the second group of spikes to the trailing edge is the ON response (open circles).
Figure 4
Figure 4
Dendritic morphology of transient ON-OFF RGCs. A: Two adjacent transient ON-OFF RGCs in the visual streak labeled with Neurobiotin following physiological identification. Both cells have densely branched bistratified dendritic trees, with dendrites in the ON sublamina (green) arising from a more dense stratification in the OFF sublamina (magenta). B: High-power image of the boxed area in A, illustrating that the ON arbor (green) is formed from short dendrites (arrowheads) arising from the OFF arbor (magenta). C: The confocal z-projection shown in B is split into three levels: OFF dendrites in blue, ON dendrites in red, and intermediate dendrites in green. This representation emphasizes the steep vertical branching between the OFF and the ON arbors, as evident in the punctate green profiles (arrowheads), which mark transitions between the two arbors. Scale bar = 100 µm in A; 20 µm in B (applies to B,C).
Figure 5
Figure 5
Stratification of transient ON-OFF RGCs. A: Side projection of a transient ON-OFF RGC labeled with Neurobiotin (green) following physiological identification. The retina is double labeled with an antibody against calbindin, which labels a population of bipolar cells (cyan). The RGC dendrites are bistratified and located above the axon terminals of the calbindin bipolar cells, which branch around the S4/S5 border. The ON and OFF arbors in S3 and S2 interconnect through vertical branches (arrowheads) and some OFF dendrites branch in S1, above the main OFF arbor (arrows). B: Side projection of a transient ON-OFF RGC labeled with Neurobiotin (green) and an overlapping ON-OFF DSGC labeled with Lucifer yellow (magenta); the arbors of the transient ON-OFF RGC stratify between the arbors of the ON-OFF DSGC. C: Mean fluorescence taken from z-sections through the ON-OFF DSGC (magenta) and transient ON-OFF RGC (green) in B and though the calbindin bipolar cells in A. D: Confocal reconstruction of overlapping dye-filled RGCs shows that the dendritic tree of the transient ON-OFF RGC (green) is slightly larger than that of the ON-OFF DSGC (magenta). Scale bars = 50 µm.
Figure 6
Figure 6
Physiology of the receptive-field surround. A: Flashing-spot stimulation of a transient ON-OFF RGC showing the position of three of the 10 spots relative to the ON (red) and OFF (black) dendritic arbors. B: Spike raster plots from the cell shown in A to 10 spots of 50–1,000-µm diameter. C: Area-response plots from seven cells to the same stimuli as B, error bars = s.e.m. D–F: Excitatory conductance, Ge ± s.e.m., averaged from 10 cells in response to a 100-µm spot (D), a 200-µm spot (E), and an 800-µm spot (F). G–I: Inhibitory conductance, Gi ± s.e.m., averaged from 10 cells in response to a 100-µm spot (G), a 200-µm spot (H), and an 800-µm spot (I).
Figure 7
Figure 7
Dendritic morphology of ON-OFF RGCs in the visual streak of the rabbit retina. The dendritic trees were reconstructed by tracing confocal projections of Neurobiotin-filled RGCs; the ON arbor is shown in red, and the OFF arbor is shown in black. The local edge detector, shown in black, stratifies at the border of the ON and OFF sublaminae. D, dorsal; V, ventral. Scale bar = 100 µm.
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