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Note to the Reader This is a revised edition of a paper published in Neuroscience in 1984.
Revised HTML edition <> copyright © 1998 by Robert W. Williams

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Binocular Interaction in the Fetal Cat Regulates the Size of the Ganglion Cell Population

L. M. Chalupa*, R. W. Williams* and Z. Henderson
*Department of Psychology and the Physiology Graduate Group, University of California, Davis, CA 95616, U.S.A. and The University Laboratory of Physiology, Oxford University, Oxford OXI 3PT, U.K.

Neuroscience Vol. 12, No. 4, PP. 1139—1146, 1984  


     Experimental Procedures



During fetal development of the cat’s visual system there is a marked overproliferation of optic nerve axons. Binocular interactions before birth contributes to the severity of fiber loss since removal of an eye during gestation attenuates axon loss in the remaining optic nerve (Williams et al., 1983; Rakic and Riley, 1983). The purpose of the present study was to determine whether this reduced loss of optic nerve fibers is due to a failure of retraction by supernumerary axon branches or to a reduction in ganglion cell death. To resolve this issue, we compared the number of ganglion cells and optic nerve fibers in adult cats which had one eye removed at known gestational ages. Retinal ganglion cells were backfilled with horseradish peroxidase and counts were made from retinal wholemounts. The axon complement was assessed with an electron microscopic assay. In the retinas of a normal cat we estimated 151,000 and 152,000 ganglion cells. The optic nerves of two other normal cats contained approximately 158,000 and 159,000 axons. In comparison, an animal enucleated on embryonic day 42 had 180,000 ganglion cells and 178,000 optic nerve fibers, while in an animal enucleated on embryonic day 51 the corresponding estimates were 182,000 and 190,000. The close agreement between cell and fiber counts indicates that axonal bifurcation does not contribute appreciably to the axon surplus in the optic nerve of prenatally enucleated cats.
     These results demonstrate that prenatal binocular interaction regulates the size of the mature retinal ganglion cell population.



Retinal projections are distributed more widely early in development than at maturity (Rakic, 1976, 1977; Cavalcante and Rocha-Miranda, 1978; Frost and Schneider, 1979; Land and Lund, 1979; Linden et al., 1981; Sengelaub and Finlay, 1982; Sanderson et al., 1982; Williams and Chalupa, 1982, 1983; Shatz, 1983; Chalupa and Williams, 1984). The events underlying the restriction of retinal connections to discrete regions within the visual centers of the brain are poorly understood. However, it is known that this process is dependent upon binocular interaction since removal of one eye in fetal monkeys (Rakic, 1981) and cats (Williams and Chalupa, 1982, 1983; Williams, 1983), as well as in neonatal rodents (Land and Lund, 1979), results in the maintenance of widespread projections from the remaining eye.
     Recently, Williams et al. (1983) and Rakic and Riley (1983) demonstrated that prenatal unilateral enucleation also attenuates the severity of optic nerve fiber loss. Adult catsand rhesus monkeys from which an eye was removed before birth have significantly more axons in the remaining optic nerve than normal animals. It was suggested (Williams et al., 1983) that this fiber surplus could result either from a failure to withdraw extra axon branches which may be present within the optic nerve early in development, or from a reduction in the magnitude of normal ganglion cell death (Dreher et al., 1983; Jeffery and Perry, 1981; Sengelaub and Finlay, 1982). To determine which of these explanations is correct, in the present study we compared the number of ganglion cells and fibers in the remaining retina and nerve of adult cats from which an eye was removed before birth.
     Previous estimates of retinal ganglion cell number have generally relied on Nissl-stained material in which the differentiation of ganglion cells from glial and displaced amacrine cells is uncertain (Hughes, 1975; Stone, 1965, 1978). To overcome this difficulty, we labeled retinal ganglion cells with horseradish peroxidase following multiple injections of this enzyme into the dorsal lateral geniculate nuclei and the superior colliculi.


Experimental Procedures

Surgical technique. The in utero surgical technique and the method used to determine gestational age have been described in previous papers (Williams and Chalupa, 1982, 1983, Williams et al., 1983). An incision was made through the uterus to expose the head of the fetus, the eyelids were parted, and an eye was removed with small curved hemostats. The eyes weighed 90 mg at embryonic day 42 (E42) and 230 mg at E51. Incisions were closed with absorbable suture material, and the litters were allowed to come to term. Parturition was on E63 for the fetus enucleated on E42, and on E64 for that enucleated on E51.

