Pyramidal cells in prefrontal cortex of primates: marked differences in neuronal structure among species

Abstract

The most ubiquitous neuron in the cerebral cortex, the pyramidal cell, is characterized by markedly different dendritic structure among different cortical areas. The complex pyramidal cell phenotype in granular prefrontal cortex (gPFC) of higher primates endows specific biophysical properties and patterns of connectivity, which differ from those in other cortical regions. However, within the gPFC, data have been sampled from only a select few cortical areas. The gPFC of species such as human and macaque monkey includes more than 10 cortical areas. It remains unknown as to what degree pyramidal cell structure may vary among these cortical areas. Here we undertook a survey of pyramidal cells in the dorsolateral, medial, and orbital gPFC of cercopithecid primates. We found marked heterogeneity in pyramidal cell structure within and between these regions. Moreover, trends for gradients in neuronal complexity varied among species. As the structure of neurons determines their computational abilities, memory storage capacity and connectivity, we propose that these specializations in the pyramidal cell phenotype are an important determinant of species-specific executive cortical functions in primates.

Keywords: baboon; cognition; connectivity; guenon; human; macaque; primate; spine.

Figure 1

Schematic illustrating some different interpretations of the number, size, and location of cortical areas in prefrontal cortex of the macaque monkey. (A) Modified from Walker (1940), (B) Petrides and Pandya (1999) and (C) Preuss and Goldman-Rakic (1991a).

Figure 2

Schematic illustrating where neurons were sampled (dots) in the dorsolateral, medial, and orbital prefrontal cortex of the macaque monkey (A), vervet monkey (B), and baboon (C).

Figure 3

Schematic illustrating how the study of pyramidal cell morphology in the transverse plane may bias for uniformity in structure. Illustrated are two cells sampled from the primary visual area (V1) and granular prefrontal cortex (gPFC) of the macaque monkey. At left are the basal dendritic trees of the two cells as seen in the tangential plane. In black is the part of the dendritic tree that would be seen in a 50-μm transverse section (of the type used in many Golgi studies). The portion of the dendrites extending beyond the section is illustrated in gray. Note the relative similarity in structure of the part of the dendritic tree revealed in the 50-μm transverse sections. At right are illustrated the dendrograms of each of the two cells, which resulted from reconstruction of the complete basal dendritic tree as seen in the tangential plane. Based on our observations, transverse sections would have to be of the order of 1 mm thick to include all dendrites (e.g., human temporal lobe; Elston et al., 2001).

Figure 4

(A–C) Low power photomicrographs of Lucifer Yellow-injected layer III pyramidal cells in tangential sections taken from the granular prefrontal cortex of the macaque monkey (area 12vl). (D–H) Higher power photomicrographs of these same neurons as viewed through a ×100 oil-immersion Zeiss objective, revealing aspects of their fine structure including dendritic spines. Scale bar = 100 μm in (A–C) and 20 μm in (D–H).

Figure 5

Frequency histograms and plots of the (A) size, (B) branching patterns, (C) spine density of the basal dendritic trees, and (D) cell body size, of layer III pyramidal neurons sampled in granular prefrontal cortex of the macaque monkey (M1 and M2), vervet monkey (VM1 and VM2) and baboon (B1 and B2). Error bars =  standard errors.

Figure 6

Plots of our estimates of the total number of dendritic spines in the basal dendritic tree of the “average” layer III pyramidal cell in visual, sensorimotor, cingulate, and prefrontal cortex of the macaque monkey, vervet monkey, and baboon. Note the remarkable similarity in the trends of these estimates in visual, sensorimotor, and limbic cortex of both animals. Note, however, the differences in these estimates in the granular prefrontal cortex among species. V1 = primary visual, V2 = second visual, V4 = fourth visual, 3b = primary somatosensory, 1/2/5/7 = somatosensory association, 4 = primary motor, 6 = premotor, 23 = posterior cingulate, 24 = anterior cingulate, 9/10/12/13/46 = prefrontal areas, 32 = cingulate.

Figure 7

Plots of our estimates of the total number of dendritic spines in the basal dendritic tree of the “average” layer III pyramidal cell in visual, somatosensory, motor, limbic, and prefrontal cortex of the vervet monkey. Sampling from the same cortical regions in the two animals (stylized at top right) resulted in remarkably similar trends in these estimates in visual, somatosensory, motor, and limbic cortex of both animals (top right). In granular prefrontal cortex (gPFC), however, we found unprecedented differences in our estimates of the total number of dendritic spines in the basal dendritic tree of the “average” layer III pyramidal cell among cortical areas (bottom left), despite standardizing the regions sampled between cases (bottom right). V1 = primary visual, V2 = second visual, V4 = fourth visual, 3b = primary somatosensory, 1/2/5/7 = somatosensory association, 4 = primary motor, 6 = premotor, 23 = posterior cingulate, 24 = anterior cingulate, 9/10/12/13/46 = prefrontal areas, 32 = cingulate.