Jonathan Stone

Synaptogenesis in the retina of the cat

We have studied the development of synapses in the retina of the cat from E(embryonic day)21 to adulthood. The inner plexiform layer (IPL) could be distinguished by E36, but at this age no synapses had formed, although compact processes had formed in the IPL and membrane specialisations had developed in adjacent processes. Conventional synapses form in the IPL from E45 and become increasingly numerous and differentiated over subsequent weeks. Extracellular space and cellular debris were prominent during the formation of these synapses. The conventional synapses appear to form principally between amacrine cells until E56, when ganglion cell dendrites could be identified as postsynaptic processes. Ribbon synapses characteristic of bipolar cells were identified around birth, suggesting that bipolar cells do not form synapses until that age. The outer plexiform layer (OPL) could be distinguished in central retina at E56. Extracellular space, debris of degenerating cells and mounds of agranular vesicles were prominent at this age but synapses were not observed until E59, when cone pedicles formed ribbon synapses onto horizontal cell processes. The first synapses clearly formed by spherules, also onto horizontal cells, were seen at E62. The central process of the postsynaptic triad, considered to be the dendrite of a bipolar cell, was first observed in both cone pedicles and rod spherules around birth, again suggesting that bipolar cells do not enter into synaptic arrangements until that age. Synaptogenesis in the OPL shows a strong centro-peripheral gradient; its initial stages were observed centrally in the late E50s but synapse formation was not complete in the retinal periphery until P(postnatal day)7 or later. We could not detect a centro-peripheral gradient in the formation of conventional synapses in the IPL, but the formation of ribbon synapses in this layer began centrally at birth and in the mid-periphery at P5. In summary, the first synapses to form in the retina are those which spread information laterally within the plexiform layers, between amacrine cells and from receptor to horizontal cells. The cells which carry information centrally, in particular bipolar cells, enter into synaptic arrangements considerably later. Further, retinal cells seem to form synapses in a distinct sequence: first amacrines, then receptors and lastly bipolar cells.

Development of retinal vasculature in the cat: processes and mechanisms.

Two principal processes can be distinguished in the development of the retinal circulation in the cat. One process, which forms most of the inner layer of vasculature, involves three stages. First, beginning prior to E (embryonic day) 26, spindle cells of mesenchymal origin spread over the inner surface of the retina. Second, beginning at approximately E48, a network of coarse capillaries forms, apparently derived from spindle cells. Third, major vessels differentiate from the capillary plexus, and the capillaries become thinner and more widely spaced. All three stages begin at the optic disc and spread towards the margin of the retina. The other process involves budding of capillary sized vessels from existing vasculature. This process forms the inner layer of vasculature at the area centralis, the outer layer of vasculature, and the radial peripapillary capillaries. It begins between P (postnatal day) 7 and P10 at the area centralis and spreads to the margins of the retina. The radial peripapillary capillaries form at a later stage (P20). The different topographies of the two processes suggest that they are controlled by distinct mechanisms. In the first process, the formation of vessels follows a pattern set by the early migration of spindle cells. In the second process, the vessels form in a pattern determined by the metabolic needs of the developing retina.

Morphology of catecholamine-containing amacrine cells in the cat's retina, as seen in retinal whole mounts

The morphology of catecholaminergic cells of the cats retina was studied by fluorescence microscopy of retinal whole mounts. Although varied in soma shape, these cells seem to represent a single group of cells with an average soma diameter of 14.5 micrometer in freeze-dried material. The fluorescent terminals of these cells formed a striking two-dimensional pattern: a significant portion of them appeared to be arranged in rings located at the boundary of the inner plexiform and inner nuclear layers. The mean diameter of these rings was 9.7 micrometer and their pattern appeared to extend unbroken across the retina. It was, in general, not possible to observe the connection between these rings and fluorescent somas, except when a ring was in a juxtasomatic position. It is suggested that the postsynaptic somas within these rings are either of other amacrines or of interplexiform cells. Using the Golgi-Colonnier technique on retinal whole mounts, an attempt was made to identify the cell type which resembles the catecholaminergic cell in its size, location and morphology. The suggested cell type appears to be among the largest amacrine cells, (mean soma size of 11.5 micrometer in Golgi material) with a considerable dendritic network at the border of the inner plexiform and inner nuclear layers, although there are branches reaching as far as the middle of the inner plexiform layer.

The optic nerve of the cat: Appearance and loss of axons during normal development

The number of axons in the optic nerve has been estimated in cats ranging in age from mid-gestation to adulthood. At mid-gestation the number of axons present in the nerve (218,000) already exceeded adult levels. The number of axons, nevertheless, more than doubled over the next 10-20 days, reaching a maximum of 450,000-483,000. In the last prenatal week and the first postnatal week, the number of axons declined rapidly, stabilizing at adult levels 2-3 weeks after birth. Myelination began just before birth and reached adult levels (over 95% of axons myelinated) 6-8 weeks after birth. Several mechanisms which may underlie the loss of axons are discussed.

