Development of prestriate visual projections in the monkey and human fetal cerebrum revealed by transient cholinesterase staining

Abstract

Cholinesterase (ChE) staining was used to reveal the timing and pattern of development of afferents to the prestriate visual cortex (areas 18, 19, 20, and 21 of Brodmann) in a series of developing human and monkey fetal brains. This investigation was possible because the nucleus pulvinaris of the thalamus, the main source of subcortical projections to the prestriate cortex, displays positive reactivity after thiocholine incubation during the last three quarters of gestation, while neighboring thalamic nuclei that project to the adjacent neocortical areas are unstained. Staining of the pulvinar and its prestriate projections passes through six broad stages. Stage I begins in both species at the end of the first third of gestation. Positively stained fibers originate from the pulvinar and enter but do not extend beyond the hemispheric stalk. During stage II, pulvinar axons gradually invade the intermediate zone of the occipital lobe, and in stage III they reach the level of the subplate zone. In stage IV, which occurs around mid-gestation in both species, cholinesterase-positive fibers accumulate within the subplate zone subjacent to the developing prestriate cortex. During stage V, ChE-positive fibers penetrate the prospective prestriate cortex but do not yet form the alternating columnar pattern characteristic of pulvinar input to this area in the adults. Rather, ChE activity is concentrated in two continuous bands situated within prospective layers III-IV and VI; also a narrow band is visible in upper layer I. In stage V a clear histochemical border forms between prestriate and striate areas with ChE activity in prospective area 17 limited mostly to the superficial strata of layers I and II. This histochemical differentiation precedes the emergence of cytoarchitectonic landmarks. During stage VI, which begins in the last fifth of gestation in both species, the pulvinar become progressively less stainable and its projections can no longer be traced by ChE histochemistry.

Unique profiles of the alpha 1-, alpha 2-, and beta-adrenergic receptors in the developing cortical plate and transient embryonic zones of the rhesus monkey

“…It should be noted, however, that since in the present study we examined only the high-affinity cu2 sites it is possible that a much closer correlation can be achieved when the entire population of ot2 receptors is taken into consideration. In contrast to the a2 receptors, the laminar patterns of otl and 0 sites do not correlate well with the distribution of any specific afferents to the occipital cortex of the developing or adult monkey (Kostovic and Rakic, 1984;Lund and Yoshioka, 1991). There is also no correspondence between the laminar distribution of noradrenergic innervation of areas 17 and 18 (Foote and Morrison, 1984;Morrison and Foote, 1986) and that of adrenergic receptor subtypes (individually or combined) in the adult or developing rhesus monkeys.…”

“…In addition, the developmental changes in the distribution of cu2 sites in area 17 do not precisely follow the developmental changes in the distribution of terminals from the parvocellular portion of the geniculocortical projections. Finally, although the developmental changes in the distribution of a2 receptors in area 18 can be correlated with the changes in the pattern of the pulvinar innervation (Kostovic and Rakic, 1984) there is a lag of nearly 30 d before the receptor distribution follows that of the innervation. For example, pulvinar terminals are found predominantly in layers I, III, IV, and VI at El00 (Kostovic and Rakic, 1984) while the 012 receptors begin to concentrate in the same layers only between El43 and birth.…”

“…Finally, although the developmental changes in the distribution of a2 receptors in area 18 can be correlated with the changes in the pattern of the pulvinar innervation (Kostovic and Rakic, 1984) there is a lag of nearly 30 d before the receptor distribution follows that of the innervation. For example, pulvinar terminals are found predominantly in layers I, III, IV, and VI at El00 (Kostovic and Rakic, 1984) while the 012 receptors begin to concentrate in the same layers only between El43 and birth. By that developmental age, the pulvinar innervation of area 18 had already changed to adult distribution, with axonal terminals concentrating in layers I, III, and IV (Benevento and Rezak, 1976).…”

“…In E65-E93 specimens, the border between areas 17 and 18 cannot be distinguished on the basis of the cytoarchitectonic criteria. Thus, for these ages, the cortical areas were identified according to position in the occipital lobe (Kostovic and Rakic, 1984).…”

Maturation of Cerebral Connections and Fetal Behavior

“…However, a new connectivity framework for possible functional involvement of the cerebral cortex develops during the midfetal period (15-20 WPC) due to concurrent increase in number of synapses 9,14 and thalamocortical afferents 14,[40][41][42] in the subplate zone 19,21,23 as well as the parallel development of efferent cortical pathways. 43 During the midfetal period, thalamocortical afferents which convey somatosensory information are still waiting within the subplate zone and did not reach their synaptic targets in the cortical plate.…”