Quantitative description of synaptogenesis in several cortical areas sampled from the same cerebral hemisphere of a series of developing macaque monkeys revealed a remarkably similar course of synaptogenesis during phase 3 in two sensory (visual and somatic), one motor, and one limbic cortical area (Rakic et al., 1986; Granger et al., 1995). Similarly rapid and synchronous accretion of both excitatory and inhibitory synapses have also been found during phase 3 in layer III of the prefrontal cortex of the macaque (Anderson et al., 1995). It has generally been implied, and we also had assumed, based in part on the classical studies of myelin staining in the developing human cerebrum, that the neocortex develops in a distinct hierarchical order, from the sensory to motor to association areas (Flechsig, 1920). Therefore, our initial finding of the concurrent acquisition of synapses in functionally diverse and anatomically separated areas of the cerebrum was unexpected (Rakic et al., 1986). In the past decade, however, additional evidence for concurrent development has been gained from brain imaging studies of the maturation of metabolic activity in the macaque cortical mantle (Jacobs et al., 1995) and the human cerebrum (Chugani, Phelps, and Mazziotta,
1987). Furthermore, quantitative studies of the presence of neurotransmitter receptors in the cortex (Lidow, Goldman-Rakic, and Rakic, 1991; Lidow and Rakic, 1992) also reveal identical profiles of receptor density within the range of human biological variation. Recently, Shan-kle et al. (1998) reanalyzed the classical cytoarchitectonic studies of Conel and concluded that the differentiation of a variety of morphological and laminar features are remarkably similar across cortical areas, and that developmental patterns in many cortical areas are not distinguishable from one another. Finally, the first two phases of synaptogenesis were also recently found to be synchronous across cortical areas in the human embryo, as they are in the macaque (Zecevic, 1998).
Although the rate of decline to adult levels in phase 4 varies in different areas, this phase of high synaptic density also exhibits an overlap in timing across the cortical regions (Rakic, Bourgeois, and Goldman-Rakic, 1994). We have suggested that this overlap may be essential for competitive interactions and the validation of synaptic connections during experience-dependent development. It should be pointed out that not all evidence is supportive of concurrent synaptogenesis, however. In particular, Huttenlocher and Dabholkar (1997) have reported that during the ascending phase of synaptogenesis in the human brain (phase 3 in macaque), the prefrontal association cortex appears to acquire synaptic junctions more slowly than in the primary visual and auditory cortices. This finding has appeal in its concordance with the general notion that executive functions based on language appear to mature latest in development. We have discussed the technical issues related to this conclusion in considerable detail in several previous publications (Rakic, Bourgeois, and Goldman-Rakic, 1994; Goldman-Rakic, Bourgeois, and Rakic, 1997). At present, neither the sample size (due to scarcity of human tissue) nor the magnitude of the effect is sufficient to challenge the idea of concurrent synaptogenesis.
togenesis Studies in human infants show that virtually all cortical functions, including language, have anlage in early infancy and do not arise de novo at a late stage of maturation. In humans, evoked activity in response to the maternal voice is present even before birth (Lecanuet and Granier-Deferre, 1993), and the development of visual acuity and depth perception begins in newborn infants (Teller, 1997, and chapter 6 of this volume). Human infants also evidence expectations based on auditory and visual stimuli that depend on the association cortex. Human infants also show competence to represent numerical entities, including action sequences
(for review, see Wynn, 1998). In the macaque, likewise, early signs of competencies that will later be fully developed are already in evidence. Thus, adult-like properties of neurons in the inferotemporal cortex, such as selective responses to face recognition, are present at only a few weeks after birth (Rodman, Gross, and Scalaidhe, 1993; Rodman, 1994). The critical periods for obtaining social skills and learning simple discriminations also take place as early as two months after birth in macaque infants (Harlow and Harlow, 1962). The cognitive process of working memory, which is subserved by the dor-solateral prefrontal association cortex, likewise emerges in monkeys soon after birth and before the end of phase 3 (Diamond and Goldman-Rakic, 1989), when basic synaptoarchitectonic features are still being laid down (Bourgeois, Goldman-Rakic, and Rakic, 1994; Goldman-Rakic, Bourgeois, and Rakic, 1997; Goldman-Rakic, 1987). Although monkeys obviously do not possess language, they do have specializations for working memory processes that are common to all informational domains, and are considered essential for language competence (e.g., Baddeley, 1986; Just and Carpenter, 1992; King and Just, 1991; Miyake, 1994).
Based on our own data and consideration of the literature, we have proposed that the integration of sensory, motor, limbic, and associative areas occurs pari passu with the structural development of the cortex as a unified structure, i.e., as "whole cloth" (Goldman-Rakic, Bourgeois, and Rakic, 1997). Further, we would argue that the level and complexity of processing advances with each progressive stage of development. Our working hypothesis is that concurrent synaptogenesis in the whole cortical mantle during the rapid phase 3 allows the early coordinated emergence of all cortical functions (Rakic, Bourgeois, and Goldman-Rakic, 1994; Rakic et al., 1986). In agreement with others, we would argue that concurrency is essential for the competitive and selective interactions among the very heterogeneous cortical inputs arriving at each point of the cortex (e.g., Changeux and Danchin, 1976; Katz and Shatz, 1996; Antonini and Stryker, 1998). However, full maturation of cortical functions is a protracted process that may require many years to be achieved in the macaque (Goldman-Rakic, Bourgeois, and Rakic, 1997) and more than a decade in the human (Rakic, Bourgeois, and Goldman-Rakic, 1994; Huttenlocher and Dab-holkar, 1997).
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