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. Author manuscript; available in PMC: 2014 Aug 3.
Published in final edited form as: Curr Biol. 2014 Jan 16;24(3):310–315. doi: 10.1016/j.cub.2013.12.020

Visual space is represented by non-matching topographies of distinct mouse retinal ganglion cell types

Adam Bleckert 1,2, Gregory W Schwartz 3, Maxwell H Turner 1,3, Fred Rieke 3,4, Rachel OL Wong 2
PMCID: PMC3990865  NIHMSID: NIHMS568246  PMID: 24440397

Summary

The distributions of neurons in sensory circuits display ordered spatial patterns arranged to enhance or encode specific regions or features of the external environment. Indeed, visual space is not sampled uniformly across the vertebrate retina. Retinal ganglion cell (RGC) density increases and dendritic arbor size decreases towards retinal locations with higher sampling frequency, such as the fovea in primates and area centralis in carnivores [1]. In these locations, higher acuity at the level of individual cells is obtained because the receptive field center of a RGC corresponds approximately to the spatial extent of its dendritic arbor [2, 3]. For most species, structurally and functionally distinct RGC types appear to have similar topographies; collectively scaling their cell densities and arbor sizes towards the same retina location [4]. Thus, visual space is represented across the retina in parallel by multiple distinct circuits [5]. In contrast, we find a population of mouse RGCs, known as alpha or alpha-like [6], that displays a nasal-to-temporal gradient in cell density, size and receptive fields, which facilitates enhanced visual sampling in frontal visual fields. The distribution of alpha-like RGCs contrasts with other known mouse RGC types, and suggests that unlike most mammals, RGC topographies in mice are arranged to sample space differentially.

Results and Discussion

Mouse ON alpha-like RGCs display a nasal to temporal gradient in cell density and dendritic arbor size

Alpha-like mouse RGCs segregate into three populations: ON-sustained (AON-S), OFF-transient (AOFF-T), and OFF-sustained (AOFF-S) [7–10]. Alpha RGCs are readily identified by labeling neurofilaments [11], and in mouse, the antibody SMI-32 directed against non-phosphorylated neurofilament heavy chain readily labels AON-S and AOFF-T alpha-like RGCs, but not AOFF-S (Figure 1A,B and Movie S1) [12, 13]. When we systematically mapped the distributions of AON-S RGCs labeled by SMI-32, we found a pronounced gradient in their density (>3 fold difference) increasing from nasal to temporal retina, peaking at a temporal-dorsal location (Figure 1A,B and S1). We then reconstructed the individual arbors of SMI-32 labeled AON-S RGCs using the Thy1-YFPH transgenic line [14], in which RGCs are sparsely labeled, and found that the increase in AON-S RGC density is paralleled by a reduction in dendritic arbor size (Figure 1C and S2). Quantification of the dendritic arbors revealed that the size of each AON-S RGC, represented by the diameter of a circle with an area equivalent to its arbor (see Experimental Procedures), scaled linearly across the nasal-temporal axis of the retina (Figure 1D), whereas no relationship existed between arbor size and retinal eccentricity from the optic nerve head (Figure 1E). Previously mouse RGC types have been believed to be uniformly distributed across the retina, and have largely been classified according to soma and dendritic arbor size, branching patterns and stratification level [9, 12, 15–19], unless a molecular-marker was available [13, 20–24]. Based on these criteria, the alpha-like RGCs in different retinal regions were likely classified as distinct cell types in previous studies (see Table S1).

Figure 1. Cell density and size of AON-S retinal ganglion cells form inverse gradients across the mouse retina.

Figure 1

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(A) Locations of AON-S RGCs (yellow dots) labeled by SMI-32 immunostaining (cyan) in a whole mount retina (left eye) from a P24 mouse (V, ventral, D, dorsal, N, nasal, T, temporal). (B) Maximum intensity projections of image stacks encompassing SMI-32 labeled RGC somata and primary dendrites (grey) within the boxed regions in (A). AON-S RGCs are identified by their relatively brighter cell bodies and dendrite labeling (yellow dots). (C) Sparse labeling of AON-S RGCs in Thy1-YFPH transgenic mice enables visualization of the complete dendritic arbors of individual SMI-32 RGCs (red dots in B). Arrowhead demarcates RGC axon. (D) Dendritic arbor sizes of AON-S RGCs represented by diameters of circles with areas equivalent to the arbor area (see Experimental Procedures) are plotted across nasal-temporal retina. Relationships between AON-S RGC size (circle diameter) and retinal eccentricity from the optic nerve head (ONH) (E), total dendritic length (F), soma size (G), mean segment length (H) and number of dendritic segments (I). (J) Number of Sholl intersections as a function of the distance from the soma for each cell, and (K) Sholl intersections after normalizing the curves according to dendritic arbor size. (n = 2 retinas, 27 RGCs). See also Figure S1 and S2, Table S1, and Movie S1.

