Skip to main page content
U.S. flag

An official website of the United States government

Dot gov

The .gov means it’s official.
Federal government websites often end in .gov or .mil. Before sharing sensitive information, make sure you’re on a federal government site.

Https

The site is secure.
The https:// ensures that you are connecting to the official website and that any information you provide is encrypted and transmitted securely.

Access keys NCBI Homepage MyNCBI Homepage Main Content Main Navigation
. 2009 Dec 1;517(4):459-80.
doi: 10.1002/cne.22145.

Morphology of retinal ganglion cells in the ferret (Mustela putorius furo)

Tomoki Isayama  1 , Brendan J O'Brien, Irma Ugalde, Jay F Muller, Aaron Frenz, Vikas Aurora, William Tsiaras, David M Berson
Affiliations

Morphology of retinal ganglion cells in the ferret (Mustela putorius furo)

Tomoki Isayama et al. J Comp Neurol. .

Abstract

The ferret is the premiere mammalian model of retinal and visual system development, but the spectrum and properties of its retinal ganglion cells are less well understood than in another member of the Carnivora, the domestic cat. Here, we have extensively surveyed the dendritic architecture of ferret ganglion cells and report that the classification scheme previously developed for cat ganglion cells can be applied with few modifications to the ferret retina. We confirm the presence of alpha and beta cells in ferret retina, which are very similar to those in cat retina. Both cell types exhibited an increase in dendritic field size with distance from the area centralis (eccentricity) and with distance from the visual streak. Both alpha and beta cell populations existed as two subtypes whose dendrites stratified mainly in sublamina a or b of the inner plexiform layer. Six additional morphological types of ganglion cells were identified: four monostratified cell types (delta, epsilon, zeta, and eta) and two bistratified types (theta and iota). These types closely resembled their counterparts in the cat in terms of form, relative field size, and stratification. Our data indicate that, among carnivore species, the retinal ganglion cells resemble one another closely and that the ferret is a useful model for studies of the ontogenetic differentiation of ganglion cell types.

