Postnatal Dendritic Growth and Spinogenesis of Layer-V Pyramidal Cells Differ between Visual, Inferotemporal, and Prefrontal Cortex of the Macaque Monkey

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.

The Protracted Maturation of Associative Layer IIIC Pyramidal Neurons in the Human Prefrontal Cortex During Childhood: A Major Role in Cognitive Development and Selective Alteration in Autism

“…Dendritic development and synaptic rearrangement of principal neurons have been extensively studied in the monkey and human prefrontal cortex ( 189 , 190 , 197 , 199 , 204 – 221 ). In the human fetal prefrontal cortex, intensive dendritic growth (second phase) of both deep layer III and V principal neurons, starts 12–15 weeks after they arrived into the cortical plate.…”

“…For most subpopulations of principal neurons in the prefrontal ( 197 , 207 , 208 , 218 , 219 , 221 , 264 , 265 ), and other regions of the human cerebral cortex ( 266 – 276 ) major postnatal dendritic growth occurs during the first year in parallel with massive synaptogenesis ( 185 , 205 , 206 , 226 , 277 – 284 ).…”

Vitamin C Recycling Regulates Neurite Growth in Neurospheres Differentiated In Vitro

“…During the first weeks of postnatal development, cortical neurons undergo dynamic processes of neuronal maturation, such as dendritic spine morphogenesis and synapse formation [ 1 , 2 , 3 ]. On the other hand, astrocytes are formed from radial glial cells (RG) during the last days of embryonic development (E16–E21) and proliferate locally in the cerebral cortex between P2–P14 [ 4 , 5 ].…”

Identification of NeuN immunopositive cells in the adult mouse subventricular zone

“…Using lightly fixed thick brain slices, the fluorescent dye Lucifer Yellow (LY, Thermo Fisher Scientific, Waltham, MA) was injected into single cells under an epi‐fluorescence microscope (Oga, Elston, & Fujita, ). Mice were deeply anesthetized by pentobarbital (50 mg/kg, ip), perfused transcardially with PBS, followed by 4% formaldehyde (FA) in PBS at a volume equal to animal weight, and post‐fixed with the same fixative for 3 hr.…”