Injection protocol. At 10- and 12-months of age, the two experimental animals and a normal adult were prepared for physiological recordings under barbiturate anesthesia. The skull overlying the dorsal lateral geniculate nuclei and the superior colliculi was removed. The animals were paralyzed by infusion with gallamine triethiodide in lactated Ringer’s. The pupils were dilated with homatropine hydrobromide, and the corneas fitted with clear contact lenses. Retinal landmarks were projected onto a tangent screen located 57 cm in front of the animal. A series of penetrations were made with a tungsten microelectrode through the dorsal lateral geniculate nucleus and superior colliculus in order to map these structures and accurately delimit their margins. Subsequently, four injections of horseradish peroxidase (60–80% Sigma Type VI in 2% dimethylsulfoxide) were made into each lateral geniculate nucleus and superior colliculus using a 10 µl syringe fitted with a 27-gauge needle. Each injection of 1.0 µl was delivered continuously over a 15 min period.

Histological procedures. Following a survival period which ranged from 12 to 24 h, animals were anesthetized deeply, and perfused transcardially with cold saline followed by 2.5% purified glutaraldehyde and 1.25% paraformaldehyde in 0.1 M phosphate buffer (pH 7.4). The eye, optic nerve, optic tracts and brain were removed. Brains were sectioned at 50 µm, and reacted using either the tetramethyl benzidine or the phenylenediamine-pyrocatechol method (Hanker et al., 1977).
     Within 1 h of fixation the retina was freed from the eye. The cornea, lens, and vitreous were discarded, and a series of radial cuts was made through the globe. The choroid layer and sclera were removed. After a wash in phosphate buffer, the retina was reacted to demonstrate peroxidase activity using the method of Hanker and colleagues (1977) as modified by Perry and Linden (1982). The retina was then flat-mounted on heavily gelatinized slides, dehydrated, cleared, and coverslipped.


Analysis. Prints of each retina were made at x10 by inserting the wholemounts into the negative carrier of an enlarger. The retinal areas were measured using a computerized planimeter (Zeiss Videoplan). Each retina was scanned at x400 using a planapochromatic oil objective. Ganglion cells could be identified unequivocally by the dark brown granules of chromogen that outlined the somata and dendrites. Labeled neurons were counted within the margins of a net graticule covering an area of 0.058 mm2. Cells intersecting the upper and right edges of the graticule were also included in the count. A sample was taken from each square millimeter of the retina, except around the area centralis, where samples were taken at 0.25 mm2intervals. The numbers of labeled cells per sample field were transferred to x10 drawings of the wholemount. Sampling loci with similar count values were connected to form a set of concentric isodensity lines. These contours were smoothed by obtaining supplemental samples.
     The number of ganglion cells in each retina was determined by adding separately the counts obtained at 1 mm2 and 0.25 mm2 sampling intervals. The resulting totals were multiplied by the ratio of the sample interval to the graticle field area. The sum of these two products provided an estimate of the ganglion cell population.
     Optic nerve counts. Optic nerves were processed for routine electron microscopy using the procedures described previously (Williams et al., 1983a). An ultrathin section through a midorbital segment of the nerve was photographed at a primary magnification between x2000 and x2500. In order to estimate the axon complement of the nerve, the average axon number of a group of more than 100 sample micrographs was multiplied by the ratio of the individual micrograph field area to the total area of the thin section.



In experimental and control animals, peroxidase reaction product filled the entire dorsal lateral geniculate nucleus the superficial portion of the pretectal complex, and the full extent of the superior colliculus on both sides of the brain. In every animal, labeled ganglion cells were distributed across the entire retina, and typical examples of perikaryal label from central and peripheral portions of the retina are depicted in Fig. 1(A) and (B). Low-power micrographs of the left and right retinas from a normal cat and those of the two experimental animals are shown in Fig. 2. Examples of the ganglion cell count distribution and isodensity profile for one of these wholemounts are illustrated in Fig. 3. Prominent features of ganglion cell distribution are readily apparent, including: (i) a dense region of labeled neurons a few millimeters above and temporal to the optic disc which comprises the area centralis; (ii) the horizontal streak, an elongated aggregate of cells extending along the temporal and nasal axis and (iii) a pronounced radial gradient of population density.

Figure 1
Figure 1. Examples of labeled ganglion cells following bilateral injections of horseradish peroxidase into the lateral geniculate and superior colliculus of the E42 enucleate. The region shown in (A) is from the central retina, about 2 mm nasal from the area centralis, while that depicted in (B) is from the periphery, more than 12 mm from the area centralis.



The two retinas obtained from the normal cat contained 151,000 and 152,000 ganglion cells. In comparison, we have previously estimated that the optic nerves of two normal mature animals contained 158,000 and 159,000 fibers (Williams et al., 1983).

