Differential distribution of parvalbumin-immunoreactive pericellular clusters of terminal boutons in developing and adult monkey neocortex

Abstract

Basket cells are GABAergic inhibitory interneurons and known regulators of pyramidal cells, the major class of excitatory neurons in neocortex. Parvalbumin (PV), a calcium binding protein, has been colocalized with GABA in cortical neurons ( Celio, 1986. Science 231: 995–998 ) and has been reported to be present in the terminal boutons of basket neurons forming pericellular clusters in monkey neocortex ( Hendry et al. 1989. Exp. Brain Res. 76: 467–472 ). In this study, we used immunohistochemical methods to evaluate the regional and laminar distributions of PV-immunoreactive (PV-IR) pericellular clusters of terminal boutons in the neocortex of neonatal, infant, adolescent, and adult rhesus monkeys. PV-IR pericellular clusters were composed of labeled terminal boutons that outlined the somata and proximal dendrites of large pyramidal neurons in layers III and V of primary motor cortex, layers V and VI of primary visual cortex, and layer V of visual association cortex (area 18). This laminar pattern was present in neonatal animals and did not change with age in motor cortex. However, in the visual regions of adolescent and adult animals, such PV-IR structures were not detected. PV-positive pericellular clusters were not observed in the prefrontal cortex at any age. The pattern of distribution of PV-containing pericellular clusters paralleled that of a subpopulation of pyramidal neurons containing nonphosphorylated neurofilament proteins (NFP); double labeling studies confirmed that a sub-group of NFP-positive pyramidal neurons were the targets of PV-IR pericellular clusters. The distribution of PV-IR pericellular clusters was compared to that of PV-IR terminal boutons of another class of interneurons, the chandelier cells. Terminal boutons of chandelier neuron axons align in vertical rod-like structures known as cartridges. Subpopulations of chandelier axon cartridges have been previously shown to be PV-IR and their distribution in visual and prefrontal cortices has been described (DeFelipe et al. 1989. Brain Res. 503: 49–54; Lewis and Lund. 1990. J. Comp. Neurol. 293: 599–615). These two types of structures composed of PV-IR terminal boutons tended to be present in different laminae in all regions and ages examined, except in layer III of primary motor cortex where both PV-IR pericellular clusters and chandelier cartridges were found. These findings indicate that in monkey neocortex PV immunoreactivity is present in pericellular clusters of terminal boutons that are likely to arise from basket cells. The differential regional, laminar and developmental patterns of PV immunoreactivity in these structures may reveal their unique pyramidal cell targets and provide insight into their functional roles in monkey neocortex.