The development of structure and function in the postnatal human cerebral cortex from birth to 72 months: changes in thickness of layers II and III co-relate to the onset of new age-specific behaviors.

HYPOTHESIS: The thickness of a cortical layer is a composite measure of neuronal, axonal, dendritic, synaptic, and glial numbers and sizes that may relate to thefunction of a cortical area.
METHODS: 35 age-specific behaviors with defined cortical localization whose onset lies between birth and 72 months were selected. Each behavior's function localized to one or more of 12 cytoarchitectonic areas (Brodmann areas 4, with homuncular subdivisions for leg, trunk, face, and hand, plus 17, 18, 19, 20, 21, 24, 36, and 37). Data on cortical thickness for each layer of 41 cytoarchitectonic areas (including the 12 above) of the postnatal human cerebral cortex from birth of 72 months were analyzed for general patterns of change. For the 12 cortical areas functionally related to theage-specific behaviors, we searched for layer thickness changes that co-related to when the behaviors began.
RESULTS: Without exception, all layers of the 41 cortical areas of the postnatal human cerebral cortex studied develop through a series of repeated thinning and thickening in a wave-like fashion. With regard to the co-relation of behavioral onset and changes in cortical layer thickness, from birth to 15 months, only layer II has agreater than expected frequency of being the layer with the greatest relative change in thickness (relative to its previous value). From 15 to 72 months, only layer IlI has a greater than expected frequency of being the layer with the greatest absolute change in thickness (81% involved a change in its direction of growth (thinning <--> thickening)). The co-occurrence of directional growth change and having the greatest layer thickness change were only statistically significant for layer III when an age-specific behavior began and was not seen for the 41 cortical areas overall (p = 0.014).
CONCLUSIONS: Cortical laminar development exhibits aprocess that is mathematically consistent with a random walk with drift and with boundaries so that uncontrolled proliferation and pruning are prevented. The directional changes in layer growth could be controlled by feedback coupled with growth promoting and growth inhibiting factors. Layer II, with its function of establishing local corticocortical connections, appears to be most important in establishing age-specific behaviors of infants from birth to 15 months. Such a process tends to produce relatively simpler behaviors. LayerIII, with its function of establishing longer distance corticocortical connections, appears to be most important in establishing age-specific behaviors of children from 15 to 72 months. This process tends to produce richer, more cross-modal behaviors than those mediated primarily by local corticocortical interactions.