Aspects of the organization of neurons and dendritic bundles in primary somatosensory cortex of the rat

Abstract

In order to analyze some aspects of the spatial organization in the primary somatosensory cortex of the rat, we have reconstructed the positions of bundles of apical dendrites and neurons in a cortical prisms measuring 0.5 mm × 0.4 mm × cortical thickness, with special reference to a hypothetical columnar organization. Complete series of semithin (0.65 μm) sections were cut, tangentially from the pial surface down to the white matter, stained and digitizalized into a computer and represented as a stack of 2D images.

The mean neuron density (N_V-value) was (60 × 10³ ± 15 × 10³) neurons/mm³. The mean number of neurons beneath 1 mm² of cortical surface (N_C-value) was (113 × 10³ ± 8 × 10³) neurons/mm². Well-defined bundles of apical dendrites emanating from layer V pyramidal cells were observed. The bundles consisted of 3–12 (mean 5 ± 2) dendrites. The dendrites within a bundle converged while ascending towards the pial surface and reached a maximal close packing in layer IV. Superficially, the packing density decreased again. The mutual positions of the dendrites within the bundles shifted only slightly along their course towards the pial surface. The occurrence of bundles in tangential sections through layer IV was about 190 bundles/mm² and the average number of neurons per bundle was estimated at approximately 600. However, when calculating Voronoi-diagrams, the number of neurons, which with this mathematical technique, is ascribed to each of the reconstructed dendritic bundles, varied between 200 and 1000. The possibility that the dendritic bundles are centers in cortical cell modules is discussed.

Introduction

One of the most influential ideas regarding the structure and function of the cerebral cortex is the compartmentalization of cortical cells and their connections into vertical modules (cf. Buxhoeveden and Casanova, 2002, Jones, 2000, Mountcastle, 1997, Mountcastle, 2003, Szentagothai, 1975, Szentagothai, 1978). The idea was introduced during the first half of the last century (von Economo, 1929, Lorento de Nó, 1949), and it was later given considerable credibility by neurophysiological findings. Microelectrode studies of the somatosensory cortex in the cat have revealed that neurons in a vertical column respond to the same sensory modality and are related to almost identical peripheral receptive fields (Mountcastle, 1957, Mountcastle and Darian-Smith, 1968). In the visual cortex, different types of vertically oriented functional columns have been found, i.e., orientation columns (e.g., Hubel and Wiesel, 1977), eye preference columns (e.g., Wiesel et al., 1974), and color columns (e.g., Michael, 1981, Peters and Yilmaz, 1993). Neurons in layer IV in parts of the rodent somatosensory cortex are organized in hollow, vertically oriented “barrels” (Woolsey and van der Loos, 1970) corresponding to the receptive fields of the mystacial vibrissae (Woolsey and van der Loos, 1970, Weller, 1993).

The lack of a strict structural correlate, except for the barrels, to the physiological findings described above, has left the modular concept, from the anatomical point of view, an open issue (Swindale, 1990; cf. Purves et al., 1992). However, there is, in the cortex, some vertically oriented structural elements that have been proposed to be the anatomical core component of the modular unit. Examples of such elements are bundles of apical dendrites emanating from pyramidal cells (Roney et al., 1979, Peters and Kara, 1987, Peters and Sethares, 1996; c.f. Jones, 2000). Dendritic bundles were first described in the somatosensory cortex of the rat, rabbit and cat (Peter and Walsh, 1972; Fleischhauer et al., 1972). Since then, bundles of apical dendrites have been found in all neocortical areas examined (mouse: Detzer, 1976, Escobar et al., 1986, White and Peters, 1993; rat: Peters and Walsh, 1972, Feldman and Peters, 1974, Serfling and Schuster, 1983, Peters and Kara, 1987, Wyss et al., 1990, Hirst et al., 1991, Gabbott and Bacon, 1996, Curtetti et al., 2002; rabbit: Fleischhauer et al., 1972, Massing and Fleischhauer, 1973, Schmolke and Schleicher, 1989, Schmolke, 1989, Viebahn, 1990; cat: Fleischhauer, 1974, Fleischhauer and Detzer, 1975, Ikeda et al., 1989, Peters and Yilmaz, 1993; macaque: Feldman and Peters, 1974, Sakai, 1985, Peters and Sethares, 1996; human: Feldman and Peters, 1974).

In the present paper, we focus on one type of these bundles; the one defined as a non-random arrangement of at least three apical dendrites of layer V pyramidal cells (Peters and Kara, 1987). While ascending, more apical dendrites are added to the bundles, usually from layer III, pyramidal cells (Peters and Walsh, 1972) and in layer II, the bundles dissolve through dendritic arborization and merging (Roney et al., 1979).

The aim of the present study is to further illuminate the three-dimensional organization of these dendritic bundles in the primary somatosensory cortex of the rat. As quantitative data are essential for elaborating valid models of cortical circuitry, we have also done spatial and numerical analysis of the neurons surrounding the bundles. We have previously reported about a computer-based method for 3D reconstruction of neurons and neuronal processes in the cerebral cortex using tangential serial sections (Berthold et al., 1992, Skoglund et al., 1993, Skoglund et al., 1995; also see Rydmark et al., 1992). In the present paper, we describe our findings when implementing this method for the analysis of the organization of dendritic bundles and their surrounding neurons.