The hierarchical development of monkey visual cortical regions as revealed by the maturation of parvalbumin-immunoreactive neurons

The prefrontal cortex is known to be involved in behavioral paradigms requiring decisions based on short-term working memory, and visually related areas of prefrontal cortex represent the final point in a proposed hierarchical sequence of visual signal processing that begins in primary visual cortex. This study asks if the development of at least certain aspects of the circuitry of each region involved in this hierarchy proceeds in a sequential fashion from primary to higher-order areas. The timing and patterns of expression of immunoreactivity for the calcium-binding protein parvalbumin were examined in areas V1, V2, TE, 7a, and 46 in two series of macaque monkeys ranging in age from embryonic day 132 to adult. The number and laminar distribution of parvalbumin-labeled neurons reached adult levels first in area V1 (primary visual cortex), followed by the adjacent visual association area V2, and then by the higher-order regions of the inferior temporal (TE), posterior parietal (7a) and prefrontal (46) cortices. The appearance of parvalbumin immunoreactivity in the axons of the two major classes of local circuit neurons that express this protein, basket and chandelier cells, followed a similar regional pattern. Furthermore, striking differences were present between these two neuronal populations in the laminar pattern and time course of parvalbumin labeling of their axons. These findings demonstrate that at least some aspects of the intrinsic circuitry of the neocortex mature in accordance with a functional hierarchy of cortical regions. In addition, they illustrate the complexity of cortical development in terms of the different timing of expression of even a single protein in different compartments within single neurons, in different cell types, in different laminae within a region, and across different cortical regions.