Anterograde movement of DiI and transneuronal transport of wheat germ aglutininhorseradish peroxidase (WGA-HRP) were used to study the temporal and laminar patterns of ingrowth of the geniculocortical projection to visual cortex in fetal and postnatal rats. The development of this projection was compared to patterns of migration and settling of L3HI-thymidine-labeled neurons destined for cortical layer IV, and to geniculocortical synapse formation. DiI-labeled geniculocortical axons were found in the intermediate zone beneath the lateral cerebral mantle at embryonic day (El17 and in the subplate layer underlying visual cortex by E18. On E l 9 they appeared to accumulate and grow radially into an expanding subplate layer and into the deep part of developing cortical layer VI. By postnatal day (P)O, DiI or WGA-HRP-labeled geniculocortical axons were found in developing cortical layers VI and V. By P1, they invaded the deep portion of the cell-dense cortical plate, where they were in position to make initial contact with neurons that would later form layer IV. A few axons traversed the cortical plate to reach the marginal zone. Layer IV became an identifiable layer on P2, and a clear projection to layer IV was evident by P3. These results suggest that geniculocortical afferents grow continuously from the intermediate zone, initially into an expanding subplate layer and then sequentially into each of the developing cortical layers without evidence of "waiting." Electron microscopic data suggest that geniculocortical axons begin to form immature synapses with dendrites and neuronal perikarya as they first encounter cortical neurons, first in the subplate layer and then in developing layers VI, V and marginal zone, in addition to the primary target layer IV. The precise targeting and overall temporal and laminar patterns of ingrowth and synaptogenesis suggest that geniculocortical axons are directed to the visual cortex by guidance cues within the internal capsule and subplate. Further, they reach the occipital pole early enough to influence the specification and histogenesis of cortical area 17, perhaps by exerting an influence on the deep-to-superficial ' Lwave'' of neuronal differentiation in sequentially developing subplate and cortical layers VI, V and IV.Key words: cerebral cortex development, DiI, transneuronal WGA-HRP, subplate, 1993 Wiley-Liss, Inc. thalamocortical projectionsThe structure and topographic organization of thalamocortical (TC) projections in adult brains have been well characterized and detailed information is now available regarding their areal and laminar patterns of termination (e.g., Lashley, '34; Ribak and Peters, '75; Peters and Feldman, "76; White, '79). This detailed information makes these projections attractive candidates for the study of developmental processes. However, our knowledge of mechanisms and temporal patterns of development remains fragmented because it is only recently that suitable techniques have been developed that allow the precise temporal and spatial resolut...
The ability of an animal to localize a sound in space requires the precise innervation of the superior olivary complex by the ventral cochlear nuclei on each side of the lower brainstem. This precise pattern of innervation could require an immutable recognition of appropriate targets by afferent processes arising from these nuclei. This possibility was investigated by destroying one cochlea of gerbil pups (Meriones unguiculatus) on the second postnatal day and assessing the projections from the ventral cochlear nucleus (VCN) on the unablated side to the superior olivary complex during the subsequent 2 weeks and after the animals had reached maturity. A crystal of 1,1'-dioctadecyl-3,3,3',3'-tetramethylindocarbocyanine perchlorate (DiI) was inserted into VCN on the unablated side in animals ranging in age from 3 to 14 days. To assess the permanence of any altered pattern of innervation, horseradish peroxidase was injected into VCN on the unablated side in adult, neonatally ablated animals. Finally, electrophysiological responses to acoustic stimuli delivered to the ear on the unablated side were recorded in the superior olivary complex of adult animals to assess whether altered innervation patterns were functional. Normative data were derived from our accompanying study of the development of VCN projections to the superior olivary complex in normal gerbils (Kil et al., this issue). Whereas VCN normally projects to the lateral aspect of the ipsilateral medial superior olive and to the medial aspect of the contralateral medial superior olive in control animals, in experimental animals VCN on the unablated side projects to both sides of these nuclei. Whereas in the gerbil, VCN normally projects only to the hilar area and to the ventrolateral limb of the contralateral