Anatomy of the Retina of the Mink (Mustela visor?) MARK WM. DUHIN AND LINDA TURNER Molecular, Cellular and Decelopmental Biology, University of Colorado, Boulder, Colorado 80309

ABSTRACT The retina of the normal pigmented mink has been studied by light and electron microscopy. This retina resembles the typical vertebrate retina in its patterns of lamination and synaptic interconnectivity. Rod and cone outer segments and receptor spherule and pedicle endings are found. At least two different types of horizontal cell processes are seen with the electron microscope, suggestive of rabbit A and B types. Ribbon and conventional synapses are found in both plexiform layers; conventional synapses are also present in the inner nuclear layer. Quantitative studies of the inner plexiform layer revealed amacrine:bipolar synapse ratios (3.3:l)similar to those of the cat and monkey. Other quantitative parameters also resembled those previously reported for species with retinas that predominantly contain concentric-type receptive fields.

The visual system of the mink has recently come under study. Sanderson ('74) characterized the lateral geniculate nucleus (LGN) of this animal in a comparative study of the LGN of carnivores. He showed that the basic pattern of lamination and innervation of the mink LGN is similar to that of the cat (Guillery, '70)and other carnivores. Although there was a partial duplication of layers A and A l , the differences in detail between mink and cat that were noted did not obscure the fundamental similarities. In another study (Sanderson et al., '74) it was shown that mink varieties with genes that reduce retinal pigmentation have abnormal retino-geniculate projections. The nature of the abnormality was found to be similar to that of the Siamese cat (Guillery, '69; Cuillery and Kaas, '71; Hubel and Wiesel, '71); axons of temporal ganglion cells cross in the optic chiasm on their way to the LGN instead of staying ipsilateral (uncrossed), as is normal. The study further showed that different mink varieties which are genetically well-defined (for breeding purposes) have varying amounts of such abnormal retino-geniculate projections. The authors suggested that this system might provide a means to test hypotheses concerning why the abnorJ. COMP. NEUR., 173: 275-288.

mal LGN segments found in some Siamese cats are suppressed in the cortex, but in others result in an unusual extra cortical representation of the visual field (Hubel and Wiesel, '71; Guillery and Kaas, '73; Guillery and Casagrande, '76).The authors anticipated that future electrophysiological studies would be carried out on the mink to explore this point and, in fact, pilot experiments have been done (Sanderson, personal communication). In light of the above results and the probable electrophysiological work that might follow, it seemed of interest to know about the anatomy of the retina of the mink. Such a study would provide a broader basis than presently available for future work on the mink visual system. This was the impetus for the present investigation. MATERIALS AND METHODS

Both eyes were taken from a normally pigmented (dark-brown) mink for electron microscopy. They were treated according to the procedures used in the previous quantitative study with which they will be compared (Dubin, '70). Each was hemisected just forward of the ora serruta, had the lens removed and vitreous drained, and

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was notched to facilitate later orientation. The eyecups were then fixed in veronalacetate buffered, 2% Os04,pH 7.9, for 20 minutes at about 0°C and for a further hour at about 20°C. The tissue was then dehydrated through a graded ethanol series, passed through propylene oxide and embedded in an Epon-Araldite resin mixture. Each embedded eye was sawed into two halves along a line near or through the nerve head. The right e y e was cut on the nasal-temporal axis, the left eye on the superior-inferior axis. Blocks were then shaped so that single, one micron thick sections could be cut extending from ora serrata to ora serrata on each of the above axes. These sections were stained with toluidine blue and were used to make certain of the light microscopic measurements described below. (No attempt was made to correct for possible shrinkage.) Thin sections (gold) were then cut at identified positions along these two axes. All sections were mounted on bar grids and stained for one to three minutes with a saturated solution of uranyl acetate in absolute ethanol and then for five to ten minutes with lead citrate (Reynolds, '63). Seven EM photomontages of the inner plexiform layer (IPL), at various places on the retina, were made and studied by previously described methods (Dubin, '70). For each montage about 12 overlapping negatives (magnification 5,000 x ) were printed to give a final magnification of about 20,000 X . It was found that exact matching of the overlapping prints was greatly facilitated by the use of plastic coated photographic paper (Kodak type RC) which does not shrink or stretch during processing. The light microscopic material available also included paraffin sections (from a number of different minks) and a methylene blue stained retinal wholemount (all kindly provided by Doctors R. W. Guillery and K. J. Sanderson). RESULTS

