Sequences of CNS myelination

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Historically, in elucidating the factors that determine the topographical and chronological sequences of CNS myelination, the process of myelination has been considered relative to the development of human behavior. This approach resulted in the analysis of the sequence of myelination in terms of relationships among anatomic systems associated with different functions. Yakovlev and Lecours (1967) held that the myelination proceeds along a hierarchy of increasingly complex CNS functions ending in the maturation of association and intracortical fibers critical to the highest intellectual functions, and that myelination represents the anatomic correlate of neurophysiological maturation. Functionally related systems myelinate together, and the timing of myelination reflects the position of the fiber system in the hierarchy of the functional organization of the developing nervous system. They referred to the temporal aspect of myelination in a fiber system, from its onset to completion, as its myelogenetic cycle and observed that this cycle may have an early or late onset with a rapid or slow course. Different sites not only begin myelination at different times, but also progress to maturation over different time intervals (Kinney et al., 1994; Yakovlev and Lecours, 1967). The early onset of myelination does not predict early myelin maturation (Kinney et al., 1988; Yakovlev and Lecours, 1967).

Myelin sheaths appear in the motor root fibers of the spinal nerves at the end of the fourth fetal month, while the sensory fibers begin to myelinate at the end of the fifth month. The motor nerve roots reach their adult pattern of myelination at about term while the sensory nerve rootlets continue to myelinate for several months after birth. Among the cranial nerves, the roots of the eighth pair are the first to show myelinated fibers. At the end of the fifth fetal month, the roots of both divisions of the eighth nerve are myelinated. The oculomotor nerves (III, IV, VI) and the motor division of the trigeminal nerve myelinate next, at about the same time. As in the spinal roots, the cranial motor roots seem to myelinate at a faster pace than the sensory roots. The cycle of myelination of the cranial nerve roots appears to be completed early in the first postnatal year.

Except for the dorsal root fibers in the posterior columns of the spinal cord, there are no myelinated fibers in the CNS before the end of the fifth fetal month. In the brain, the vestibulocochlear system of fibers is the first to demonstrate myelination, having not only an early beginning but also a very short cycle of myelination. The fibers of this system in the brainstem complete the cycle of myelination at about the middle of the ninth fetal month, and from the sixth fetal month to term they dominate the myelin-staining preparations of the brainstem.

The cycles of myelination of the inferior, middle, and superior cerebellar peduncles exhibit remarkable differences. The inner, vestibulocerebellar division of the inferior cerebellar peduncle begins to myelinate early in the sixth fetal month and attains an adult pattern of myelination by the end of eighth fetal month. The cycle of the inner division is about the same as that of the vestibulocochlear system. In sharp contrast, the outer division, containing spino-, olivo- and reticulocerebellar fibers, shows no myelinated fibers until the eighth fetal month and thereafter continues to myelinate until about the third postnatal month; its cycle is long and comparable to that of the medial lemniscus. Myelination of the superior cerebellar peduncles begins in the eighth fetal month, approximately 6 weeks later than the inner division of the inferior peduncle but before myelinated fibers are present in the outer division of this peduncle. In comparison with the superior and inferior peduncles, the middle cerebellar peduncles demonstrate the most protracted cycle of myelination. Myelinated fibers in the transverse bundles of the pons appear only during the first postnatal month, and myelination extends into the middle cerebellar peduncles during the second postnatal month. The pontocerebellar fibers continue to gain slowly in intensity of myelination at least until the fourth postnatal year.

In man the reticular formation of the brainstem exhibits a very long cycle of myelination and, in this respect, matches the protracted cycle of myelination in the commissural and association fiber systems of the telencephalon.

In the supratentorial brain, no myelinated fibers are encountered before the seventh fetal month. Early in the seventh month the first myelinated fibers appear in the fasciculus habenulointerpeduncularis, which myelinates rapidly and completes its cycle of myelination before term. In the last trimester intense myelination occurs in the subthalamic region, thalamus, and pallidum.

