Developmental Reorganization of the Human Association Cortex during Perinatal and Postnatal Life

Abstract

The development of synaptic connections (Kostovic et al., 1988; Molliver et al., 1973) and electrophysiological activity of the human cerebral cortex (Dreyfus-Brisac, 1979) begin during the early fetal life, many months before the onset of cognitive cortical functions. However, in this early fetal phase, development of cortical connections is not a dominant neurogenetic event. Other events, such as proliferation, migration of neurons and initial growth of dendrites and axons are main neurogenetic processes in the early fetal human brain. After 13 weeks of gestation begins a new phase characterized by transient arrangement of cortical afferents, synapses, and neurons. The most pronounced pattern of transient organization is present between 22 and 34 weeks of gestation (Kostović, 1990). The behavioral states of the human premature infants change dramatically during this period (Dreyfus-Brisac, 1979; Leijon, 1982; Parmelee, 1975; Prechtl, 1974; Trevarthen, 1979; Wolff and Ferber, 1979). However, the correlative studies of structural and behavioral developmental events should be ihterpreted cautiously since simultaneous ontogenetic emergence may be pure coincidence (Prechtl, 1984). The presence of transient patterns of cortical organization raises the question of their subsequent perinatal and postnatal reorganization. The reorganizational events in the human cerebral cortex extend at least up to the third year of postnatal life (Kostovic, 1990). The reorganization of cortex involves the disappearance of fetal layers (Kostovic, 1990; Kostovic and Rakic, 1990) and cells (Kostovic and Rakic, 1980; Shatz et al., 1988), rearrangements of cortico-cortical fibers (Chalupa and Killackey, 1989; Dehay et al., 1988; Goldman-Rakic, 1982, 1987; Innocenti, 1981, 1982; LaMantia and Rakic, 1990), reduction of synapses (Huttenlocher and de Courten, 1987) and changes in chemical properties of thalamocortical pathways (Kostovic and Goldman-Rakic, 1983; Kostovic and Rakic, 1984). The final phase of cortical maturation occurs during childhood and adolescence and is characterized by the very gradual chemical maturation of associative neurons of layer III (Kostovic, 1990; Kostovic et al., 1988). This late phase of the human cortical development is important for our understanding of cognitive development. This report is concerned with the transformation of transient patterns of cortical organization and maturational changes during the late phase of cortical development. Special attention will be devoted to the developmental changes of circuitry elements (afferents, postsynaptic cells, spines and synapses) in associative cortical areas.