Abnormal ipsilateral visual field representation in areas 17 and 18 of hypopigmented cats.

We compared the central projections of retinal ganglion cells in temporal retina and the cortical representation of visual fields in areas 17 and 18 in cats with various hypopigmentation phenotypes (albino, heterozygous albino, Siamese, and heterozygous Siamese). In all cats studied, we found that the extent of abnormal ipsilateral visual field representation varied widely, and more of the ipsilateral visual field was represented in area 18 than in area 17. The greatest degree of ipsilateral visual field representation was found in albino cats, followed by Siamese, heterozygous albino and heterozygote Siamese cats, respectively. Additionally, in the different groups there was wide variation in the numbers of contralaterally projecting alpha and beta ganglion cells in temporal retina. In all cases, however, contralaterally projecting alpha cells were found to extend further into temporal retina than beta cells. We found that in each cat studied, the maximum extent of the abnormal ipsilateral visual field representation in areas 18 and 17 corresponded to the location of the 50% decussation line (i.e., the point where 50% of the ganglion cells in temporal retina project to the contralateral hemisphere) for alpha and beta cells, respectively, for that cat. Our results suggest that the extent of the abnormal visual field representations in visual cortex of hypopigmented cats reflects the extent of contralaterally projecting retinal ganglion cells in temporal retina.

Concomitant sensitivity to orientation, direction, and color of cells in layers 2, 3, and 4 of monkey striate cortex.

The receptive field properties of cells in layers 2, 3, and 4 of area 17 (V1) of the monkey were studied quantitatively using colored and broad-band gratings, bars, and spots. Many cells in all regions studied responded selectively to stimulus orientation, direction, and color. Nearly all cells (95%) in layers 2 and 3 exhibited statistically significant orientation preferences (biases), most exhibited at least some color sensitivity, and many were direction sensitive. The degree of selectivity of cells in layers 2 and 3 varied continuously among cells; we did not find discrete regions containing cells sensitive to orientation and direction but not color, and vice versa. There was no relationship between the degree of orientation sensitivity of the cells studied and their degree of color sensitivity. There was also no obvious relationship between the receptive field properties studied and the cells' location relative to cytochrome oxidase-rich regions. Our findings are difficult to reconcile with the hypothesis that there is a strict segregation of cells sensitive to orientation, direction, and color in layers 2 and 3. In fact, the present results suggest the opposite since most cells in these layers are selective for a number of stimulus attributes.

Postnatal development of different classes of cat retinal ganglion cells.

Previous investigators have documented the postnatal development of alpha and beta type ganglion cells in cat retinae (Ramoa et al. [1987] Science 237:522-525; Ramoa et al. [1988] J. Neurosci. 8:4239-4261; Dann et al. [1987] Neurosci. Lett. 80:21-26; Dann et al. [1988] J. Neurosci. 8(5):1485-1499). The development of the remaining cells (about 50%), which constitute a heterogeneous group and are referred to here collectively as gamma cells (Boycott and Wässle, '74), has not been studied in detail. The purpose of this study was to compare the postnatal development of alpha, beta, and gamma cells in kitten and adult retinae using horseradish peroxidase histochemistry and the fluorescent dye DiI. In the kitten, alpha, beta, and gamma cells are recognizable. We find, as have others, that kitten alpha and beta cell bodies and dendritic fields are significantly smaller than in the adult. However, kitten gamma cells are nearly adult sized. In fact, at birth the cell bodies of beta cells throughout the retina are significantly smaller than those of gamma cells. During the first 12 weeks of life, alpha and beta cell bodies increase in size from 90% to 680% depending upon eccentricity. Gamma cells hardly increase in size at all. Also, the normal adult center-to-peripheral cell size gradient for alpha and beta cells is not seen in the neonate. Gamma cells show no such gradient in the neonate or adult. Our results suggest that the morphological development of alpha and beta cells occurs later than that of gamma cells and may explain some of the differences in the effects of visual deprivation and surgical manipulation upon the parallel Y-, X-, and W-cell pathways.

Selective depletion of beta cells affects the development of alpha cells in cat retina.

The results of previous studies suggest that class-specific interactions contribute to the development of the different classes of retinal ganglion cells. We tested this hypothesis by examining the morphologies and distributions of alpha (alpha) cells in regions of mature cat retina selectively depleted of beta (beta) cells as a result of visual cortex lesions at birth. We find that alpha cells in regions of central retina depleted of beta cells are abnormally large while alpha cells in regions of peripheral retina depleted of beta cells are abnormally small. The normal central-to-peripheral alpha cell soma-size gradient is absent in hemiretinae depleted of beta cells. The dendritic fields of alpha cells in the border of beta-cell-depleted hemiretina extend preferentially into the beta-cell-poor hemiretina. In spite of this, alpha cell bodies retain their normal retinal distribution and remain distributed in a nonrandom mosaic-like pattern. Thus, it appears that the development of alpha retinal ganglion cells is influenced by interactions both with other alpha cells (class-specific interactions) and with surrounding beta cells (nonclass-specific interactions).