The site of commencement of retinal maturation in the rabbit

In the developing retina of the rabbit the ganglion cell layer can first be identified between E(embryonic day) 20 and 24, but the regional variations found in the adult retina, particularly the visual streak, are not well developed until shortly before birth. At about E31, the last day of gestation, the laminar structure of the retina begins to mature, cytogenesis begins to cease and the outer plexiform layer starts to form. These processes commence in far temporal retina, at or near the site of the area centralis, and spread preferentially along the visual streak.

Parallel processing of information in the visual pathways: A general principle of sensory coding?

Abstract For many decades, clinicians have known that bodily sensation comprises several ‘submodalities’. More recently, neuroscientists have shown that the neural pathways which subserve somatic sensation are organized into parallel-wired neuronal ‘channels’. Each channel extends from the peripheral sense organ to the cerebral cortex, and subserves a different submodality. Over the past 15 years, a comparable pattern of organization has been demonstrated in the visual system. Clinicians and psychologists have distinguished submodalities of visual function, and neuroscientists have distinguished parallel-wired neuronal channels within the visual pathways. This parallel processing of different aspects of sensation may be fundamental to the operation of the visual as well as the somatosensory systems, and may prove to be a feature of all sensory pathways.

The Interpretation of Variation in the Classification of Nerve Cells

Within any biological population there is considerable variation in the physical characteristics of individual members, and the understanding and classification of such populations always depends on the interpretation of this variation. A major point of this paper is that groups of neurones can also be regarded as biological populations, and that at least three distinct types of variation can be found within any neural population:role-indicating variation, which enables different cells or groups of cells to perform different functions; systematic variation, which allows different cells (or sometimes the same cell) to perform a particular function under varying conditions; and residual variation, which is principally related to mechanisms of evolution and provides the population with its biological adaptability. Examples of these three types of variation are suggested for a number of properties of retinal ganglion cell populations. A second major point is that any functional classification of nerve cells should contain multiple taxonomic levels, corresponding to different levels of complexity and interaction within the nervous system. Thus, individual cells can belong to more than one group, each at a different taxonomic level, and these groups of cells can be viewed as interacting with each other rather than as operating in isolation. A multiple-level classification of cat retinal ganglion cells is presented with two broad groups, each subdivided into two lower-level groups, and an attempt is made to identify the categories of visual function to which these groups are related.

Cell division in the developing cat retina occurs in two zones

Cytogenesis in the kitten retina has been investigated with [3H]thymidine autoradiography and a stain for mitotic figures. The nuclei of cells in S-phase are located adjacent to the inner margin of the cytoblast layer, near the inner plexiform layer. The nuclei then migrate toward the outer limiting membrane (OLM) to divide. Evidence is presented that in a small population of mitotic cells, the nucleus does not migrate to the OLM, but divides in the inner part of the cytoblast layer or, after the outer plexiform layer has formed, in the inner nuclear layer. Cell division in this inner zone begins and ends later than at the OLM. Cells dividing there are fewer in number than those at the OLM, their mitotic spindles are oriented randomly rather than parallel to the retinal surface and their nuclei move little between S- and M-phases of the mitotic cycle. The zones of cytogenesis at the OLM and in the inner cytoblast layer resemble, respectively, the ventricular and subventricular zones of other areas of the developing central nervous system.

Distribution of cholinergic amacrine cells in the retinas of normally pigmented and hypopigmented strains of rat and cat

We have examined the soma size, number, and distribution of cholinergic amacrine cells in the retinas of albino and pigmented rats and of Siamese and common cats, using an antibody against choline acetyl transferase (ChAT). In the pigmented strains of rat and cat, ChAT-immunoreactive (ChAT-IR) somata were located in both the inner part of the inner nuclear layer (INL) and ganglion cell layer (GCL), and their processes spread in distinct strata of the inner plexiform layer (IPL). The diameters of the somata in the INL and GCL did not differ significantly at any retinal location. Furthermore, soma diameter did not vary with eccentricity, except at the area centralis of the common cat, where ChAT-IR somata in both layers were relatively smaller. In both species, ChAT-IR somata in the GCL outnumbered those in the INL at all retinal locations. Both populations of cells tended to concentrate at the area of peak ganglion cell density and along the visual streak. Additionally, areas of relatively high density extended superiorly from the area of peak density. The same features of morphology and distribution were identifiable in the hypopigmented strains of rat and cat, but the numbers of ChAT-IR cells were consistently higher.

Brain stem afferents to visual cortical areas 17, 18 and 19 in the cat, demonstrated by horseradish peroxidase.

The origins of brain stem projections to the cytoarchitectonically different areas 17, 18 and 19 of the cats visual cortex were studied following small horseradish peroxidase (HRP) injections. Labelled cells were counted in a dopaminergic nucleus (nucleus linearis rostralis (NLR)), other catecholaminergic nuclei (locus coeruleus, parabrachialis nuclei and nucleus subcoeruleus) and serotonergic nuclei (nucleus raphe dorsalis (NRD) and nucleus centralis superior (NCS)). Area 18 receives afferents from more locus coeruleus cells than either of areas 17 or 19. The number of labelled cells in the catecholaminergic nuclei far exceeds that in the serotonergic nuclei.