The linear organization of cell columns in human and nonhuman anthropoid Tpt cortex

Abstract

Neurons in the cerebral cortex are organized horizontally into laminae and vertically into columns and modules. Little is known about the structural variation of neuronal organization in the vertical (pia to white matter) dimension. We describe here a new computer-assisted methodology that quantifies the linear arrangement of cells and shows how cortical columns in a homologous region differ by species and age. Perikarya in eulaminate temporal cortex, Tpt, were segmented from the background on the basis of their optical densities and sizes in human, rhesus (Macaca mulatta), and chimpanzee (Pantroglodytes) brains. Within each lamina, the two-dimensional arrays of neurons were divided into repetitive, objectively defined vertical clusters. Following this, ratios and indices quantified the displacement of perikaryal centroids from the central axis and from the center point in each cell cluster. The extremely linear and vertical arrangement of cells in the prelaminated fetal cortical plate served as the template to which the other arrays were compared. In all species, the linear arrangements of perikarya in lamina III, and to a lesser extent, in lamina V, closely resemble that of the early fetal template, whereas perikaryal arrangements in layers II and IV diverge from the template formation. Corroborating subjective visualization, each lamina had its own 'fingerprint'. As expected, cell density is less in the species with larger brains, with most of the differences in density coming from increased spacing between cellular columns rather than among the cells within columns. Not all aspects of perik-aryal organization alter when bigger brains are compared with smaller ones. Although chimpanzee brains are about four times bigger than those of rhesus monkeys and human brains are about three times larger than chimpanzee brains, absolute measures of cellular linearity in chimpanzees and rhesus monkeys resemble each other more closely than the same measures do in humans and chimpanzees. After accounting for differences in interval widths, the parameters of linearity sorted on the basis of brain weight in pyramidal cell layers III and V, but not in the stellate cell layers II and IV. Human perikarya have the widest horizontal dispersion and this displacement is most pronounced in layer II, least in layer III.

Description of microcolumnar ensembles in association cortex and their disruption in Alzheimer and Lewy body dementias

“…The size and shape of these anatomically defined microcolumnar ensembles resembles the size and shape of ''neuronal domains,'' which are functionally defined 50-m-wide by 200-m-tall regions, recognized by using optical recordings of neuronal populations labeled with calcium-sensitive indicators (33). Computer-assisted analysis led Buxhoeveden et al to conclude that there were structures of size 34 m wide by 400 m tall in layer III of the Tpt area in both nonhuman primates and humans (2). The exact relationship between the microcolumnar ensembles we describe here and these other anatomical and functional units remains to be determined.…”

“…A natomical investigations into the organization of cortical structure have relied on tools similar to those used by the great neuroanatomists of the 19th and early 20th centuriesnamely, an appreciation of neuronal size and packing density in lamina, supplemented by information from electrophysiology and tract tracing experiments (1)(2)(3)(4)(5)(6)(7)(8)(9). These studies have revealed a somewhat dichotomous view of cortical architecture: an anatomical appreciation of a classic six-layered organization of neocortex and a neurophysiological recognition that functional units frequently reflect a vertical pattern of organization.…”

The Minicolumn and Evolution of the Brain

“…Then too, minicolumns differ from rigidly defined structures such as the planum temporale or corpus callosum; they are less tangible, comprising a variety of different components, only some of which are detectable in any given tissue stain or preparation. Researchers have variously defined the 'anatomical' minicolumn according to cell soma [Krmpotic-Nemanic et al, 1984;Schlaug et al, 1995;Buxhoeveden et al, 1996;Buldyrev et al, 2000], apical dendrite bundles [Peters and Sethares, 1991;Peters and Yilmaz, 1993], myelinated bundles [Peters and Sethares, 1996], and double bouquet axon bundles [De Felipe et al, 1990].…”

“…This area, called the peripher- Table 1. Anatomical indicators of vertical organization 1 Cell soma -methods for detection a Cell density based on light microscopy and computer imaging [Schlaug et al, 1995;Buxhoeveden et al, 1996;Buldyrev et al, 2000]. b Patterns of cell location: Periodicity in GABAergic neurons [Schwartz et al, 1988].…”

Lateralization of Minicolumns in Human Planum temporale Is Absent in Nonhuman Primate Cortex

“…Therefore, lateralization differences at the macroscopic level might not accurately reflect microscopic distinctions. Columnar organization is a common feature of mammalian cortical anatomy, yet column structure varies across species and across areas [Fleischauer et al, 1972;Peters and Walsh, 1972;Schmolke, 1989;Peters and Payne, 1993;Schlaug et al, 1995;Buxhoeveden et al, 1996Buxhoeveden et al, , 2000Peters and Sethares, 1996]. To identify and quantify differences between human and primate brains, research must concentrate on the internal operations of the cortex; thus we examined the cortical minicolumn in the human PT.…”