The occipitoparietal pathway of the macaque monkey: comparison of pyramidal cell morphology in layer III of functionally related cortical visual areas.
The dendritic morphology of pyramidal cells located at the base of layer III in the primary visual area (V1), the second visual area (V2), the middle temporal area (MT), the ventral portion of the lateral intraparietal area (LIPv) and in the portion of cytoarchitectonic area 7a within the anterior bank of the superior temporal sulcus was revealed by injecting neurons with Lucifer Yellow in fixed, flattened slices of macaque monkey visual cortex. These areas correspond to different levels of the occipitoparietal cortical 'stream', which processes information related to motion and spatial relationships in the visual field. The tissue was immunocytochemically processed to obtain a light-stable diaminobenzidine reaction product, revealing the dendritic morphology in fine detail. Retrogradely labelled MT-projecting neurons in supragranular V1 (layer IIIc of Hassler's nomenclature, corresponding to Brodmann's layer IVb) were predominantly pyramidal, although many spiny multipolar (stellate) cells were also found. The average basal dendritic field area of pyramidal neurons in sublamina IIIc of V1 was significantly smaller than that in the homologous layer of V2, within the cytochrome oxidase-rich thick stripes. Furthermore, the average basal dendritic field areas of V1 and V2 pyramidal neurons were significantly smaller than those of neurons in MT, LIPv and area 7a. There was no difference in basal dendritic field area between layer III pyramidal neurons in areas MT, LIPv and 7a. While the shape of most basal dendritic fields was circularly symmetrical in the dimension tangential to the cortical layers, there were significant biases in complexity, with dendritic branches tending to cluster along particular axes. Sholl analysis revealed that the dendritic fields of neurons in areas MT, LIPv and 7a were significantly more complex (i.e. had a larger number of branches) than those of V1 or V2 neurons. Analysis of basal dendritic spine densities revealed regional variations along the dendrites, with peak densities being observed 40-130 microns from the cell body, depending on the visual area. The peak spine density of layer III pyramidal neurons in V1 was lower than that observed in V2, MT or LIPv, which were all similar. Pyramidal neurons in area 7a had the greatest peak spine density, which was on average 1.7 times that found in V1. Calculations based on the average spine density and number of dendritic branches at different distances from the cell body demonstrated a serial increase in the total number of basal dendritic spines per neuron at successive stations of the occipitoparietal pathway. Our observations, comparing dendritic fields of neurons in the homologous cortical layer at different levels of a physiologically defined 'stream', indicate changes in pyramidal cell morphology between functionally related areas. The relatively large, complex, spine-dense dendritic fields of layer III pyramidal cells in rostral areas of the occipitoparietal pathway allow these cells to sample a greater number of more diverse inputs in comparison with cells in 'lower' areas of the proposed hierarchy.
Elston
G N
GN
Department of Physiology and Pharmacology, University of Queensland, Australia.
Rosa
M G
MG
D000818:Animals; D003712:Dendrites / Q000502:physiology; D005456:Fluorescent Dyes; D007150:Immunohistochemistry; D007546:Isoquinolines; D008252:Macaca fascicularis; D009474:Neurons / Q000502:physiology; D009778:Occipital Lobe / Q000166:cytology* / Q000502:physiology; D010296:Parietal Lobe / Q000166:cytology* / Q000502:physiology; D017966:Pyramidal Cells / Q000502:physiology / Q000648:ultrastructure*; D014793:Visual Cortex / Q000166:cytology* / Q000502:physiology; D014794:Visual Fields / Q000502:physiology; D014795:Visual Pathways / Q000166:cytology* / Q000502:physiology
D005456:Fluorescent Dyes; D007546:Isoquinolines; C017475:lucifer yellow