Light microscopy General considerations The mink retina resembles all other ver-

tebrate retinas when observed in cross section; photoreceptors, three nuclear layers and two plexiform layers are found (fig. l j . Examination of numerous thick sections with the light microscope, and low power EM studies of thin sections showed nothing obviously unusual in regards to cell body type or placement. Thus it seems reasonable to conclude that the standard retinal cell types are present in their normal positions. The retina extends approximately 5.25 to 5.5 mm from nerve head to ora serrata in the superior, temporal and inferior directions but extends about 6.5 mm in the nasal direction. In this regard, it is worth noting that the mink has laterally placed eyes and, most likely, a significant monocular field (Sanderson, '74) subserved by the nasal portion of the retina. The thickness of the various retinal layers was measured at 250 p m intervals along the na5al-temporal and superior-inferior axes. In all four directions, from the nerve head to a point half-way between the optic disc and the retinal margin, each layer maintained an approximately uniform thickness similar to that shown in figure 1. The peripheral retina then grew gradually thinner as the oru serrutu was approached. Ganglion cell density distributions, also measured along the same two axes showed similar central uniformity and peripheral diminution, with the exception of a higher relative density found in the superior-temporal region. At all positions, the ganglion cell layer was usually one cell thick.

Specijc considerations The photoreceptor layer is made up of both rods and cones. The thin arrow in figure 1 indicates a cone, and numerous others can be seen. Although no exhaustive quantitative analysis was made, from a study of outer segments seen in light microscopy and pedicles seen in EM, it was clear that relatively more cones per unit area are found in the central regions of the retina than in the peripheral regions. Related to this is the finding, noted above, that there is a region in the superior-temporal quadrant of the retina, found to be

THE RETINA OF THE MINK

Fig. 1 Light micrograph of the central nasal region of the retina. Normal retinal layering is evident. Both rods and cones can he observed in the phatoreceptor layer at top. The thin arrow indicates a cone. The thick arrow in the outer plexiform layer indicates a large horizontal cell process. Scale mark, 20 pin.

about 2.5 mm from the disc (in the whole mount), that has a relatively high ganglion cell density as compared to the rest of the retina. This is probably an area centralis. No foveal pit was seen, although a number of paraffin thick section series through entire eyes were examined. A number of blood vessels cut in section can be seen in figure 1. Such vessels are found at all retinal levels from the outer plexiform layer to the inner limiting membrane. Finally, although not shown in the figure, the mink eye has a colored reflective tapetum behind the retina.

Descriptive electron microscopy All major synaptic patterns seen in other vertebrate retinas (Dowling, '70; Stell, '72; Dubin, '74) are found in the mink retina. (The papers referenced should be consulted for the specific points concerning

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other species mentioned below). At the level of each plexiform layer both ribbon and conventional synapses are present. NO extensive serial reconstructions were carried out, therefore association of certain synaptic types with specific cell types is mainly by homology with previous work on other vertebrate retinas. However, an occasional tracing of each major type of synapse reported was made back to a cell body in the position expected from the tentative synaptic attribution. Further, in no case was a ribbon synapse and a conventional synapse found pre-synaptically in the same cell or process in a single section, or short series of sections. To summarize, the following is asserted: outer plexiform layer (0PL)-photoreceptors make ribbon synapses, horizontal cells make conventional synapses; inner plexiform layer-bipolar cells make ribbon synapses, amacrine cells make conventional synapses. Osmium fixation of the limited material available was used in this study so that the quantitative work reported below would be directly comparable with previous work. Therefore, no statements can be made concerning gap junctions or other specialized membrane junctions or cell associations that would be preserved only by glutaraldehyde fixation.

