Postnatal maturation of the direct corticospinal projections in the macaque monkey.
Postnatal changes in the topography of the multiple corticospinal projections in the macaque monkey were followed using retrogradely transported fluorescent tracers, and related to the monkey's acquisition of manual dexterity; both behavioral and anatomical maturation were completed by about 8 postnatal months. Cortical origins of the corticospinal projections were examined by constructing planar projection maps of the distributions of labeled corticospinal neuron somas; these somas were found only in lamina V. At birth elaborate somatotopically organized corticospinal projections from primary motor cortex (area 4), the mesial supplementary motor area and cingulate areas 23 and 24, area 12, dorsolateral area 6a beta, the dorsolateral and ventral area 6a alpha (area F4), parietal areas 2/5, 7b and the peri-insular cortex (including area SII), were clearly defined, with axons extending to all spinal cord segments. While this pattern of regional projections broadly resembled that of the mature macaque, there were, however, substantial maturational changes during the 8 months after birth. These included (1) a halving of the area of cerebral cortex from which the contralateral corticospinal projection originated and (2) a threefold reduction in the number of labeled corticospinal neurons projecting to all segments of the cord. Collateral elimination rather than neuronal cell death was the likely mechanism for this reduction in the population and areal extent of corticospinal neurons in the maturing macaque. The surviving corticospinal axon terminals also developed substantially during the postnatal period. At birth some terminals had invaded the intermediate zone in each spinal segment, but few had penetrated the dorsal and ventral horns. By 6 postnatal months, however, many corticospinal neurons were retrogradely labeled following the injection of fluorescent labels into each of these spinal zones in cervical and lumbar spinal segments. These data demonstrate a considerable postnatal reduction in corticospinal neurons projecting to the contralateral spinal cord, and imply that many of the axons that are eliminated never synapse on spinal neurons. It is suggested that during the middle fetal period the axons of many of the cortical neurons in lamina V that in the mature monkey will terminate on particular neuron populations in the thalamus, brainstem, or spinal cord, traverse a common pathway down through the internal capsule into the spinal cord, passing close to these successive targets, and possibly forming collaterals at these levels. In the postnatal period each such neuron establishes a stable, effective synaptic input to only one or a few of these subcortical target populations, and the remaining collateral branches regress. The postnatal maturation of corticospinal neurons, examined in this study, is compatible with such a model.
Galea
M P
MP
Department of Anatomy and Cell Biology, University of Melbourne, Parkville, Victoria, Australia.
Darian-Smith
I
I
D000818:Animals; D001522:Behavior, Animal / Q000502:physiology; D001931:Brain Mapping; D002540:Cerebral Cortex / Q000166:cytology / Q000254:growth & development* / Q000502:physiology; D005456:Fluorescent Dyes; D006651:Histocytochemistry; D008252:Macaca fascicularis; D008254:Macaca nemestrina; D009412:Nerve Fibers / Q000502:physiology; D009434:Neural Pathways / Q000166:cytology / Q000254:growth & development / Q000502:physiology; D017729:Presynaptic Terminals / Q000502:physiology; D011597:Psychomotor Performance / Q000502:physiology; D013116:Spinal Cord / Q000166:cytology / Q000254:growth & development* / Q000502:physiology
D005456:Fluorescent Dyes