Structural and functional maturation of the developing primate brain

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Abstract

Descriptive studies have established that the developmental events responsible for the assembly of neural systems and circuitry are conserved across mammalian species. However, primates are unique regarding the time during which histogenesis occurs and the extended postnatal period during which myelination of pathways and circuitry formation occur and are then subsequently modified, particularly in the cerebral cortex. As in lower mammals, the framework for subcortical-cortical connectivity in primates is established before midgestation and already begins to remodel before birth. Association systems, responsible for modulating intracortical circuits that integrate information across functional domains, also form before birth, but their growth and reorganization extend into puberty. There are substantial differences across species in the patterns of development of specific neurochemical systems. The complexity is even greater when considering that the development of any particular cellular component may differ among cortical areas in the same primate species. Developmental and behavioral neurobiologists, psychologists, and pediatricians are challenged with understanding how functional maturation relates to the evolving anatomical organization of the human brain during childhood, and moreover, how genetic and environmental perturbations affect the adaptive changes exhibited by neural circuits in response to developmental disruption.

Section snippets

Prenatal emergence of the cerebral cortex

The human cerebral cortex is a laminated structure, which in all mammalian species features 3 to 6 layers of cells that are organized to receive information from the environment, mostly through the thalamus, integrate such information within and across functional domains (from 20 to 200 different cortical functional areas), and then send information to other brain centers that generate an appropriate functional response.9 Expansion of the cortex during evolution occurs mostly in the tangential

Structural analysis of postnatal primate brain development

The most detailed assessments of brain development in human beings are from imaging studies in which gray and white matter volumes have been measured over time.52., 53., 54. There is a continuous increase in gray matter from birth and extending through 4 to 5 years of age, followed by a gradual decrease in gray matter (in contrast to white matter) through the third decade. Myelinating white matter tracts grow rapidly after birth and continue in most subcortical tracts through the third decade

General phases of cortical synaptogenesis

As noted above, the subplate receives the first synapses in the developing cerebral wall. At 10 weeks' gestation in the human being, the subplate is a thin zone, with the thickness ratio of the subplate: cortical plate approximately 1:5. There is, however, a remarkable transition that occurs as fiber systems grow into the cortex.37., 43. By 15 weeks, the ratio is dramatically reversed as the subplate becomes less dense cellularly than the cortical plate, but with a thickness ratio of almost

Development of specific neurochemical systems

As noted above, the data regarding the timing of formation and remodeling of synaptic connections in the primate cerebral cortex is based on quantitative analysis of asymmetric synaptic profiles at the ultrastructural level. There is rather limited understanding of the quantitative developmental changes of inhibitory GABAergic connections and other specific neurochemical (neuropeptides, neurotransmitters and neuromodulators) systems in the primate cortex, particularly during postnatal

The mystery of human postnatal brain development

The fields of developmental neurobiology and psychology are faced with understanding the relation between normal alterations in structure with complex function changes that occur in infancy, childhood, and through puberty. This has been difficult, even in experimental models such as the rodent, but the problem seems almost intractable in human development at this time. Whereas different domains of human behavioral development have been described in remarkable detail,99 we lack a detailed

Conclusions

The emergent organization of the primate cerebral cortex is complicated, with different neuronal systems exhibiting distinct developmental trajectories during prenatal and postnatal development. For all systems that have been examined thus far, it appears that an initial, transient organization is followed by structural and molecular reorganization. This remodeling is a hallmark of primate cortical development, starting just before the preterm infant and extending through neonatal and early

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    Supported in part by NIMH grant 45507, NICHD core grant HD15052, and NIDA grant 11165 and the John D, and Catherine T. MacArthur Foundation Research Network on Early Brain Experience and Brain Development.

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