The organization of forebrain afferents to the paraventricular and supraoptic nuclei of the rat

Abstract

Axonal transport techniques were used to define the organization of projections from the forebrain to the paraventricular (PVH) and supraoptic (SO) nuclei of the hypothalamus in the adult rat. First, injections of a retro‐gradely transported fluorescent tracer, true blue, were placed in the region of the PVH, and the distribution of retrogradely labeled cells was charted. Then, the autoradiographic method was used to confirm the results of the retrograde transport experiments, to describe the route taken by inputs to the PVH and SO, and to determine the distribution of each projection within the various subdivisions of the nuclei that have been recognized previously on the basis of cytoarchitectonics, efferent projections, and immunohisto‐chemistry. The results can be summarized as follows. First, direct projections to the PVH arise from all areas of the hypothalamus (except the SO, the medial and lateral mammillary nuclei, and the magnocellular preoptic nucleus), and from the subfornical organ and the bed nucleus of the stria terminalis. Second, every forebrain region projecting directly to the PVH appears to innervate cell groups in parvocellular parts of the nucleus that in turn project to the neurohemal zone of the median eminence, and to autonomic centers in the brainstem and spinal cord. In addition, each input has a unique distribution within the parvocellular division. Third, relatively few regions in the forebrain project directly to magnocellular neurosecretory parts of the PVH, and are thus in a position to influence directly the release of posterior pituitary hormones. These regions (each of which also projects to the parvocellular division) include the dorsomedial nucleus of the hypothalamus, the median preoptic nucleus, the subfornical organ, and the bed nucleus. Therefore, inputs from the hippocampal formation, amygdala, and lateral septum that have been shown to influence the magnocellular neurosecretory system appear to be relayed by way of short projections from other parts of the hypothalamus (including perhaps parvocellular parts of the PVH) and from the bed nucleus. Fourth, most of these cell groups innervate preferentially either oxytocinergic (dorsomedial and bed nuclei) or vasopressinergic (subfornical organ) parts of the magnocellular division of the PVH. Only the projection from the median preoptic nucleus appears to be distributed uniformly over parts of the magnocellular division in which oxytocin‐ and vasopressin‐con‐taining cells are concentrated. And fifth, each region that preferentially innervates either oxytocinergic or vasopressinergic neurons in the PVH also preferentially innervates the same cell type in the SO (which does not contain a distinct parvocellular division). The results indicate that the coordination of neuroendocrine and autonomic responses from the PVH is mediated at least in part by a complex series of neural inputs, each of which innervates more than one functional subdivision within the nucleus.