The circumventricular organs: an atlas of comparative anatomy and vascularization.

The circumventricular organs are small sized structures lining the cavity of the third ventricle (neurohypophysis, vascular organ of the lamina terminalis, subfornical organ, pineal gland and subcommissural organ) and of the fourth ventricle (area postrema). Their particular location in relation to the ventricular cavities is to be noted: the subfornical organ, the subcommissural organ and the area postrema are situated at the confluence between ventricles while the neurohypophysis, the vascular organ of the lamina terminalis and the pineal gland line ventricular recesses. The main object of this work is to study the specific characteristics of the vascular architecture of these organs: their capillaries have a wall devoid of blood-brain barrier, as opposed to central capillaries. This particular arrangement allows direct exchange between the blood and the nervous tissue of these organs. This work is based on a unique set of histological preparations from 12 species of mammals and 5 species of birds, and is taking the form of an atlas.

Sensory circumventricular organs and brain homeostatic pathways.

Circumventricular organs (CVOs), small structures bordering the ventricular spaces in the midline of the brain, have common morphological and endocrine-like characteristics that distinguish them from the rest of the nervous system. Among their unique features are cellular contacts with two fluid phases--blood and cerebrospinal fluid--and neural connections with strategic nuclei establishing circuitry for communications throughout the neuraxis. A variety of additional morphological and functional characteristics of the CVOs implicates this group of structures in a wide array of homeostatic processes. For three of the circumventricular organs--the subfornical organ (SFO), the organum vasculosum of the lamina terminalis (OVLT), and the area postrema (AP)--recent findings demonstrate these structures as targets for blood-borne information reaching the brain. We propose that these three sensory CVOs interact with other nuclei in the maintenance of several homeostatic processes by way of neural and humoral links. We emphasize the collective role of brain CVOs in the maintenance of body fluid homeostasis as a model for the functional integration of these fascinating "windows of the brain" within central neurohumoral systems.

Projections from the hypothalamus and its adjacent areas to the posterior pituitary in the rat.

Cholera toxin conjugated horseradish peroxidase was injected into the posterior pituitary and its afferents traced in 21 albino rats. The neuronal processes as well as the perikarya were elaborately displayed. The principal and retrochiasmatic supraoptic nuclei and the magnocellular paraventricular subnuclei were densely labelled. The accessory cell groups or nuclei labelled included: the medial preoptic and anterior hypothalamic areas, the anterior and posterior fornical nuclei, the lateral hypothalamic area, the nucleus circularis and nucleus of the forebrain bundle and hitherto unknown or not fully appreciated retrochiasmatic area, the dorsal accessory groups in an area between the stria medullaris and fornix, on the one hand, and the stria terminalis and internal capsule, on the other, and a well developed subependymalperiventricular zone. The medial preoptic nucleus, subfornical organ and organ vasculosum laminae terminalis were also weakly stained. Dendrites of the magnocellular paraventricular nucleus have been said by some to be largely confined to the subnuclei in which they lie. Immunohistochemical studies have proved that they extended beyond their nuclear confinement. The present study has found much wider extension of their dendritic fields. In fact, dendrites of the magnocellular neurosecretory cells in general were long and had a certain degree of directional bias. Several sites projecting to the posterior pituitary were closely related to the cerebrospinal fluid. Namely, the subependymal neuronal plexuses along the third ventricle and beneath the interventricular foramen, and the subpial dendritic plexuses of the supraoptic and retrochiasmatic supraoptic nuclei. Neurons were seen to squeeze in-between the ependymal cells, bringing themselves very close to the cerebrospinal fluid. No direct cerebrospinal fluid-contacting elements, either cell bodies or processes, however, could be ascertained. It is proposed that these plexuses may monitor changes in the cerebrospinal fluid. Besides the principal neurohypophysial tract the posterior pituitary was found in the present study to receive its afferents via two accessory fasciculi, one coursing in the medial forebrain bundle and the other running along the lateral wall of the infundibular recess subependymally.

Anatomical evidence that neural circuits related to the subfornical organ contain angiotensin II.

Bidirectional connections between the subfornical organ and the hypothalamus are reviewed, and emphasis is placed on recent evidence for the presence of angiotensin II in some of these pathways. Additionally, evidence is presented suggesting that this peptide may serve as a neurotransmitter or neuroendocrine factor in the efferent projections of cell groups receiving neural inputs from the subfornical organ. It appears that angiotensin II may serve as one of the chemical messengers at each link in multi-synaptic pathways related to the subfornical organ.

Altered CNS neuroanatomical organization of spontaneously hypertensive (SHR) rats.