Outer plexiform layer Two basic types of photoreceptor synaptic terminals are seen. These resemble the rod spherule and cone pedicle previously described for other species (Dowling, '70). Figure 2 shows a typical spherule ending. The numerous post-synaptic processes are found deep in a single invagination and are associated with a single synaptic ribbon complex. Vesicles of the size of synaptic vesicles are sometimes seen in certain of the post-synaptic elements, but no conventional synapses were found within an invaginated region. The post-synaptic processes are generally not as orderly in their arrangement as is sometimes found in other species (for example, Dubin, '74: fig. 4). Figure 3 presents a common variant of the spherule pattern in which the synaptic ribbon and invagination are found ex-

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MARK W M . DUHlN AND LINDA TURNER

tremely close to the nucleus of the photoreceptor cell. A bell-shaped pedicle ending is illustrated in figure 4. The invaginated postsynaptic elements typically do not extend deeply into the pedicle. Numerous ribbon complexes are seen in a single section, two ribbons being clearly evident in the figure. A number of processes can be seen to have specialized membranes where they are in contact with pedicle base and it is likely that serial reconstructions of glutaraldehyde fixed material would reveal the complex pedicle-process associations seen in other species. Although small vesicles are seen in numerous of the post-synaptic processes, no conventional synapses were found in regions immediately adjacent to the base of a pedicle. Figures 5 and 6 illustrate other synaptic arrangements, as well as horizontal cell process morphology within the OPL. It can be seen that although osmium fixation was used, making identification difficult, both neurofilaments and some neurotubules are preserved. In figure 6, especially, a large process containing neurotubules (star) and rocess containing neurofilaments a(asterisk large are evident. The latter also contains small circular profiles that may well be neurotubules cut in cross-section (as does the presynaptic terminal in fig. 5a). It has been shown in other species that such large OPL processes are derived from horizontal cells (Dowling et al., '66; Fisher and Boycott, '74) and there is no reason to question that this is the case here as well. Fisher and Boycott ('74) have suggested that neurofilament-containing horizontal cell processes seen in EM correspond to processes of A type (axonless) horizontal cells seen in Golgi studies, and that processes devoid of' neurofilaments correspond to processes of B type horizontal cells (Dowling et al., '66).Figure 6 provides evidence which suggests that a similar division into two morphologically different types of horizontal cells may apply in the case of the mink retina. Fisher and Boycott further propose that in the rabbit, and possibly in the cat, the A type horizontal cells are

P

presynaptic at OPL conventional synapses. The large presynaptic profile in figure 5a contains some material that can be interpreted as filaments cut obliquely or, in other cases, in cross-section. This suggests that at least some OPL conventional synapses in the mink follow the pattern seen in the rabbit, with A type horizontal cells being presynaptic. However, the presynaptic elements in figures 5b and 6, typical of those usually seen in this retina, are small and cannot be identified as to cell type. While these may be processes of horizontal cells, it is also possible that they could be the terminations of interplexiform type amacrine cells (Dowling and Ehinger, '75; Boycott et al., '75). Similarly, there is not enough evidence to conclusively determine the identity of the postsynaptic processes seen at OPL conventional synapses. If it were to become important to know more about the cells involved in these synapses, further work involving serial reconstructions or drug marker studies (Dowling and Ehinger, '75) would be needed.