Further quantification of AON-S RGCs indicated that their arbor size is proportional to total dendritic length, whereas soma size is uniform across cells (Figure 1F,G). AON-S arbor size also correlated with mean dendritic segment length, but not with the total number of dendritic segments (Figure 1H,I). To compare the branching patterns of AON-S RGCs across the retina, we quantified dendritic branch number as a function of distance from the soma by calculating the number of Sholl intersections (Figure 1J). We found that the Sholl curves of AON-S RGCs across retinal locations overlapped when normalized by their dendritic diameter size (Figure 1K; see Experimental Procedures). This suggests that AON-S RGCs simply scale up or down their dendritic arbors to increase or decrease their dendritic territory depending upon their position in the retina. These differences in size may be dictated by the local density of AON-S RGCs, because homotypic interactions are known to regulate the dendritic territories of other mouse retinal neurons [25–29]. Furthermore, manipulations to increase the total RGC density in cat retinas cause a decrease in alpha RGC size [30]. However, homotypic regulation may not be consistent across all retinal neurons in mice [31].

AON-S RGCs across the retina are arranged in mosaic distributions and have similar ON-sustained responses to light

To further confirm that the SMI-32 labeled AON-S RGCs represent variations of a single type of RGC, we performed two additional sets of experiments. First, we determined whether these cells exhibit a mosaic distribution, a feature delineating separate cell types in the retina. We mapped the distribution of AON-S RGCs in 1 mm2 regions of nasal and temporal retina and calculated their density recovery profile (Figure 2 and S1; see Experimental Procedures). Populations in both regions displayed a zone of exclusion indicated by a decreased cell density near a reference cell; such an exclusion zone is a hallmark of cells distributed in a mosaic pattern [32]. The effective radius of this exclusion and the nearest neighbor distances in nasal retina were greater than those in temporal retina (Figure 2B). Second, we measured the light responses of AON-S RGCs by recording whole-cell currents in response to brief steps of light from darkness (see Experimental Procedures). Cells in both temporal and nasal regions showed sustained excitatory and inhibitory currents in response to light onset, physiological hallmarks of AON-S RGCs [7, 10, 33]. The retinas were fixed after electrophysiology and the recorded cells were subsequently confirmed to be SMI-32 positive (n = 11 out of 11 cells, 5 T and 6 N). Furthermore, nearest neighbor distributions confirmed that recorded small-arbor cells were in temporal retina, whereas large-arbor cells were located in nasal retina (examples; Figure 2C,D). Our structural and functional analyses therefore together uncovered a single population of RGC in the mouse retina resembling the ON-alpha RGC populations in other species [6].

Figure 2. AON-S RGCs have mosaic distributions and characteristic ON sustained responses to light stimuli.

Figure 2

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(A) Example spatial distributions of AON-S RGCs (black dots), sampled from nasal (N) and temporal (T) retina. The density recovery profile (DRP) was calculated using a 200 μm radius (red circles). Nearest neighbor distances (grey lines) were calculated for every RGC within a region. (B) DRP plots of AON-S RGCs as a function of distance from the reference cell (red) compared to the DRP of cells with a random distribution (black). The effective radius of exclusion for nasal regions is greater than for temporal (grey vertical lines, N = 93.2, T = 46.5 μm, p < 0.0002), but the packing factor was not (T = 0.31, N = 0.36, p = 0.10). The average nearest neighbor distance is greater in nasal compared to temporal retina (N = 168.0, T = 88.4 μm, p < 0.0002). n = 8 retinas for all measures. (C) Left: An example AON-S RGC targeted for electrophysiological recording in nasal retina. Dendritic arbors were visualized upon cell-filling with Lucifer yellow (LY), and neighboring AON-S RGCs (red dots) were identified subsequently by SMI-32 labeling. Mean neighbor distances for the recorded cell are displayed as red in (B,right). Middle: Targeted AON-S RGCs showing co-labeling of LY and SMI-32. Right: Excitatory (red traces) and inhibitory (grey traces) currents show characteristic sustained responses to light stimuli (grey bar, 500 ms). (D) An example AON-S RGCs targeted in temporal retina show the same characteristic responses as in nasal retina. Data are shown as mean ± SEM. See also Figure S1.

