Abstract
Pyramidal cells in the primate cerebral cortex, particularly those in layer III, exhibit regional variation in both the time course and magnitude of postnatal growth and pruning of dendrites and spines. Less is known about the development of pyramidal cell dendrites and spines in other cortical layers. Here we studied dendritic morphology of layer-V pyramidal cells in primary visual cortex (V1, sensory), cytoarchitectonic area TE in the inferotemporal cortex (sensory association), and granular prefrontal cortex (Walker's area 12, executive) of macaque monkeys at the ages of 2 days, 3 weeks, 3.5 months, and 4.5 years. We found that changes in the basal dendritic field area of pyramidal cells were different across the three areas. In V1, field size became smaller over time (largest at 2 days, half that size at 4.5 years), in TE it did not change, and in area 12 it became larger over time (smallest at 2 days, 1.5 times greater at 4.5 years). In V1 and TE, the total number of branch points in the basal dendritic trees was similar between 2 days and 4.5 years, while in area 12 the number was greater in the adult monkeys than in the younger ones. Spine density peaked at 3 weeks and declined in all areas by adulthood, with V1 exhibiting a faster decline than area TE or area 12. Estimates of the total number of spines in the dendritic trees revealed that following the onset of visual experience, pyramidal cells in V1 lose more spines than they grow, whereas those in TE and area 12 grow more spines than they lose during the same period. These data provide further evidence that the process of synaptic refinement in cortical pyramidal cells differs not only according to time, but also location within the cortex. Furthermore, given the previous finding that layer-III pyramidal cells in all these areas exhibit the highest density and total number of spines at 3.5 months, the current results indicate that pyramidal cells in layers III and V develop spines at different rates.
Highlights
Layer-III cells in area TE can grow an average of 10,400 spines by 3.5 months, and those in area 12 as many as 15,900, and in both cases there is a net increase in the number of spines between birth and adulthood (Elston et al, 2009, 2010a)
We studied the basal dendritic tree morphology of layer-V pyramidal cells in V1, cytoarchitectonic area TE, and Walker’s area 12 in macaque monkeys that ranged in age from 2 days to 4.5 years
Cells: Comparison between Layer V and Previously, we showed that basal dendritic field area of layerIII pyramidal cells in area TE and area 12 increased with age, whereas those of V1 cells decreased (Figure 8B)
Summary
Pyramidal cells in the primate cerebral cortex are characterized by different rates of growth and atrophy of both their dendrites and spines during development, resulting in marked phenotypic variation in their cellular structure among different areas in the mature brain (Elston et al, 1996, 2009, 2010a,b, 2011b; Elston and Rosa, 1997, 1998; Jacobs et al, 1997, 2001; Petanjek et al, 2008, 2011; Amatrudo et al, 2012; Bianchi et al, 2013). In some cortical areas, such as macaque primary visual cortex (V1), the basal dendritic trees of layer-III pyramidal cells grow to their full extent around birth, become successively smaller through infancy, adolescence, and adulthood (Boothe et al, 1979; Elston et al, 2009, 2010a). Layer-III cells in area TE can grow an average of 10,400 spines by 3.5 months, and those in area 12 as many as 15,900, and in both cases there is a net increase in the number of spines between birth and adulthood (Elston et al, 2009, 2010a)
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