Tissue compartments in laminae II-V of rabbit visual cortex--three-dimensional arrangement, size and developmental changes

The neuropil in laminae II/III and IV of the mature rabbit visual cortex is subdivided into (a) dendrite bundles consisting of apical dendrites of pyramidal cells and associated axons and glial processes, (b) bundles of myelinated axons ascending vertically from the white matter up to lamina IV and (c) neuropil between bundles comprising mainly thin unmyelinated axons, small dendrites and associated glial processes. In this investigation the three-dimensional structure of these compartments was analysed. In addition, the volume fractions of the three neuropil compartments, perikarya and blood vessels in the different laminae and their quantitative changes from the late fetal period up to young adulthood and in a group of aged animals were determined. Serial 1-micron epoxy sections were analysed. Dendrite bundles are more numerous and more intensively intertwined in lamina II/III than in lamina IV. At 28 days after conception the tissue in laminae II-V consists of approximately equal amounts, i.e. between 40 and 50%, of perikarya and neuropil. The volume fraction of blood vessels is about 4% and does not change much during development. During the first 16 days after birth the volume fraction of the neuropil increases to more than 70%, and conversely the volume fraction of nerve cells decreases to about 20%. Later, significant changes are seen only when the volume fractions of the three neuropil compartments are considered separately. The volume fraction of the neuropil between bundles increases throughout all laminae investigated, whereas the volume fraction of dendrite bundles is found to decrease. After 1 month, in lamina IV further increase of the neuropil between bundles is less marked, because here the bundles of myelinated axons become visible as an additional compartment. In young adult animals, the volume fractions of dendrite bundles are about 28% in the upper half, 16% in the lower half of lamina II/III and 7% in lamina IV. The neuropil between bundles comprises about 52% in the upper half, 65% in the lower half of lamina II/III and 62% in lamina IV. In lamina IV 14% is occupied by bundles of myelinated axons. In aged animals, the volume fraction of the neuropil between bundles decreases significantly in all laminae investigated. From previous ultrastructural studies, the extracellular space is known to be about 30% larger in the neuropil between bundles than in the dendrite bundles. Moreover, due to the prevalence of thin cell processes, the degree of tortuosity is larger in the neuropil between bundles than in the dendrite bundles. The present results together with these previous data are an indication of lamina-specific differences in the structure of the extracellular space. This may help to explain the electrical conductivity in the respective laminae of the cerebral cortex. The time course of postnatal changes of the neuropil compartments coincides with fundamental steps of structural and functional maturation of the rabbit visual cortex that are documented in the literature, and thus may be a valid parameter to investigate the degree of maturation or aging by morphological means.