Cytological and quantitative characteristics of four cerebral commissures in the rhesus monkey

Abstract

The number, types, and distribution of distinct classes of axons and glia in four cerebral commissures of the adult rhesus monkey (Macaca mulatta) were determined using electron microscopic and immunocytochemical methods. The two neocortical commissures, the corpus callosum, and the anterior commissure contain small but cytologically distinct archicortical components: the hippocampal commissure, which lies ventral to the splenium of the corpus callosum, and the basal telencephalic commissure, which forms a small crescent at the anterior margin of the anterior commissure. Each archicortical pathway is delineated from the adjacent neocortical commissure by a glial capsule. The glia cells that form this border are immunoreactive with antisera directed against glial fibrillary acidic protein (GFAP) and issue long processes that form numerous desmosomal junctions with one another. Braids of these glial processes envelop axonal fascicles within the archicortical commissures. In contrast, the GFAP-positive cells of the corpus callosum and anterior commissure are randomly distributed cells with relatively short stellate processes that do not form boundaries around axon fascicles. Quantitative electron microscopic analysis reveals that approximately 60 million axons connect the two cerebral hemispheres: the corpus callosum contains 56.0 million ± 3.8 million axons (n = 8), the anterior commissure contains 3.15 million ± 0.24 million axons (n = 8), the hippocampal commissure has 237,000 axons ± 31,000 (n = 6), and the basal telencephalic commissure has 193,000 axons ± 28,000 (n = 5). The number of axons is not directly proportional to the cross-sectional area in any of the commissures because of variation in axonal composition. On the basis of an estimate of approximately 3 billion neurons in the monkey cortex (Shariff, '53), we estimate that between 2 and 3% of all cortical neurons project to the opposite cerebral hemisphere. Subregions of the corpus callosum as well as each of the other commissures consist of characteristic subsets of five classes of axons and contain different proportions of myelinated to unmyelinated fibers. The largest myelinated axons and the smallest proportion of unmyelinated axons (≈ 6%) are found in regions of the corpus callosum that carry projections from primary sensory cortices, whereas the smallest myelinated axons and largest proportion of unmyelinated axons (≈ 30%) are found in regions of the corpus callosum that carry projections from association cortices. Axon composition in the anterior commissure is uniform and resembles that of callosal sectors that contain association projections. The hippocampal commissure contains predominantly small and medium-sized myelinated axons and few unmyelinated axons (≈ 10%), whereas the basal telencephalic commissure is composed of 80% unmyelinated axons and 20% of the smallest caliber myelinated axons. The differential distribution of distinct classes of axons along the anteriorposterior axis of the corpus callosum is in register with the segregation of projections from functionally and cytroarchitectonically distinct neocortical areas. The significance of this quantitative cytological data is discussed in the context of cortical physiology, cerebral dominance, sexual dimorphism, and telencephalic evolution.