Neocortical pyramidal cells are characterized by markedly different structure among cortical areas in the mature brain. In the ventral visual pathway of adult primates, pyramidal cells become increasingly more branched and more spinous with anterior progression through the primary (V1), second (V2), and fourth (V4) visual areas and cytoarchitectonic areas TEO and TE. It is not known how these regional specializations in neuron structure develop. Here, we report that the basal dendritic trees of layer III pyramidal cells in V1, V2, V4, TEO, and TE were characterized by unique growth profiles. Different numbers of spines were grown in the dendritic trees of cells among these cortical areas and then subsequently pruned. In V1, V2, and V4, more spines were pruned than grew resulting in a net decrease in the number of spines in the dendritic trees following the onset of visual experience. In TEO and TE, neurons grew more spines than they pruned from visual onset to adulthood. These data suggest that visual experience may influence neuronal maturation in different ways in different cortical areas.

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Pyramidal cells grow and mature at different rates among different cortical areas in the macaque monkey. In particular, differences across the areas have been reported in both the timing and magnitude of growth, branching, spinogenesis, and pruning in the basal dendritic trees of cells in layer III. Presently available data suggest that these different growth profiles reflect the type of functions performed by these cells in the adult brain. However, to date, studies have focused on only a relatively few cortical areas. In the present investigation we quantified the growth of the dendritic trees of layer III pyramidal cells in the anterior ventral portion of cytoarchitectonic area TE (TEav) to better comprehend developmental trends in the cerebral cortex. We quantified the growth and branching of the dendrities, and spinogenesis and pruning of spines, from post-natal day 2 (PND2) to four and a half years of age. We found that the dendritic trees increase in size from PND2 to 7 months of age and thereafter became smaller. The dendritic trees became increasingly more branched from PND2 into adulthood. There was a two-fold increase in the number of spines in the basal dendritic trees of pyramidal cells from PND2 to 3.5 months of age and then a 10% net decrease in spine number into adulthood. Thus, the growth profile of layer III pyramidal cells in the anterior ventral portion of the inferotemporal cortex differs to that in other cortical areas associated with visual processing.

Neurons in the mammalian primary visual cortex (V1) are systematically arranged across the cortical surface according to the location of their receptive fields (RFs), forming a visuotopic (or retinotopic) map. Within this map, the foveal visual field is represented by a large cortical surface area, with increasingly peripheral visual fields gradually occupying smaller cortical areas. Although cellular organization in the retina, such as the spatial distribution of ganglion cells, can partially account for the eccentricity-dependent differences in the size of cortical representation, whether morphological differences exist across V1 neurons representing different eccentricities is unclear. In particular, morphological differences in dendritic field diameter might contribute to the magnified representation of the central visual field. Here, we addressed this question by measuring the basal dendritic arbors of pyramidal neurons of layer-IIIC and adjoining layer III sublayers (in the Hassler’s nomenclature) in macaque V1. We labeled layer-III pyramidal neurons at various retinotopic positions in V1 by injecting lightly fixed brain tissue with intracellular dye, and then compared dendritic morphology across regions in the retinotopic map representing 0–20° of eccentricity. The dendritic field area, total dendritic length, number of principal dendrites, branching complexity, spine density and total number of spines were all consistent across different retinotopic regions of V1. These results indicate that dendrites in layer-III pyramidal neurons are relatively homogeneous according to these morphometric parameters irrespective of their locations in this portion of the retinotopic map. The homogeneity of dendritic morphology in these neurons suggests that the emphasis of central visual field representation is not attributable to changes in the basal dendritic arbors of pyramidal neurons in layer III, but is likely the result of successive processes earlier in the retino-geniculo-striate pathway.

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