The brachia of the inferior colliculi and the medial geniculate nuclei are among the earliest extrinsic thalamic afferents to myelinate. They begin to myelinate in the seventh fetal month, well in advance of the terminal fibers of the medial lemniscus and optic tract, and complete the cycle at about the fourth postnatal month. The contrast between early myelination of the acoustic and late myelination of the optic colliculi is noteworthy. Myelination of the optic nerves and tracts, of the superior colliculi and their brachia, and of the lateral geniculate nuclei begins late in the ninth fetal month. However, the optic system, as a whole, completes the cycle rapidly near the third postnatal month. By the middle of the eighth fetal month, the myelinated fibers of the medial lemniscus reach their thalamic nuclei. Their myelination is complete by the eighth postnatal month. The reticulum and the intrinsic fibers of the thalamus myelinate at a slower pace.

Myelination of thalamocortical radiations is related to the thalamic nucleus involved and has been described in terms of so-called "specific" and "nonspecific" tha-

lamic nuclei. Projections from the specific nuclei of the basal complex (or "relay" nuclei) myelinate earlier and exhibit a shorter cycle than do projections from the nonspecific nuclei of the anteromedial and dorsal complex. Among the specific thalamic projections, the optic radiations to the primary visual cortex of the occipital lobe exhibit the shortest cycle of myelination, beginning late in the first postnatal month and reaching maturity about the fourth postnatal month. Myelination of the projections from the ventrobasal complex of the thalamic nuclei to the postcentral cortex appears in the lenticulothalamic region of the posterior limb of the internal capsule at the end of the ninth month and during the tenth month rapidly extends into the core of the postcentral gyrus; but, in contrast to the optic radiations, these projections seem to complete the cycle only at about the first postnatal year. Myelination of the acoustic radiations from the medial geniculate to Heshl's gyrus in the temporal lobe and from the latero-ventral complex to the precentral cortex of the frontal lobe exhibits a still longer cycle, which is completed at about 4 years of age. It is also noteworthy that myelination of the cortical end of the acoustic system in the temporal lobe is protracted beyond the first postnatal year, in sharp contrast to the visual system, which myelinates rapidly soon after birth in one short spurt from retina to its end about the calcarine fissure.

The first myelinated fibers in the internal capsule appear in the ninth fetal month in the lenticulothalamic sector of the posterior limb. From the ninth fetal month to the fourth postnatal month, the myelination spreads fanwise posteriorly into the retrolenticular sector of the posterior limb and, much more slowly, anteriorly into the anterior limb. The thalamocortical radiations reach the postcentral cortex (somesthetic area) during the first postnatal month, and later appear in the precentral gyrus (propriokinesthetic area). During the first postnatal month there is also a spurt of myelination of the corticofugal fibers from the postcentral and the precentral cortices. Myelination of the fibers in the anterior limb of the internal capsule lags behind that of the posterior limb but accelerates from the fourth postnatal month, and by the eighth month is similar to that of the posterior limb.

Myelination of the pyramidal tract is synchronized closely with that of specific thalamocortical projections from the ventrobasal complex of thalamic nuclei. Myelination of the pyramidal tract fibers appears first at the pontine level and spreads cephalad into the cerebral peduncles and internal capsule and caudad into the bulbar pyramids. Below the pons, fibers of the bulbar pyramids complete their myelination cycle at about 1 year. Of all the long descending transcapsular tracts, the corticopontine tracts myelinate latest and longest. The cycle of myelination of the corticopontine tracts appears to be synchronized with the cycle of myelination of the nonspecific thalamocortical projections from the medial dorsal and pulvinar nuclei.

In the white matter of the telencephalon, myelination of the long association and commissural fiber systems is protracted, lasting until at least the end of the first decade of life. The commissural fibers in the splenium of the corpus callosum and forceps major begin to myelinate at about the fourth postnatal month. Myelination spreads gradually and slowly from the splenium toward the genu, the rostrum, and forceps minor of the corpus callosum. From pathologic studies, myelination of commissural fibers in the corpus callosum seems to continue slowly even after the first decade. The intra-cortical neuropil of the anterolateral convexity of the frontal lobes, of the inferior parietal lobes, and of the basolateral convexity shows even longer myelination cycles.

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