Inner pbexiform layer Long, tubular appearing axons running distal-proximal through this layer often end in ribbon containing bag-like endings and are easily identified as bipolar cell axons. Such large endings are most prominent at the IPL-ganglion cell layer boundary, but are generally not as conspicuous as in other species. Large pieces of ganglion cell dendrites are distinguished by the presence of smooth ER and some ribosomes, coupled with the complete absence of synaptic vesicles. Occasional cell bodies displaced into the middle of the IPL are seen. Typical IPL conventional synapses are shown in figure 7, in which two amacrine cell processes and a post-synaptic ganglion cell dendrite are involved in a serial synapse. In general, the more complex synaptic serial configurations such as those described in the frog retina (Dowling, '68) are rarely seen in the mink retina. Figure 8 shows a conventional synapse in which the post-synaptic element is a cell body that

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THE RETINA OF THE MINK TABLE 1 Ratio Ainacrine (runventiunal) synapaes

amacrins: bipolar synapses

% arnacrine synapses in srrial configuration

Area p d

30 40

151 154 I27 117 87 115

2.7:l 3.5:1 4.1:l 4.3:1 2.9:l 2.9:1

7.3 2.6 3.1 3.4 9.2 3.5

1,635 1,470 1,510 1,580 1.370 1,505

17 35

64 117

3.8:1 3.3:1

6.1 4.8

1,765 1,548

Bipolar (ribbon) synapses

1 2 3 4 5 6 7

Temporal Temporal Temporal Nasal Inferior Superior Periphery nasal Average

56 44 31

27

was in the middle stratum of the inner nuclear layer (INL). Two other similar synapses were seen in sections of other retinal regions. The pre-synaptic process was usually oriented so as to suggest that it originated in the IPL, but this is not certain without serial sections. Such synapses involving a cell process, presumably some distance from its cell body, and an INL soma have not commonly been described in other species although INL conventional synapses have been reported (Fisher, '72; Wong-Riley, '74). Ribbon synapse configurations are shown in figures 9 through 11. In general, ribbons were always associated with two post-synaptic elements in the well-known dyad configuration, with all possible combinations of post-synaptic processes found. The dyad configuration was the usual one seen in single sections; no attempt was made to explore its possible further complexity by serial reconstructions (Allen, '69; Witkovsky and Stell, '73;Wong-Riley, '74). Bipolar cell ribbon synapses were seen at all levels of the IPL with the ribbons in small endings such as those shown in the figures, in larger endings, and en passent in bipolar cell axons.

Quuntitative electron microscopy of the IPL Seven separate EM photomontages each covering a region of about 1,500 pm2 were made of the IPL. Each extended from the ONL-IPL border to the IPL-ganglion cell layer (GCL) border. On each, all ribbon

and conventional synapses were identified, counted and measured using criteria and methods previously described (Dubin, '70). The results are presented in tables 1 and 2. Three of the montages were made of the central-temporal retina, 2.5 mm from the nerve head along the horizontal plane through the nerve head, and one each at the same distance from the nerve head in the nasal, superior and inferior regions of the retina. One montage was made of thin peripheral nasal retina, at a point 0.5 mm from the ora serratu. Montages 1 and 2 were made from almost contiguous areas in order to exhibit the variability of the method in this retina. Montage number 3 was intentionally made of an area that fully included a displaced soma in the middle of the IPL. The immediate region around the soma, encompassed by the montage, contained numerous large profiles, possibly associated with the soma, and was thus somewhat atypical as compared to all of the other montages. Table 1 presents primary data of the study; the actual number of each synaptic type counted, the percentage of serial conventional synapses and the area of each montage is given. The primary derivative parameter of the study, the ratio of amacrine cell synapses to bipolar cell synapses (A:B ratio), is indicated as well. Note that the average values shown are representative of the entire set of montages and that none of the A:R ratios differ significantly from any of the others. That is, no regional differences across this retina were