Extrinsic determinants of retinal ganglion cell development in primates.

As in all mammals studied to date, primate retina contains morphologically distinct classes of retinal ganglion cells (Polyak: The Retina. Chicago: University of Chicago Press, '41; Boycott and Dowling: Philos. Trans. R. Soc. Lond. [Biol.] 225:109-184, '69; Leventhal et al.: Science 213:1139-1142, '81; Perry et al.: Neuroscience 12:1101-1123, '84; Rodieck et al.: J. Comp. Neurol. 233:115-132, '85; Rodieck: In H.D. Steklis and J. Erwin (eds): Comparative Primate Biology, Volume 4: Neurosciences. New York: Alan R. Liss, Inc., pp. 203-278, '88). We have now studied the morphologies, central projections, and retinal distributions of the major morphological classes of ganglion cells in the normal adult monkey, the newborn monkey, and the adult monkey in which restricted regions of retina were depleted of ganglion cells at birth as a result of small lesions made around the perimeter of the optic disc. Both old-world (Macaca fascicularis) and new-world (Saimiri sciureus) monkeys were studied. Our results indicate that, at birth, the major morphological classes of monkey retinal ganglion cells are recognizable; cells in central regions are close to adult size whereas cells in peripheral regions are much smaller than in the adult. As in the adult (Stone et al.: J. Comp. Neurol. 150:333-348, '73), in newborn monkeys there is a very sharp division between ipsilaterally and contralaterally projecting retinal ganglion cells (nasotemporal division). Consistent with earlier work (Hendrickson and Kupfer: Invest. Ophthalmol. 15:746-756, '76) we find that the foveal pit in the neonate is immature and contains many more ganglion cells than in the adult. In the adult monkey in which the density of retinal ganglion cells in the central retina was reduced experimentally at birth, the fovea appeared immature, and an abnormally large number of retinal ganglion cells were distributed throughout the foveal pit. The cell bodies and dendritic fields of ganglion cells that developed within cell-poor regions of the central retina were nearly ten times larger than normal. In peripheral regions the effects were smaller. The dendrites of the abnormally toward the foveal pit. They did not extend preferentially into the cell-poor region as do the abnormally large cells on the borders of experimentally induced cell-poor regions of cat central retina (Leventhal et al.: J. Neurosci. 8:1485-1499, '88) or, as we found here, in paracentral regions of primate retina.(ABSTRACT TRUNCATED AT 400 WORDS)

Extrinsic determinants of retinal ganglion cell structure in the cat.

The degree to which a retinal ganglion cell's environment can affect its morphological development was studied by manipulating the distribution of ganglion cells in the developing cat retina. In the newborn kitten there is an exuberant ganglion cell projection from temporal retina to the contralateral lateral geniculate nucleus (LGNd) (Leventhal et al., 1988) and from nasal retina to the ipsilateral LGNd. Neonatal, unilateral optic tract section results in the survival of many of these ganglion cells (Leventhal et al., 1988). The morphology of ganglion cells which survive in regions of massively reduced ganglion cell density was studied. As reported previously (Linden and Perry, 1982; Perry and Linden, 1982; Ault et al., 1985; Eysel et al., 1985), we found that the dendritic fields of all types of ganglion cells on the border of an area depleted of ganglion cells extended into the depleted area. The cell bodies and dendritic fields of alpha and beta cells within depopulated areas, as well as on the borders of the depopulated areas, were larger than normal. The dendritic fields of these cells also exhibited abnormal branching patterns. For alpha and beta cell types the relative increase in size tended to be greatest where the relative change in density was the greatest. In fact, isolated beta cells within the cell-poor area centralis region resembled normal central alpha cells in the cell-rich region of the area centralis in the same retina. Interestingly, in the same regions of reduced density where alpha and beta cells were dramatically larger than normal, the cell body and dendritic field sizes of other cell types (epsilon, g1 and g2 were unchanged. These results indicate that neuronal interactions during development contribute to the morphological differentiation of retinal ganglion cells and that different mechanisms mediate the morphological development of different classes of cells in cat retina.

Experimental induction of an abnormal ipsilateral visual field representation in the geniculocortical pathway of normally pigmented cats.

