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Growth cones are also scattered widely within individual fascicles and are as common on the inside next to other growth cones and axons as they are around the outside next to glial cell processes. A clear example of a group of growth cones in the center of a fascicle is illustrated in Figure 5. Here, a group of 4 growth cone profiles is shown close to the center of a large central fascicle, which itself is located at the center of the nerve. None of the 4 growth cones contact a glial cell process at this level.

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The superficial-to-deep difference appears to be more extreme when growth cone percentages per fascicle are plotted instead of absolute densities (Figs. 9A, squares). For instance, at E49 the percentage of growth cone profiles averages about 0.5% in central fascicles and is as high as 15% in superficial fascicles, a 30-fold difference. In comparison, the absolute density difference is only 4–5-fold. The explanation is that the average size of fibers in superficial and deep fascicles differs greatly. Central fascicles typically contain many more small fibers than do superficial fascicles (Fig. 10B, C). This in turn leads to an increase in axon packing density and a sharp decrease in the percentage of growth cone profiles in the total fiber population in these central fascicles. The reason there are more small axons in central fascicles is related to axon age: small axons are typically older; they have been in the nerve for a longer time, and their growth cones have progressed farther into the brain. In contrast, large axons are relatively young axons or even the trailing part, the shank, of the growth cone (Fig. 5; Williams and Rakic, 1985).

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Between E39 and E45, the optic nerve is transformed rapidly by the addition of thousands of fibers. The lumen of the stalk is obliterated, and the dorsal half of the nerve becomes filled with fibers. During this period, fiber number doubles approximately every 24 hr, and by E45 the nerve contains 380,000 ± 10,000 fibers and has a cross-sectional area of about 40,000 µm. Of this area, 70–75% is occupied by fibers; the remainder is occupied by glial cells and a few blood vessels.

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The geometry of growth cones can vary with position and age (Tosney and Landmesser, 1985; Bovolenta and Mason, 1987; Nordlander, 1987; Holt, 1989). This shape variation could generate false gradients in growth cone density. In preliminary work and work still in progress, we have found that the form of growth cones in the monkey varies comparatively little with age or position within the nerve (Williams and Rakic, 1987). For instance, the shape and ultrastructure of large sets of growth cones in the center and periphery of the nerve and on the nasal and temporal sides of the nerve cannot be distinguished either qualitatively or quantitatively. Furthermore, we have not been able to detect any quantitative morphological differences between growth cones close to the retina and those close to the optic chiasm, Finally, direct comparisons of serially sectioned tissue in the optic nerve also demonstrate rather modest age variation in growth cone morphology (Williams and Rakic, 1984). Nonetheless, it should be obvious from the foregoing remarks that estimates of growth cone distribution should be interpreted cautiously. As a rule, relative comparisons of growth cone density within single sections can be made with few reservations. If there are twice as many growth cone profiles 10 µm from the pial margin as compared to 50 µm from the margin, and if the profiles have the same shape and size, then this result reflects almost precisely a 2-fold difference in the absolute number of growth cones.
An additional factor to consider in this context is that there may be substantial differences in the mean velocity of axonal growth (Agiro et al., 1984; Maggs and Scholes, 1986; Davies, 1989). Consequently, equal densities of growth cones in two regions of the nerve do not necessarily signify that the same number of growth cones will traverse the two regions in a given period of time. A 2-fold difference in mean velocity could give rise to a 2-fold difference in the flow of growth cones. Because this difference is invisible in static images, one must recognize the possibility that there are velocity gradients along the pathway from the retina to the target and from subpial fiber bundles to those located deep in the pathway.

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The particular fiber architecture of the optic nerve depends primarily on the behavior of growth cones early in development. For instance, in cichlid fish, retinal ganglion cell growth cones definitely grow together in a single compact bundle at the surface of the nerve (Maggs and Scholes, 1986). This characteristic ultimately gives rise to a mature nerve that is ribbon shaped. One consequence of the peripheral affinity of growth cones in goldfish is that fibers from different parts of the retina that grow out of the eye at the same stage merge in the nerve. Here they form annuli or bands of new fibers beneath the pia (Easter et al., 1981; Scholes, 1981; Bunt, 1982; Taylor, 1987). As a result, the optic pathway becomes stratified—the oldest axons are located deepest; the youngest are located more superficially. This organization is referred to as chronotopic.
The structure of the adult mammalian optic nerve differs in important ways from the highly ordered chronotopic pattern characteristic of fish. Retinal axons in the optic nerves of humans, monkeys, cats, and several other mammalian species are arranged in a comparatively disorderly, but still roughly retinotopic, pattern (Polyak, 1957; Hoyt and Luis, 1962; Naito, 1986, 1989). This class difference may reflect the more chaotic spatiotemporal pattern of ganglion cell genesis in mammals or the greater density of growth cones traversing the pathway. Serial-section analysis of single axons and growth cones has shown that this disorder is present as early as E39 in the monkey and that the disorder is most likely caused by the meandering paths taken by individual growth cones (Williams and Rakic, ). However, it is clear that growth cones do not wander too far from their initial axonal neighbors, because a limited degree of retinotopy is maintained throughout the nerve (Naito, 1989). Evidently, the particular retinal site from which a fiber originates is somewhat more important in mammals than the time at which the fiber and cell body are generated.
The notable differences in the architecture of the optic nerve, particularly between teleosts and mammals, suggest that there may be equally revealing differences in the behavior and substrate affinities of retinal growth cones in this particular part of the pathway. A simple difference in the expression of substrate preferences of homologous neurons in different vertebrate classes and in different parts of the optic pathway may underlie the architectural differences and may explain differences in the ultimate targets chosen by retinal ganglion cell growth cones. Similarly, a relaxation in substrate preferences in the optic nerve of mammals may also account for the considerable degree of mixing among fibers.

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[Growth Cone Gradient in the Optic Chiasm. On embryonic day E39 the first few thousand axons cross midline and begin to form an optic chiasm. At this stage, growth cones are found in all fascicles. Most fascicles are located 5–20 µm from the pial surface and do not yet form the dense aggregate of fibers typical of the more mature chiasm. By E45 a definitive chiasm has formed. Fasicles can no longer be recognized. Already at this age close to 300,000 fibers from each nerve cross midline in a dense tract criss-crossed by surprisingly few glial processes. While growth cones are distributed throughout the chiasm, there is a distinct deep-to-superficial gradient (Fig. 12). In contrast to the nerve, whorl-like aggregates of growth cones are common in the chiasm at this age. At E54 and E58 the deep-to-superficial gradient is even more marked, although growth cones are still common up to 100 µm from the pial surface.]