MARK WM. DUBIN AND LINDA TURNER

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TABLE 2 Uncorrected no.1p.I

1 2 3 4 5 6 7

Temporal Temporal ’Temporal Nasal Inferior Superior Periphery nasal

Ribbon synapses

Conven. synapses

0.43 0.37 0.26 0.21 0.27 0.33

0.12

Corrected

no.11~~ Total

Total

synapses

Ribbon synauses

Conven. svnnuses

svnawes

1.15 1.31 1.05 0.92 0.79 0.96

1.58 1.68 1.31 1.13 1.06 1.29

0.19

0.17 0.12 0.11 0.12 0.16

0.40 0.45 0.36 0.30 0.29 0.33

0.59 0.62 0.48 0.41 0.41 0.49

0.45

0.57

0.06

0.16

0.22

found in terms of the A:B ratio. All possible pair-wise chi-square tests of the actual counts failed to show any significant differences between individual montages even at the P=O.O5 level. The serial synapse percentages represent four to eight synapserelated processes on the individual montages and it is not felt that significant differences are reflected in the results shown. Attention is called to the fact that the average A:B ratio is 3.3:l and the average serial synapse percentage is 4.8%. These figures will be discussed later. Counts such as those in table 1 must be corrected for the effect that the size of a synapse has on the probability of seeing that synapse in a given thin section. This problem is addressed in simple form by Abercrombie (’46) and is discussed at length by Dubin (’70),who presents a modified-Abercrombie correction for dealing with the particular situation found in the retina. This correction was applied to the present data. Size distribution histograms of synapse size, (comparable to those in figs. 13 and 14 of the previous study, Dubin, ’70) were made for both the ribbon and conventional synapses of every montage. The results were very similar and directly comparable to those of the previous work. This is important in that it validates the further calculations made, as well as the comparisons made with the previous results. The corrected size of the synapses found in the present seven montages ranged from 1,300-1,750A for the ribbon synapses and 2,400-2,725A for the conventional synapses. The corrected A:B ratios ranged from 2.0 to 3.0 with an average of

2.5. No significant differences between the individual montages were uncovered by the correction technique. The volume density of the synapses seen on the montages is presented in table 2. The thickness of the gold sections was taken as 800 A, to convert to cubic microns. The results of expressing the raw counts in this manner are shown in the columns headed “Uncorrected,” while the results after application of the modified-Abercrombie correction are presented in the columns headed “Corrected.” The synaptic density, and especially the conventional synapse density, appears to be slightly higher in the temporal portion of the retina than the other regions. This is even more evident if montage 3, which contained the displaced soma, is discounted. It should be recalled that the temporal region montages were taken at the edge of the presumptive area centralis. (The potential differences suggested by the data would require very extensive studies to yield counts that could show statistically a real difference of the magnitude noted.) The densities found in temporal montage number 3 are somewhat lower than the other two montages from the same region, but neither these figures nor those of table 1 show any radical departure from the rest for this atypical region which contained the misplaced cell body. Finally, the synaptic densities in the thinner peripheral region are about half those found in the central areas. DISCUSSION

The goal of this work was to make a limited study of the general anatomy of the

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THE RETINA OF THE MINK

mink retina, and a comparative study of the IPL in terms that could be related to previous work on other species. Overall, it was found that the mink has a typical retina that closely resembles the cat retina both quantitatively and qualitatively. It has previously been shown that vertebrate retinas can be classified into two distinct groups based upon quantitative studies of the complexity of their amacrine cell synaptic interconnections (Dowling, '68; Dubin, '70). Further, these two anatomically derived groups correspond very well to similar groupings based upon physiological, receptive field properties of their ganglion celIs. Species in group I (cat, monkey, [human], rat) have a low ratio of amacrine cell synapses to bipolar cell synapses and also have ganglion cells that are predominantly of the concentric receptive field type. Group I1 species (rabbit, ground squirrel, pigeon, frog) have a higher proportion of amacrine cell synapses, and numerous non-concentric type receptive fields of a complex nature-such as directionally-selective receptive fields. A causal relationship between the IPL synaptic anatomy and ganglion cell receptive field physiology has been suggested (Dubin, '70). Further support for this idea is provided by the recent work of Wyatt and Daw ('76). They showed that ganglion cell properties such as directional selectivity and local edge detection, in the rabbit, could be disrupted or degraded by the use of antagonists of neurotransmitters known to be present in amacrine cells. Quantitatively, the mink retina resembles the least retinally complex, group I animals. As noted, the receptive fields of those animals, determined electrophysiologically, are predominantly the concentric, center-surround, antagonistic type. Thus, we predict that the receptive fields of the mink ganglion cells are mainly the concentric type, based on the quantitative (anatomic) similarity at the IPL level of the mink and the group I retinas. Specifically, the average A:B ratio of 3.3:l in the mink retina compares well with the group I ranee of values of 1.7:l to 3.3:l and is c l e k y below the average group I1 values

