Basal Dendrites of Layer-III Pyramidal Neurons do not Scale with Changes in Cortical Magnification Factor in Macaque Primary Visual Cortex

Abstract

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.

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

“…Given that shrinkage of brain tissue caused by perfusion has been estimated to be small (2.5%; see Oga et al, 2016 ), and any such shrinkage is consistent with previous cell injection studies, the measured values were not corrected for tissue shrinkage. Statistical analyses were performed with Matlab version 2016a (Mathworks, Inc., Natick, MA, USA).…”

“…Data sampled from a specific cortical area/layer in a number of different individuals have been reported for each individual in the galago (Elston et al, 2005 ), the marmoset (cf. Elston et al, 1996 , 1999b ), the South American Agouti (Elston et al, 2006b ) and macaque (Oga et al, 2016 ), revealing highly conserved structure in age/gender/area/layer/topography matched pyramidal cells among individuals. The exception, thus far, is the granular prefrontal cortex where studies in the baboon, vervet monkey and macaque monkey reveal inter-individual variation in pyramidal cell structure among age/gender/area/layer/topography matched pyramidal cell structure not observed in any other cortical region (Elston et al, 2011a —in particular, see Figure 7 ).…”

“…In brief, following overdose with sodium pentobarbital (>75 mg/kg intravenously or intraperitoneally; Dainippon Sumitomo Pharma, Osaka, Japan) animals were perfused intracardially with 0.9% saline in 0.1 M phosphate buffer (pH = 7.2) and then 4% paraformaldehyde in the same phosphate buffer, followed by removal of the brain. Tissue for V1 was taken from the dorsolateral region of the exposed occipital operculum, corresponding to the central 5–7 degrees of visual representation (Figure 1E ; Daniel and Whitteridge, 1961 ; Oga et al, 2016 ). We sampled tissue for inferotemporal cortex from the middle third of the inferior temporal gyrus immediately anterior to the posterior middle temporal sulcus (TE; TEp of Seltzer and Pandya, 1978 ; TEpd of Yukie, 1997 ).…”

“…Care was taken to select the same region within each cortical area from which we sampled layer-III pyramidal cells in our previous studies (Elston et al, 2009 , 2010a ), such that cells included in the present study were located immediately below those sampled in layer III. Pyramidal cells were injected under visual guidance with continuous current (up to 100 nA), and the slices were processed for a light-stable reaction product by immunohistochemistry (Figure 2 ; see Elston and Rosa, 1997 ; Oga et al, 2016 ).…”

Developmental Changes in Pyramidal Cell Morphology in Multiple Visual Cortical Areas Using Cluster Analysis

“…This architecture allows users to query neuronal morphometric parameters by animal species, brain regions, cell types and archive name. We queried the database for the Fujita (Elston et al, 2011;Oga et al, 2016) archive using an R client neuromorphr (Bates et al, 2020) to interact with the API. This dataset consisted of a total of 782 reconstructions that were included for analysis.…”