In the normally pigmented neonatal cat, many ganglion cells in temporal retina project to the contralateral dorsal lateral geniculate nucleus (LGNd) and medial interlaminar nucleus (MIN). Most of these cells are eliminated during postnatal development. If one optic tract is sectioned at birth, much of this exuberant projection from the contralateral temporal retina is stabilized (Leventhal et al., 1988b). To determine how the abnormal projection from the contralateral temporal retina is accommodated in the central visual pathways, neuronal activity was recorded in the visual thalamus and cortex of adult cats whose optic tracts were sectioned as neonates. The recordings showed that up to 20 degrees of the ipsilateral hemifield is represented in the LGNd and MIN. Recordings from areas 17 and 18 of the intact visual cortex showed that up to 20 degrees of the ipsilateral visual field is also represented and that the ipsilateral representation is organized as in a Boston Siamese cat (Hubel and Wiesel, 1971; Shatz, 1977; Cooper and Blasdel, 1980) or a heterozygous albino cat (Leventhal et al., 1985b). The extent of the ipsilateral visual field representation was greater in area 18 than in area 17; the extent of the ipsilateral hemifield representation in areas 17 and 18 varied with elevation, increasing with distance from the horizontal meridian. The receptive fields of cells in the LGNd and visual cortex subserving contralateral temporal retina were abnormally large. Otherwise, their receptive field properties seemed normal. In the same animals studied physiologically, HRP was injected into the ipsilateral hemifield representation in the LGNd and MIN of the intact hemisphere. The topographic distribution of the alpha and beta cells, respectively, labeled by these injections correlated with the elevation-related changes in the ipsilateral visual field representation in areas 18 and 17. Our results indicate that the retinotopic organization of the mature geniculocortical pathway reflects the abnormal pattern of central projections of ganglion cells in neonatally optic tract sectioned cats. Thus, if they do not die, retinal ganglion cells normally eliminated during development are capable of making seemingly normal, functional connections. The finding that an albino-like representation of the ipsilateral hemifield can be induced in the visual cortex of normally pigmented cats suggests that the well-documented defects in the geniculocortical pathways of albinos are secondary to the initial misrouting of ganglion cells at the optic chiasm (Kliot and Shatz, 1985) and not a result of albinism per se.

Class-specific cell death shapes the distribution and pattern of central projection of cat retinal ganglion cells.

The development of the nasotemporal division in cat retina was studied. We find that in the normally pigmented neonatal cat significant numbers of ganglion cells of all types in temporal retina project to the contralateral dorsal lateral geniculate nucleus (LGNd); far fewer cells in temporal retina project contralaterally to the LGNd in the normal adult. Thus, most of these cells must be eliminated during development. Experimental interruption of one optic tract in the neonate results in the retrograde degeneration of the ipsilaterally projecting ganglion cells in the temporal retina ipsilateral to the lesion. Consequent to the loss of the ipsilaterally projecting cells in this hemiretina, many of the ganglion cells projecting to the intact contralateral LGNd, which are normally eliminated, survive. Also, unlike in the normal cat, in which very few of the small ganglion cells in temporal retina project contralaterally to the thalamus, in optic tract sectioned (OTX) cats, significant numbers of the smallest ganglion cells in the temporal retina ipsilateral to the lesion project contralaterally to the intact thalamus. In order to make a quantitative comparison of the distributions of ipsilaterally and contralaterally projecting cells in the temporal retinae of normal cats, OTX cats, and neonatal kittens, it was necessary to determine the position of the vertical meridian in all animals. We defined the vertical meridian as the median edge (Stone, 1966). The median edge was determined from the distribution of the most nasally located, ipsilaterally projecting cells in temporal retina. The results indicate that the angle of the vertical meridian (median edge) with respect to the area centralis and optic disc is specified before birth and does not differ in normal cats, OTX cats, or neonatal kittens. Since the location of the vertical meridian does not change with age in postnatal life and is not affected by optic tract section, corresponding regions of retina in the different groups could be compared. A quantitative analysis of ganglion cell density in the temporal retina contralateral to the section, ipsilateral to the intact hemisphere, indicated that there was a reduction in the population of ipsilaterally projecting ganglion cells that was complementary to the abnormally large number of contralaterally projecting cells surviving in the temporal retina ipsilateral to the lesion.(ABSTRACT TRUNCATED AT 400 WORDS)

The nasotemporal division in primate retina: the neural bases of macular sparing and splitting.

In primates, each hemisphere contains a representation of the contralateral visual hemifield; unilateral damage to the visual pathways results in loss of vision in half of the visual field. Apparently similar severe, unilateral lesions to the central visual pathways can result in two qualitatively different central visual field defects termed macular sparing and macular splitting. In macular sparing a 2 degrees to 3 degrees region around the fovea is spared from the effects of unilateral damage to the visual pathways. In macular splitting there is no such spared region and the scotoma produced by unilateral brain damage bisects the fovea. The patterns of decussation of the different classes of retinal ganglion cells in both New World (Saimiri sciureus) and Old World (Macaca fascicularis) monkeys have been determined by horseradish peroxidase injection. In both species the distributions of ipsilaterally and contralaterally projecting ganglion cells in the central retina are different from those in other mammals and suggest neural bases for macular sparing and splitting, respectively.