of 6 : l to 9:1 (Dubin, '70). (The same can be said of the corrected A:R ratio values.) The average percentage of amacrine cell synapses in serial configuration of 4.8% in the mink compares well with the group I range of 2 4 % as opposed to the group I1 values of 10-15%. The synaptic density values presented in table 2 (periphery excluded) agree closely with those of the previous study both uncorrected and corrected. Concentrating on the latter, the ribbon synapse density range of the mink, 0.11-0.19 per pm3, is comparable to the range 0.07-0.16 found for similar retinal regions of other retinas. This agreement serves to strengthen the idea that ribbon synapse density is relatively constant in all higher vertebrates. Only in fish (Witkovsky and Dowling, '69) and Necturus (Dowling and Werblin, '69), which have retinas with extremely large cell processes, is ribbon density different (lower) from that found in all other animals studied. The conventional synapse density range in the mink of 0.29-0.45pm3 compares well with the range 0.20-0.38 of the previous group I animals. However, it should be noted that the comparable and ground squirrel values in rabbit (0.4), (0.6),suggest that the higher values seen in the central temporal montages 1 and 2 of the mink, namely 0.4 and 0.45, may be indicative of a potential difference between the physiological character of this part of the mink retina and the other regions. Against this is the fact that no such differences are reflected in the A:B ratios. Similarly, no differences are shown by the A:B ratio of the mink peripheral retina, even though the synaptic densities there are clearly lower than in mink central retina. Further study would be needed to determine the changes in cellular morphology, and/or density of synapses per unit area of cell process, that are the basis of this lower peripheral density. However, it can be said that the retina is significantly thinner in the far peripheral region studied than it is at its center, and the proportion of the plexiform layer occupied by glial processes is somewhat increased. Adiustine for the amount of space occupied b; the extra v

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MARK WM. DUBIN AND LINDA

glial elements did not greatly affect the density values. The paucity of synapses may reflect the low ganglion cell density in the far peripheral retina, although the A:B ratio implies that those cells present have receptive field properties similar to the rest of the ganglion cell population. Finally, no obvious reflection of the partial layer doubling in the LGN was observed in the retina. In sum, both qualitative and quantitative considerations allow the prediction that the mink retina will turn out to be much like the cat or monkey retina in its predominant receptive field characteristics. This study also furthers the concept of the typical vertebrate retina at the quantitative as well as qualitative level, in that the A:B ratio and synaptic density values of yet another retina have now been shown to fall well within the general range previously determined. In terms of the work on the mink LGN, and atypically crossed retinogeniculate projections in some mink varieties (Sanderson, ’74; Sanderson et a]., ’74), it would appear that the mink and cat visual systems are alike enough at the retinal level to validate comparisons at other levels of the visual system. ACKNOWLEDGMENTS