TABLE 1: Effects of Prenatal Unilateral Enucleation upon Ganglion Cell and Optic Axon Number [updated edition]

  Ganglion Cell     Axon     Retinal
Animal* Number     Number     Area (mm2)

Control 1 151,000 (R)**     —-     519
  152,000 (L)     —-     522
Control 2 —-     158,000     —-
Control 3 —-     159,000     —-
Control 4       164,000     —-

E42 enucleate 180,000(L)     178,000     501
E51 Enucleate 182,000 (L)     190,000     561
E45 Enucleate —-     198,000     —-
E46 Enucleate —-     200,000     —-

*Optic nerve estimates from Williams et al., 1983. All animals were mature
**(R) right retina; (L) left retina


     In both experimental animals there was close correspondence between the ganglion cell and fiber counts. The animal enucleated at E42 had a ganglion cell population of 180,000, whereas the nerve contained 178,000 optic fibers. A similar analysis of the E51 enucleate yielded a cell count of 182,000 and a corresponding fiber count of 190,000. The discrepancies are minimal; l% in the first case and 4% in the second case. Both ganglion cell and fiber counts revealed a moderate, but consistent increase between 16 and 20%—attributable to the absence of binocular interaction following fetal enucleation. The difference in the number of ganglion cells between normal and prenatally enucleated animals is statistically significant (t = 26.38, P < 0.01, df = 2), as is that of the fiber counts (t = 4.24, P <0.05, df = 2). It should also be noted that the retinal surface areas were not appreciably greater than normal in the prenatally enucleated animals. These results are summarized in Table 1.


Figure 2
Figure 1. Retinal wholemounts from an adult cat and from two animals that had an eye removed at E42 and E51. Note that ganglion cells were labeled in all regions of each retina. At this magnification only the largest ganglion cells are readily distinguished.



Are the surplus ganglion cells in the prenatally enucleated animals confined to a particular retinal region? To answer this question we performed a regional analysis of the ganglion cell population for each retina. Three sets of comparisons were made: area centralis vs the periphery, temporal vs nasal retinal fields, and the region of the decussation line (a 2-mm-wide strip centered over the border between temporal and nasal sides of the retina) vs the remaining portion of the retina. These results, summarized in Table 2, revealed that the population increment was not limited to a particular region of the retina in either experimental animal. In the cat enucleated at the earlier prenatal age (E42) a greater excess of ganglion cells appears to be concentrated in the central region; however, there is considerable variability in the area centralis counts in the normal retinas and, most likely, this reflects the difficulty of obtaining an accurate count in this region due to the high density of labeled cells.

Figure 3
Fig. 3. Color-coded isodensity plots of the left retina of an adult cat from whcihn one eye was removed two weeks before birth (E51). An example of the counts derived from the retinal wholemounts. In the upper tracing, the numbers indicate the ganglion cell counts in each of the sites that were sampled in this retina. The size of the sampling area was 0.058 mm2. Click on the image to obtain a larger image or download a high-resolution 300 KB image with the original numerical data superimposed on the wholemount map.



TABLE 2: Assessement of Regional Effects on Cell Density following Prenatal Enucleation

Regions E42 enucleate E51 enucleate Normal (R) Normal (L)
Compared N (% increase) N (% increase) N N

Center vs 36,638 (33%) 33,746 (23%) 23,730 31,350
Periphery 143,362 (16%) 148,254 (20%) 127,270 120,650
Nasal vs 127,240 (23%) 127,518 (23%) 103,447 107,450
Temporal 52,760 (15%) 54,482 (18%) 47,553 44,550
Decussation vs 33,574 (19%) 32,385 (16%) 28,069 27,806
Remainder 146,526 (19%) 149,615 (21%) 129,931 124,195

The central retian is defined as the region in which the ganglion cell density exceeds 50 cells per sample area (0.058 mm2).
The region of decussation is defined as a vertically oriented strip of retinal tissue, 2-mm-wide, passing through the middle of the area centralis.
By percent increase we mean the percentage by which the number of ganglion cells in a particular regiopn is greater than the average of the control retinas.