Visual space in temporal retina has an enhanced sampling by AON-S RGCs, but not by their dominant presynaptic partners

Why might AON-S RGCs have an increased density in temporal retina? To gain insight, we first asked whether the dominant excitatory presynaptic partner of AON-S RGCs [34], the type 6 cone bipolar cell (T6 BC) also scales its axonal field proportionally to the AON-S RGCs dendritic arbor. Surprisingly, we found no change in the distribution of T6 BC axon sizes in nasal compared to temporal retina (Figure 3A). Thus, in this circuit, the presynaptic T6 BCs maintain a uniform sampling of visual space across the retina, whereas the postsynaptic AON-S RGCs bias their sampling towards temporal retina. This is in contrast to species with specialized areas of central vision, where bipolar and ganglion cells both scale towards areas of peak density [1, 35].

Figure 3. Increased density of AON-S RGCs in temporal retina results in an enhanced sampling of the visual field, which is not paralleled by their dominant presynaptic partner.

Figure 3

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(A) Axonal terminals of nasal (N) and temporal (T) located type 6 bipolar cells visualized by expression of tdTomato in the Grm6-tdTomato mouse (see Experimental Procedures). Their axonal territory sizes (area of the polygon) are plotted here for cells in nasal and temporal retina. (n = 4 retinas, 37 N and 34 T cells). (B) Plot of the diameter of AON-S RGC dendritic arbors against mean nearest neighbor distances. (C) Dendritic field coverage factor (CF) of AON-S RGCs in nasal and temporal retina (CFn = 3.9, CFt = 5.1). Coverage factor (colored) maps were calculated from maps of AON-S RGCs dendritic field overlap predicted from their neighbor distances (B, see Experimental Procedures). (D) Top: Example dendritic fields from AON-S RGCs targeted across the retina, whose receptive field diameters were mapped using sequential bars of light (see Experimental Procedures). Middle: Average excitatory current traces from example nasal (black) and temporal (grey) cells recorded in response to light stimuli at the indicated bar positions. Bottom: Response profiles were fit to the normalized charge transfers (dots) with Gaussian functions (smooth curves). (E) Dendritic diameters of AON-S RGCs were reconstructed from the recorded cells and plotted against their respective receptive field diameters (see Experimental Procedures) (n = 14 cells). Receptive fields of temporal cells (grey dots) are larger than their dendritic fields (p = 0.03), (dashed red line shows unity), but the two measures appear similar for nasal cells (black dots (p = 0.4) (See Experimental Procedures). (F) Receptive field CF of AON-S RGCs in nasal and temporal retina (CFn = 4.1, CFt = 8.8). Coverage factor maps were calculated for the same nasal and temporal regions in (C). Data are shown as mean ± SEM.

To quantify how the change in size and density of AON-S RGCs could affect sampling of the visual field, we first calculated their dendritic coverage factor (Figure 3B,C; see Experimental Procedures). In temporal retina, dendritic coverage of AON-S RGCs is 1.3× greater than in nasal retina (Figure 3D), i.e. any point in the retina is sampled, on average, by more AON-S RGCs in temporal versus nasal retina. We next compared this dendritic coverage to the functional coverage of AON-S RGCs by mapping the receptive field sizes for targeted AON-S RGCs across the retina. The receptive field size of AON-S RGCs does not parallel dendritic field size; temporal AON-S RGCs have greater receptive field size than their dendritic field size, whereas nasal AON-S RGC dendritic and receptive field sizes appear more similar (Figure 3E; see Experimental Procedures). This increase in receptive field size results in a further enhancement (2.2×) in coverage of the visual field by AON-S RGCs in temporal compared to nasal retina (Figure 3F). Thus, each AON-S RGC in temporal retina, not only encodes a smaller unit of visual space than in nasal retina, but also every point in space is sampled by a greater number of AON-S RGCs.

What function might a population of RGCs with enhanced visual sampling in temporal retina serve? In rodents, ipsilateral projecting RGCs that underlie binocular vision are located in temporal retina [37, 38], and alpha-like RGCs, are overrepresented, ~10% of RGCs in the ipsilateral projecting population, whereas they constitute only ~1% of the total RGC population [37, 39]. Furthermore, the location of peak density of AON-S RGCs is near the center of the rodent frontal visual fields [37, 38, 40, 41] (Figure 4A,B). The mouse retina has commonly been believed to have a relatively uniform distribution of cell types across the retina [15, 42], and a cell type with a temporal - nasal gradient similar to those found in animals with clear binocular vision [11, 43], is unexpected for mice. In addition to previous work showing alpha-like RGCs are adept at detecting fine-scale spatial patterns [34], processing chromatic information [44], and possibly displaying intrinsic photosensitivity [45, 46], our work places AON-S RGCs in this unique location specialized for encoding frontal vision.