We wish to thank R. M. Shackelford, R. W. Guillery and K. J. Sanderson for providing the mink and Doctors Guillery and Sanderson for slides of mink retina and for suggestions concerning the manuscript. Doctor S. K. Fisher provided valuable comments and conversations during the course of manuscript preparation. This work was supported by NIH-NEI grant EY00998 to M. W. D. LITERATURE CITED Abercrombie, M. 1946 Estimation of nuclear population from microtome sections. Anat. Rec., 94: 239-247. Allen, R. A. 1969 The retinal bipolar cells and their synapses in the inner plexiform layer. In: The Retina. B. Straatsma et al., eds. University of California Press, Los Angeles, pp. 101-143. Boycott, B. B., J. E. Dowling, S. K. Fisher, H. Kolb and A. M. Laties 1975 Interplexiform cells of the mam-

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malian retina and their comparison with catecholamine-containing retinal cells. Proc. Roy. Soc. (London) 0.. 191: 353-368. Dowling, J. E. 1968 Synaptic organization of the frog retina: An electron microscopic analysis comparing the retinas of frogs and primates. Proc. Roy. Soc. (London) B., 170: 205-228. 1970 Organization of vertebrate retinas. Invest. Ophthal. 9: 655-680. Dowling, J. E., J. E. Brown and D. Major 1966 Synapses of horizontal cells in rabbit and cat retinas. Science, 153: 1639-1641. Dowling, J. E., and B. Ehinger 1975 Synaptic organization of the amine-containing interplexiform cells of the goldfish and cehus monkey retinas. Science, 188: 270-273. Dowling, J. E., and F. S. Werhlin 1969 Organization of the retina of‘ the mudpuppy, Necturus mculosa. I. Synaptic structure. J. Neurophysiol., 32: 315-338. Dubin, M. W. 1970 The inner plexiform layer of the vertebrate retina: A quantitative and comparative electron microscopic analysis. J. Comp. Neur., 140: 479-506. - 1974 Anatomy of the vertebrate retina. In: The Eye. Vol. 6. H. Davson and L. Graham, eds. Academic Press, New York, pp. 227-256. Fisher, S . K. 1972 A somato-somatic synapse between amacrine and bipolar cells in the cat retina. Brain Res., 43: 587-590. Fisher, S. K., and B. B. Boycott 1974 Synaptic connections made by horizontal cells within the outer plexiform layer of the retina of the cat and the rabbit. Proc. Roy. SOC.(London) B., 186: 317-331. Guillery, R. W. 1969 An abnormal retinogeniculate projection in Siamese cats. Brain Res., 14: 739741. 1970 The laminar distribution of‘ retinal fibers in the dorsal lateral geniculate nucleus of the cat: A new interpretation. J. Comp. Neur., 138: 339368. Guillery, R. W., and V. A. Casagrande 1976 Adaptive synaptic connections formed in the visual pathways in response to congenitally aberrant inputs. C.S.H.S.Q.B., 40:611-617. Guillery, R. W., and J. H. Kaas 1971 A study of normal and congenitally abnormal retinogeniculate projections in cats. J. Comp. Neur., 143: 73-99. 1973 Genetic abnormality of the visual pathways in a “white” tger. Science, 180: 12871289. Hubel, D. H., and T. N. Wiesel 1971 Aberrant visual projections in the Siamese cat. J. Physiol. (London), 218: 33-62. Reynolds, E. S. 1963 The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J. Cell Biol., 17: 208-212. Sanderson, K. J. 1974 Lamination of the dorsal lateral geniculate nucleus of the weasel (rnustelidae), racoon (procyonidae) and fox (canidae) familes. J. Comp. Neur., 153: 239-266. Sanderson, K. J., R. W. Guillery and R. M. Shackelford

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1974 Congenitally abnormal visual pathways in mink (Mustela oison) with reduced retinal pigment. J. Comp. Neur., 154: 225-248. Stell, W. K. 1972 Thr morphological organization of the vertebrate retina. In: Handbook of Sensory Physiology. Vol. VII/Q. 51. G . F. Fuortes, ed. Springer-Verlag, Berlin, pp. 112-213. U'itkovsky, P., and J. E. Dowling 1969 Synaptic relationships in the plexiform layers of carp retina. Z. Zellforsch., 100: 60-82.

