Organization of cerebral cortical afferent systems in the rat. II. Magnocellular basal nucleus

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Abstract
The organization of the magnocellular basal nucleus (MBN) projection to cerebral cortex in the rat has been studied by using cytoarchitectonic, immunohistochemical, and retrograde and anterograde transport methods. The distribution of retrogradely labeled basal forebrain neurons after cortical injections of wheat germ agglutinin-horseradish peroxidase conjugate was essentially identical to that of neurons staining immunohistochemically for choline acetyltransferase. These large (20–30 μm perikaryon diameter) multipolar neurons were found scattered through a number of basal forebrain cell groups: medial septal nucleus, nucleus of the diagonal band of Broca, magnocellular preoptic nucleus, substantia innominata, and globus pallidus. This peculiar distribution mimics the locations of pathways by which descending cortical fibers enter the diencephalon. Each cortical area was innervated by a characteristic subset of MBN neurons, always located in close association with descending cortical fibers. In many instances anterogradely labeled descending cortical fibers appeared to ramify into diffuse terminal fields among MBN neurons which were retrogradely labeled by the same cortical injection. Double label experiments using retrograde transport of fluorescent dyes confirmed that MBN neurons innervate restricted cortical fields. Anterograde autoradiographic transport studies after injections of 3H-amino acids into MBN revealed that MBN axons reach cerebral cortex primarily via two pathways: (1) The medial pathway, arising from the medial septal nucleus, nucleus of the diagonal band, and medial substantia innominata and globus pallidus MBN neurons, curves dorsally rostral to the diagonal band nucleus, up to the genu of the corpus callosum. Most of the fibers either directly enter medial frontal cortex or turn back over the genu of the corpus callosum into the superficial medial cingulate bundle. Many of these fibers enter anterior cigulate or retrosplenial cortex, but some can be traced back to the splenium of the corpus callosum, where a few enter visual cortex but most turn ventrally and sweep into the hippocampal formation. Here they are joined by other fibers which, at the genu of the corpus callosum, remain ventrally located and run caudally through the dorsal fornix into the hippocampus. (2) The lateral pathway arises in part from medial septal, diagonal band, and magnocellular preoptic neurons whose axons sweep laterally through the substantia innominata to innervate primarily piriform, perirhinal, and entorhinal cortex. Some of these fibers may also enter the hippocampal formation from the entorhinal cortex via the ventral subiculum. By far the largest part of the lateral pathway arises in the substantia innominata and globus pallidus. These axons sweep laterally through the substantia innominata and ventral part of the putamen to enter the external capsule, from which they distribute to the cortex of the lateral wall of the hemisphere. A few fibers also directly enter the piriform and entorhinal cortex. MBN axons in neocortex are found in highest concentration in layer V, and in the deepest part of layer VI, and in more moderate density in layers I and III, with only minor regional variation. In the subicular, entorhinal, and piriform cortex, the superficial molecular and deep cellular layers are most densely innervated. In the hippocampus, densest innervation was seen just adjacent to the alveus and in the superficial stratum lacunosum-moleculare; the supra- and infragranular layers were most densely innervated in the dentate gyrus. Throughout the hippocampus, MBN axons seemed to avoid the more densely cellular layers: stratum pyramidale in the CA fields and granular layer in the dentate gyrus (though the dentate hilus was moderately densely innervated). These results emphasize that a highly topographically ordered relationship with MBN is a basic feature of the organization of every portion of the cerebral cortex. Not only does MBN provide a similarly distributed innervation to each area of cerebral cortex, but MBN neurons probably receive inputs from the same cortical areas which they innervate. Despite its spatial dispersion, the relationship of each portion of MBN with descending axons from its cortical terminal field appears to be relatively constant. MBN, on cytoarchitectural, biochemical, and connectional grounds, is a single nucleus, and its spatially dispersed distribution can be explained on the basis of its cortical relations.