PubMed Disclaimer

Figures

Figure 1
Figure 1
Camera lucida drawings of representative alpha cells of the ferret retina stained by intracellular injection. Both cells had filled axons but these have been omitted for clarity. Distance from the area centralis, or eccentricity (“e”), and distance from the axis of the visual streak (“s”) as follows. A): e = +0.7 mm; s = +0.7 mm; B) e = +5.7 mm; s = +1.4 mm. Negative values of e indicate locations in temporal hemiretina; negative values of s indicate locations in inferior retina. Scale bar = 100 μm.
Figure 2
Figure 2
Camera lucida drawings of beta ganglion cells of the ferret retina. Cells A-C all lay within the nasal visual streak but at progressively greater eccentricities, from left to right. Cells D-F all lay outside the visual streak, with increasing eccentricity and distance from the visual streak from left to right. Axons omitted for clarity. Cell locations as follows (conventions as for Fig. 1): A: e = +0.1, s = +0.1; B: e = +3.3, s = +0.0; C: e = +6.9, s = +0.1; D: e = −1.6, s = −0.4; E: e = +3.0, s = +3.0; F: e = +5.8, s = +4.3. Scale bar = 100 μm.
Figure 3
Figure 3
Topographic dependence of dendritic field size for ferret alpha and beta ganglion cells. A,B: Dependence of dendritic field diameter on (A) eccentricity (i.e. distance from the center of the area centralis) and (B) distance from the axis of the visual streak. No distinction is made in A, nor in B between superior and inferior hemiretinas. Lines indicate linear least-squares fits to the data. Regression constants shown in Table 2. C,D: Plots illustrating relative contribution of eccentricity and distance from the visual streak to dendritic field size of alpha (C) and beta cells (D). Each symbol type indicates a range of distance from the axis of the visual streak, as indicated in the key. Negative eccentricities lie in the temporal hemiretina.
Figure 4
Figure 4
Depths of dendritic stratification for ferret alpha and beta ganglion cells. A - D. Camera lucida drawings of representative radial sections. A: OFF alpha; B: ON alpha; C: OFF beta; D: ON beta. Black somata and processes belong to the injected cell; the soma for the cell in A lies out of the plane of the section illustrated. Shaded profiles represent other cell bodies of the ganglion cell and inner nuclear layers. Scale bar: 20 μm. E-F. Histograms of relative frequency of dendritic processes at depths in the inner plexiform layer (IPL), expressed as a percentage of its total thickness. 0% corresponds to the distal border and 100% to the proximal border of the IPL. For both alpha cells (E) and beta cells (F), stippled bars indicate dendrites of ON type, black bars those of OFF type. Data drawn from one ON alpha, one OFF alpha, three ON beta and three OFF beta cells. G, H: Relative depths of stratification of alpha and beta cells as revealed by quantitative through-focus analysis in a single retinal wholemount of cells with overlapping dendritic profiles. For each panel, a single alpha cell was selected as a reference cell. At each point of intersection between the dendritic profiles of the reference cell and another cell with an overlapping field, the difference in depth between the two dendrites was measured. The histograms plot the distribution of these depth differences. G: Comparisons between a reference ON alpha cell (horizontal line) and two overlapping cells, an OFF alpha (black bars) and an ON beta cell (stippled bars). H: Comparisons between a reference OFF alpha cell and two overlapping beta cells, one OFF (black bars) and one ON (stippled bars). Cell locations (conventions as for Fig. 1) G: e = +4.4, s = −3.4; H: e = +4.7, s = +−3.4.
Figure 5
Figure 5
Photomicrographs of representative ferret non-alpha/non-beta ganglion cells. A. Low power micrograph of a delta cell. Cell location (conventions as for Fig. 1): e = +0.6 mm, s = +0.6 mm. B. Low power micrograph of a epsilon cell: e = +4.2 mm, s = −1.7 mm. C. Low power micrograph of a zeta cell: e = +5.2 mm, s = +1.5 mm. D. Low power micrograph of an eta cell: e = +3.0 mm, s = +2.7 mm. E. Low power micrograph of a theta cell: e = +5.1 mm, s = −4.6 mm. F-H. An iota cell, shown at low magnification (F) and at higher magnification at planes of focus corresponding to the proximal (G) and distal (H) dendritic arbors. Cell location: e = 5.8 mm, s = −0.6 mm. All scale bars = 50 μm.
Figure 6
Figure 6
Camera lucida drawings of representative delta ganglion cells of the ferret (A, B) and cat (C) retina. Asterisk in this and subsequent figures indicates examples from the cat. Axons omitted for clarity. Cell locations (conventions as for Fig. 1): A: e = +5.4 mm, s = +5.2 mm; B: e = −0.9 mm, s = −0.6 mm; C: e = +3.5 mm, s = +1.8 mm. Scale bar = 100 μm.
Figure 7
Figure 7
Camera lucida drawings of epsilon ganglion cells of the ferret (A,C) and cat (B) retina. Axons omitted for clarity. Cell locations (conventions as for Fig. 1). A: e = +4.9 mm, s = +1.8 mm; B: e = +2.4 mm; C: e = +2.2 mm; s = +2.2 mm. Scale bar = 100 μm.
Figure 8
Figure 8
Camera lucida drawings of zeta ganglion cells of the ferret (A,B) and cat (C) retina. Axons omitted for clarity. Cell locations (conventions as for Fig. 1): A: e = +4.1 mm; s = +1.0 mm; B: e = +6.1 mm, s = +0.3 mm; C: e = +6.4 mm; s = −0.2 mm. Scale bar = 100 μm.
Figure 9
Figure 9
Camera lucida drawings of eta ganglion cells of the ferret (A,B) and cat (C) retina. Axons omitted for clarity. Cell locations (conventions as for Fig. 1): A: e = +4.8 mm, s = +1.8 mm; B: e = +3.9 mm; s = +2.9 mm; C: e = +6.0 mm; s = +0.6 mm. Scale bar = 100 μm.
Figure 10
Figure 10
Camera lucida drawings of theta ganglion cells of ferret (A,B) and cat (C) retina. Axons omitted for clarity. Cell locations (conventions as for Fig. 1): A: e = +1.3 mm, s = +1.3 mm; B: e = +3.5 mm, s = +3.3 mm; C: e = +1.5 mm, s = +1.3 mm. Scale bar = 100 μm.
Figure 11
Figure 11
Camera lucida drawings of iota ganglion cells of the ferret (A,B) and cat (C). Inner (1) and outer (2) arbors are displayed separately at reduced magnification for the cell in B. Axons omitted for clarity. Cell locations (conventions as for Fig. 1): A: e = +6.1 mm, s = +0.2 mm; B: e = +3.5 mm, s = +3.2 mm; C: e = +4.0 mm, s = +3.8 mm. Scale bar = 100 μm.
Figure 12
Figure 12
Comparisons of dendritic stratification among ganglion cell types of the ferret retina. A: Schematic radial section of the inner plexiform layer (IPL) summarizing the patterns of dendritic stratification inferred for each type from the data in Fig. 4, and other through-focus observations as described in text. S1-S5: strata 1 - 5 of the IPL. Heavy dashed line marks the boundary between the OFF sublamina (a) and the ON sublamina (b). B: Summary of data on relative depth of stratification of various types obtained by through-focus inspection of overlapping dendritic arbors. Symbols in each cell of the matrix indicate whether the ganglion cell type listed to the left (row heading) stratifies proximal (formula image), at the same depth (formula image), or distal (formula image) to the type listed above (column heading). Numbers indicate the number of overlapping arbors studied. For the bistratified types (theta and iota) the inner (ON) and outer (OFF) arbors are considered separately.
Figure 13
Figure 13
Comparison of dendritic field size among six non-alpha, non-beta ganglion cell types of the ferret retina. A: Dendritic field diameters of each type as a function of distance from the axis of the visual streak. Negative eccentricities correspond to locations in the temporal hemiretina. Statistics for each type are shown in Table 1. B: Comparison among these types and with alpha and beta cells of the ferret retina. Each outline represents the envelope of the field-size distribution of a single type, drawn from data shown in Figs. 3B and 13A. No distinction has been made between nasal and temporal hemiretinas.
Figure 14
Figure 14
Comparison of soma size among ferret ganglion cell types. Statistics for each type appear in Table 1.
See this image and copyright information in PMC

Similar articles

See all similar articles

Cited by

References

    1. Amthor FR, Jackson CA. Staining of retinal neurons in the isolated eyecup by extracellular horseradish peroxidase injection. Vision Res. 1986;26(2):269–274. - PubMed
    1. Amthor FR, Oyster CW, Takahashi ES. Morphology of on-off direction-selective ganglion cells in the rabbit retina. Brain Res. 1984;298(1):187–190. - PubMed
    1. Amthor FR, Takahashi ES, Oyster CW. Morphologies of rabbit retinal ganglion cells with complex receptive fields. J Comp Neurol. 1989;280(1):97–121. - PubMed
    1. Berson DM, Isayama T, O’Brien BJ, Pu M. The kappa ganglion cell type of cat and ferret retina. Invest Ophthalmol & Visual Sci. 1999a;40:S813.
    1. Berson DM, Isayama T, Pu M. Morphology of presumed ON-OFF direction selective ganglion cell of cat retina. Soc Neurosci Abstr. 1997;23:730.

Publication types