We have demonstrated that the increase in the cat’s optic nerve fiber population that results from prenatal unilateral enucleation is matched closely by the number of ganglion cells in the remaining eye. In one case (E42 enucleate) the estimates of optic fibers and ganglion cells diverge by less than l%, while in the other (E5l enucleate) this difference amounts to about 4%. This indicates that axonal bifurcation within the retina or the optic nerve does not contribute significantly to the over-abundance of optic nerve fibers in unilaterally enucleated cats. Since the fetal retina of the cat contains many more ganglion cells than the mature retina (Lia et al., 1983; Stone et al., 1982), we conclude that prenatal binocular interactions influence ganglion cell survival in the cat’s retina. Furthermore, the degree to which binocular interactions regulate the severity of ganglion cell loss does not appear to depend critically on the gestational age at which one eye is removed. At E42 the fiber population within the cat’s optic nerve is near its peak or more than 500,000, while by E51 there are less than 300,000 axons (Williams et al., 1983b, [see 1986]). Removal of an eye at these two gestational ages resulted in essentially the same number of ganglion cells within the remaining retina.
     Previous studies that have examined the ganglion cell population in the cat have yielded diverse estimates (Stone, 1965, 1978; Hughes 1975). We believe this is due primarily to the difficulty in differentiating ganglion cells from other cell types (see review by Perry (1982) for discussion of methodological considerations). In contrast, our procedure provides unequivocal identification of ganglion cells, and it is therefore not surprising that the variability between the left and right retinas from the normal cat is negligible. Furthermore, our estimates of the ganglion cell population are almost identical to that provided by Illing and Wässle (1981) who also identified ganglion cells by backfilling with peroxidase enzyme (their estimate: 151,000). The reliability of the fiber estimation procedures we have used has been discussed recently in detail (Williams et al., 1983). The close correspondence between the estimates of cell number and axon number lends credibility to both methods of quantification.
     While our findings demonstrate that optic nerve fibers do not branch to any significant degree in normal and prenatally enucleated animals, this does not rule out the possibility that supernumerary collaterals contribute to the organization of the fetal nerve (Ng and Stone, 1982; Rager and Rager, 1976; Rakic and Riley, 1983; Williams et al., 1983ab). Indeed, retraction or degeneration of axonal branches has been implicated in the development of several pathways, including the corpus callosum, as well as the trochlear (Sohal and Weidman, 1978) and cochlear nerves (Jackson and Parks, 1982). Furthermore, extensive axonal branching has also been observed in the regenerating optic nerve of the goldfish. It would therefore be worthwhile to apply the methods used in the present study to determine whether or not optic nerve axons bifurcate in the fetal cat. [This study was undertaken several years later by Lia, Williams, and Chalupa (1986). We found that axons of retinal ganglion cells do not have branches within the optic nerve during development.]
     It should also be pointed out that our study does not address the possibility that prenatal eye removal could augment the number of branching fibers at the optic chiasm or within the optic tract. However, early unilateral eye enucleation in the hamster has been found to cause only a very small increase in axonal collateralization at the chiasm (Hsaio and Schneider, 1980).
     It has been suggested that prenatal unilateral enucleation may double the number of postsynaptic sites available to fibers from the remaining eye (Rakic, 1981; Williams and Chalupa, 1983). Although the intact retina does innervate the entire contralateral and ipsilateral nucleus, there is a clear reduction in the volume of the geniculate, particular, contralateral to the removed eye (Chalupa and Williams, 1984; Rakic, 1981; Williams, 1983). This could explain, in part, why we obtained only a relatively modest increase in the ganglion cell population following unilateral enucleation during fetal life.
     It also seems quite likely that factors other than the availability of target sites serve to limit the number of ganglion cells that survive to maturity. These may include: (1) the elimination of ganglion cells which terminate on inappropriate target cells–inappropriate in the sense that such connections result in topographic or functional mismatches; (2) the geometry of the postsynaptic target cells, and (3) intrinsic programs of retinal development. In terms of the latter, the recent work of Perry and Linden (1982) is particularly noteworthy. They have proposed that dendrodendritic competition regulates the magnitude of ganglion cell loss (Perry et al., 1983). If this were the case, it might be expected that the dendritic fields of ganglion cells in prenatally enuceleated animals would be smaller than normal. Since the areas of the retinal wholemounts in these animals are not greater than normal, a decrease in size of dendritic fields would permit accommodation of the excess ganglion cell population without disrupting the retinal mosaic.

Concluding remarks

While the results of the present study indicate clearly that prenatal binocular interaction regulates the size of the ganglion cell population, the underlying basis for this interaction remains largely speculative. One obvious possibility is that during early development projections from each eve compete for the control of individual target cells. In the cat a well-defined retinal decussation pattern is present as early as E44: therefore, binocular competition would involve axonal terminals emanating from ganglion cells in the nasal contralateral retina and the temporal ipsilateral retina. The reorganization that has been described in the visual system following early eye removal, including the results of the present study could be interpreted as being due to interruption of an inter-ocular competitive process. In line with the binocular competition hypothesis is the recent finding that some lateral geniculate lateral geniculate neurons in the prenatal cat can be activated by stimulation of both optic nerves. However. anatomical evidence for binocular innervation of individual neurons during fetal development is yet to be provided. At present, therefore, it is equally plausible that removal of one eye makes available additional postsynaptic territory that can be occupied by some of the waiting or later arriving axons derived from ganglion cells of the intact eye. Such an interpretation of binocular interaction also accounts for known consequences of early unilateral monocular enucleation.



We are grateful to Deborah van der List for calculations of cell distribution and the preparation of illustrations. This study was supported by Grant EY03991 from the National Eye Institute to L.M.C., a Jastro Shields Research Award to R.W.W., and Grant G979/49 from the Medical Research Council, London to Z.H.



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Accepted 27 January 1984


Neurogenetics at University of Tennessee Health Science Center

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