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Witkovsky, P., and W. K. Stell 1973 Retinal structure in smooth dogfish Mustelus canis: Electron microscopy of serially sectioned bipolar cell synaptic terminals. J. Comp. New., 150: 147-167. U'ong-Kiley, M. T. T. 1974 Synaptic organization of the inner plexiform layer in the retina of the tiger salamander. J. Neurocytol., 3: 1-33. Wyatt, H. J., and N. W. Daw 1976 Specific effects of neurotransmitter antagonists on ganglion cells in rabbit retina. Science, 191: 204-205.

PLATE I EXPLANATION OF FIGURES

2 A rod spherule with numerous invaginated processes near a single ribbon is shown. Many of the invaginated processes have darkened specialized membranes, opposite similarly specialized presynaptic membranes. The scale mark on this and all subsequent figures is 0.5 Fm. Note that figures 2 through 4 are at the same magnification for purposes of comparison.

3 An altered rod spherule pattern is shown. The invagination and ribhon are adjacent to the cell's nucleus. In this picture the synaptic ribbon, arcuate density below the ribbon, and the pre- and postsynaptic membrane densities are clearly seen. Scale mark, 0.5 Fm.

4 A cone pedicle. Note that numerous processes abut the base of the pedicle in shallow invaginations. Two synaptic ribbons are present in this plane of section. The ribbon at the right (arrow) is presynaptic to a typical cone pedicle triad of postsynaptic processes. This pedicle is typical in size and should be compared with the smaller spherule shown in figure 2.Scale mark, 0.5 pm. 5 Both a and b show conventional synapses found within the outer plexiform layer. See text for further remarks. This figure and figures 6 , 7 , 8 insert, and 9 through 11 are all at the same magnification for purposes of comparison. Scale mark, 0.5 pm.

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THE RETINA OF THE MINK

PLATE 1

Mark Wrri. Diihin and Linda Turner

285

PLATE 2 EXPLAhKIION Ok FIGLKES

6 A conventional synapse in the outer plexiform layer (arrow) is indicated. The star is in a large process which contains numerous neurotubules and which has a different appearance than the other large process (asterisk) that contains neurofilarnents. Both large processes are probable horizontal cell processes (see text). Scale mark, 0.5 p m .

7 A serial conventional synapse in the inner plexiform layer. Scale mark, 0 5 pin.

8 A conventional synapse in the inner niiclear layer. The synapse (arrow) is shown enlarged in the inset. The nucleus of the soma that is postsynaptic may be seen at top. The synapse is near the middle of the nuclear layer and the arrow points in the direction inner plexiform layer to outer plexiform layer. Scale marks, 0.5 pm.

9 A ribbon synapse with a typical postsynaptic dyad in the inner plexiform layer is illustrated. One postsynaptic process makes a conventional reciprocal synapse (arrow) back onto the bipolar cell process. The other postsynaptic process contains no synaptic vesicles and is probably a ganglion cell dendritic element. Scale mark, 0.5 p m . 10 An inner plexiform layer ribbon dyad synapse in which both post-synaptic processes are amacrine cell elements. Note that one of the post-synaptic processes makes a conventional synapse onto the other. Scale mark, 0.5 pm.

11 An inner plexiform laycr ribbon synapse in which both of the postsynaptic dyad elements are ganglion cell dendritic processes. Scale mark, 0.5 pm.

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THE RETINA OF THE MINK Mark Wm. Diibin and Linda Turner

PLATE 2

287

Anatomy of the retina of the mink (Mustela vison).

Anatomy of the Retina of the Mink (Mustela visor?) MARK WM. DUHIN AND LINDA TURNER Molecular, Cellular and Decelopmental Biology, University of Colora...
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