Figure 4. Sampling of frontal visual space is enhanced in AON-S RGC distributions, which contrast with the distributions of known RGC types.

Figure 4

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(A) Azimuthal equilateral projections of retina space for AON-S RGC distributions from right (red) and left (blue) eyes shown in Figure 1 and S1, reconstructed and plotted using the retistruct package [41]. Isodensity lines demarcate 5, 25, 50, 75, and 95% contours of the peak density located at the asterisk (~180 cells / mm2). Cyan lines delineate computed sutures of the original relief cuts made for flat mount preparation. (B) Sinusoidal projection of mouse visual space for AON-S RGC distributions from retinas in (A) (see Experimental Procedures). Red outline represents the edge of the right retina; blue outline represents the edge of the left retina. N - nasal, D - dorsal, V - ventral, T - temporal, indicate the projection of the corresponding pole of the retina. Grey circle represents the position of the optic nerve head. Note the peak densities for right and left retinas (red and blue asterisks) and increased density (75% and 50% isodensity lines) are biased towards the vertical midline (0) corresponding to rostral frontal visual fields of mice. (C) The density of the total RGC population peaks at a location just nasal and ventral of the optic nerve head (black asterisk) (schematized from [51] see also [42, 52]). (D) In contrast, we show here that AON-S and likely AOFF-S RGCs have peak densities in the temporal-dorsal retina, whereas AOFF-T RGCs are relatively more uniformly distributed across the retina. (E) Furthermore, the distributions of previously characterized RGCs show varied or flat distributions. The density colormaps in (C and E) are schematics based on previously reported RGC densities, and changes in dendritic arbor sizes (see Experimental Procedures). Density colormaps in (D) are schematics based on the distributions of AON-S and AOFF-T RGCs shown in Figure S1, and predicted from AOFF-S dendritic arbor sizes illustrated in Figure S2. See also Figure S2.

The distributions of ON and OFF alpha-like RGCs differ from those of other known mouse RGCs and suggest an independent sampling of visual space by distinct RGC types

We next asked if the two known OFF alpha-like RGCs found in mouse also display similar distributions to ON alpha-like RGCs [7, 10]. We observed one OFF population of RGCs that varied in dendritic arbor size between nasal and temporal retina, in a manner paralleling AON-S RGCs. The dendritic stratification and morphology of these cells are characteristic of AOFF-S RGCs [7, 10] (Figure S2). This suggests that AOFF-S RGCs are also organized for enhanced sampling of visual space in temporal retina. Conversely, we found that the distribution of SMI-32 labeled AOFF-T RGCs varied much less across the retina (Figure S1) in contrast to most mammals [6], although similar to other rodents [36], which may be accompanied by some change in dendritic field size [13, 47]. Taken together, our current mapping of the topographic distributions of cell densities and dendritic arbor sizes of alpha-like RGCs, strongly contrasts with that of known mouse RGCs (Figure 4C–D). Previous studies demonstrated a peak in W3 RGCs (presumed local edge detector) in ventral retina [22], an increased density of M1 and M2 RGCs (intrinsically photosensitive) in dorsal retina [23], and relatively flatter distributions for direction-selective RGC types, such as JAM-B [19, 20], DRD4 [21, 48], BD RGCs [19, 21] and Hoxd10 [24]. This raises a striking difference between the mouse retina and that of other mammals, whereby diverse RGC types in the mouse appear to exhibit distinct topographies and have adopted a strategy to customize the distributions of each RGC type to sample the visual environment.

Conclusions

In summary, our findings suggest that sampling of the visual scene by AON-S RGCs is modulated across the retina by a non-uniform topographic distribution of their densities and receptive field sizes, distinct from the topographic patterns of other known mouse RGC types. The diversity of RGC distributions in the mouse retina suggests that visual space is not sampled uniformly by parallel processing circuits across the retina in mice, but instead distinct populations of RGCs may be organized in separate topographies to encode specific visual features or regions [20, 22, 48–50].

Supplementary Material

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Highlights.

  1. A functionally distinct RGC type has a density and size gradient across the retina.

  2. Gradient allows for enhanced sampling of frontal visual space.

  3. Peak density in temporal retina contrasts with distributions of known RGC types.

  4. Diverse topographies of RGC types suggest visual space is sampled differentially.

Acknowledgements

Funded by NIH EY10699 (R.O.L.W.), NIH Developmental Biology Training Grant T32HD007183 and Neurobiology and Behavior Training Grant 5 T32 GM07108 (A.B.), NEI Vision Training Grant EY07031 (M.H.T.), Howard Hughes Medical Institute (F.R.) and Helen Hay Whitney Foundation Fellowship (G.W.S).

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