Compared to Wistar-Kyoto (WKY) normotensive control rats, spontaneously hypertensive (SHR) rats have significantly reduced brain weights (-10.6%) and brain volumes (-11.8%). Computerized morphometric analysis of soma cross-sectional areas of single neurons in 12 selected hypothalamic regions revealed significant differences between SHR and WKY animals. Neurons from the periventricular, medial and lateral preoptic nuclei and ventromedial hypothalamus show significantly increased soma cross-sectional areas in SHR animals when compared to normotensive controls. Cells located in the two circumventricular organs, organ vasculosum lamina terminalis (OVLT) and subfornical organ (SFO), also showed significantly greater cross-sectional areas in the SHR. In contrast, neurons in the paraventricular and arcuate nuclei and dorsomedial hypothalamus were significantly smaller in spontaneously hypertensive rats when compared to normotensive controls. Only neurons in supraoptic nucleus, lateral and anterior hypothalamus have equivalent cross-sectional areas in WKY and SHR animals. Differences also exist in the number of cells in certain nuclei in SHR animals. Cell densities in periventricular preoptic nucleus, paraventricular nucleus, arcuate nucleus, ventromedial and anterior hypothalamus, organ vasculosum lamina terminalis and subfornical organ were reduced in SHR animals compared to WKY controls. Because of decreased brain weight and volume along with observed morphometric differences in individual neuronal soma size and cell densities, it is suggested that the SHR brain differs significantly from normotensive control rats. The differences may underlie some of the abnormalities in cardiovascular and endocrine regulation associated with neurogenic hypertension.

The efferent projections of the subfornical organ of the rat: a circumventricular organ within a neural network subserving water balance.

The efferent projections of the subfornical organ (SFO) of rats were traced using the autoradiographic method of following anterograde transport of labelled proteins through axons. The efferents of the SFO go to two different areas. The first is the anteroventral third ventricular area of the preoptic region and the second is the hypothalamus particularly the neurosecretory, magnocellular nuclei. Specifically, the apparent terminal fields in the first area are in the nucleus medianus of the medial preoptic area (NM), the organum vasculosum of the lamina terminalis (OVLT), and the anterior periventricular area (PeV). Many efferent fibers to this area emerge from the rostral SFO, pass anteriorly over the anterior commissure in the midline and either descend along the anterior border of the NM or enter the PeV dorsally just beneath the anterior commissure. The apparent terminal fields within the hypothalamus are in the anterior and tuberal supraoptic nuclei (SONa and SONt), the paraventricular nucleus (PVN) including its rostral accessory cluster, the nucleus circularis (NC), the dorsal perifornical area (PFd), and in both the lateral preoptic area and lateral hypothalamus adjacent to the SON. Many efferent fibers to the hypothalamus emerge from the rostral SFO and enter the columns of the fornix, diverge with the ventral stria medullari to disperse medially and laterally over the columns of the fornix and along their dorsal border at the anterior dorsal level of the columns trajectory through the hypothalamus. These findings are discussed in terms of the SFO's role within a neural network mediating water balance behaviorally and physiologically.

Fine structural evidence of degeneration in supraoptic nucleus and subfornical organ of rats with lesions in the anteroventral third ventricle.

Lesions of the tissue surrounding the anteroventral third ventricle (AV3V) alter mechanisms controlling body fluid homeostasis and hemodynamics. A period of adipsia and impaired antidiuresis follows AV3V destruction, which causes lesioned animals to become severely dehydrated. In lesioned rats, mechanisms maintaining water balance appear to be refractory to angiotensin and osmotic stimuli. To further investigate the neural basis for the observed alterations in body fluid balance, the supraoptic nucleus (SON) and subfornical organ (SFO) of rats with adipsia-producing lesions in the AV3V were examined by electron microscopy. In SONs of lesioned rats, degenerating fibers and terminals were present. Degenerating axonal terminals were seen in both axodendritic and axoaxonal synapses on magnocellular neurosecretory cells. These affected terminals in the SONs of lesioned rats may arise from osmoreceptors and angiotensin receptors which have somas or fibers in the lesioned area. Some fibers containing neurosecretory granulated vesicles also underwent degeneration. Neuronal somas displaying retrograde degenerative changes were present in SFOs after AV3V lesions. Degenerating fibers, some of which may be fibers of passage through the SFO, were common. However, little evidence of degenerative changes was seen in axon terminals in the SFOs. The evidence that lesions in the AV3V damaged an efferent projection field of the SFO is discussed in light of reports that AV3V lesions destroy responses in which the SFO is believed to participate.