lateral superior olive, in experimental animals VCN on the unablated side projects throughout this nucleus. This induced projection is specific in that the efferents to each limb of the contralateral nucleus are linked to the normal projection to the homotopic region of the ipsilateral nucleus. Whereas VCN innervates the contralateral medial nucleus of the trapezoid body in control animals, in experimental animals VCN on the unablated side provides calyces of Held in the ipsilateral nucleus as well. The induced projections to these three major subnuclei of the superior olivary complex first appear within 24 hours of the cochlear ablation and continue to develop over at least the subsequent 11 days. Thus, prior to the day when the cochlea becomes functional, VCN has established specific ectopic projections to loci normally innervated by VCN on the ablated side.(ABSTRACT TRUNCATED AT 400 WORDS)
The histochemical localization of cytochrome oxidase within the normal retina and lateral geniculate nucleus (LGN) of cats, ferrets, and monkeys revealed that distinct layers, types of cells, and portions of neurons are more intensely stained than others. The dark staining of photoreceptor inner segments and cone pedicles and the light staining of photoreceptor outer segments, somata, and rod spherules demonstrates that different segments of the same cell may have disparate but distinct levels of oxidative enzyme activity. In tangential sections of retina, regular mosaic arrays were evident for each of several darkly reactive retinal components, such as cone inner segments, cone pedicles, and horizontal cells. In the cat and ferret, regular mosaic arrays were also formed by metabolically distinguishable populations of ganglion cells. Ia and IIa ganglion cells (OFF-; Nelson, R., E. V. Famiglietti, Jr., and H. Kolb (1978) J. Neurophysiol. 41: 472-483) were more darkly reactive than the other classes. The darker staining of sublamina a of the inner plexiform layer (OFF-; Famiglietti, E. V., Jr., and H. Kolb (1976) Science 194: 193-195) in the cat and ferret retina, as well as sublamina A' and A1' of the ferret LGN (OFF-; Stryker, M.P., and K.R. Zahs (1983a) J. Neurosci. 3: 1943-1951) suggest that, under typical rearing conditions, the OFF-channels may be metabolically more active than the ON-channels in these species. In Macaca and Saimiri, darker staining was observed in sublamina b of the inner plexiform layer (ON-; Famiglietti, E.V., Jr., and H. Kolb (1976) Science 194: 193-195) and laminae 1, 2, and 6 of the LGN, implying that, under similar rearing conditions, a different pattern is observed. The dark staining of many large retinal ganglion cells, as well as most of the larger LGN neurons (presumed Y/Y-like), in all species studied is evidence that the Y/Y-like pathway is also highly active.
Migration of neurons and formation of laminae in the developing neocortex were studied by means of thymidine autoradiography. Timed pregnant rats received a single pulse injection of [3H]thymidine in the morning of embryonic day (E)13, 14, 15, 16, 17, 18 or 19. Pups were killed on postnatal day (P)0, 1, 2, 3, 4, 6, 10, 30, or 60 and brains were processed for autoradiography. Neurons in posterior (visual) cortical areas labeled by [3H]thymidine administration on E13 or E14 were found predominantly in the cortical subplate; cells labeled on E15 in layer VI; cells labeled on E16 in layers VI and V, cells labeled on E17 in layers V and IV; E18 in layers IV and III; and E19 in layers III and II. By the day of birth (P0), neurons labeled from E13-16 injections were already in their mature laminae in cortex. Many of the cells labeled on E17 were still situated within the cell-dense cortical plate (CP) at P0, and within layer V by P1. Cells labeled on E18 were found in the most superficial part of the CP on P0, in the deep part of the CP on P1, and formed layer IV on P2 and P3. At P0, many E19 labeled cells appeared to be in migration to the cortex and were found in the CP on P1, in layer III by P4, and in layer II by P6. Cells in the auditory cortex labeled by [3H]thymidine injections on a particular day were situated more superficially than comparable labeled cells in the visual cortex, indicating a lateral to medial gradient in which the auditory cortex is formed earlier than the visual cortex. Distributions of labeled cells in the somatosensory cortex were similar to those in the visual cortex. These data provide a detailed and comprehensive description of the position of varied populations of cortical neurons during the early postnatal period, as well as a description of the formation of cortical laminae at times when major systems of afferents are growing into the cortex and making synaptic connections with their target cells.
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