Actual problems of the cerebrospinal fluid-contacting neurons

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Abstract
Cerebrospinal fluid (CSF)‐contacting neurons form a part of the circumventricular organs of the central nervous system. Represented by different cytologic types and located in different regions, they constitute a CSF‐contacting neuronal system, the most central periventricular ring of neurons in the brain organized concentrically according to our concept. Because the central nervous system of deuterostomian echinoderm starfishes and the prochordate lancelet is composed mainly of CSF‐contacting‐like neurons, we hypothesize that this cell type represents ancient cells, or protoneurons, in the vertebrate brain. Neurons may contact the ventricular CSF via their dendrites, axons, or perikarya. Most of the CSF‐contacting nerve cells send their dendritic processes into the ventricular cavity, where they form ciliated terminals. These ciliated endings resemble those of known sensory cells. By means of axons, the CSF‐contacting neurons also may contact the external CSF space, where the axons form terminals of neurohormonal type similar to those known in the neurohemal areas. The most simple CSF‐contacting neurons of vertebrates are present in the terminal filum, spinal cord, and oblongate medulla. The dendritic pole of these medullospinal CSF‐contacting neurons terminates with an enlargement bearing many stereocilia in the central canal. These cells are also supplied with a 9 × 2 + 2 kinocilium that may contact Reissner's fiber, the condensed secretory material of the subcommissural organ. The Reissner's fiber floating freely in the CSF leaves the central canal at the caudal open end of the terminal filum in lower vertebrates, and open communication is thus established between internal CSF and the surrounding tissue spaces. Resembling mechanoreceptors cytologically, the spinal CSF‐contacting neurons send their axons to the outer surface of the spinal cord to form neurosecretory‐type terminals. They also send collaterals to local neurons and to higher spinal segments. In the hypothalamic part of the diencephalon, neurons of two circumventricular organs, the paraventricular organ and the vascular sac, of the magnocellular neurosecretory nuclei and several parvocellular nuclei, form CSF‐contacting dendritic terminals. A CSF‐contacting neuronal area also was found in the telencephalon. The CSF‐contacting dendrites of all these areas bear solitary 9 × 2 + 0 cilia and resemble chemoreceptors and developing photoreceptors cytologically. In electrophysiological experiments, the neurons of the paraventricular organ are highly sensitive to the composition of the ventricular CSF. The axons of the CSF‐contacting neurons of the paraventricular organ and hypothalamic nuclei terminate in hypothalamic synaptic zones, and those of magno‐ and parvocellular neurosecretory nuclei also form neurohormonal terminals in the median eminence and neurohypophysis. The axons of the CSF‐contacting neurons of the vascular sac run in the nervus and tractus sacci vasculosi to the nucleus (ganglion) sacci vasculosi. Some hypothalamic CSF‐contacting neurons contain immunoreactive opsin and are candidates to represent the “deep encephalic photoreceptors.” In the newt, cells derived from the subependymal layer develop photoreceptor outer segments protruding to the lumen of the infundibular lobe under experimental conditions. Retinal and pineal photoreceptors and some of their secondary neurons possess common cytologic features with CSF‐contacting neurons. They contact the retinal photoreceptor space and pineal recess, respectively, both cavities being derived from the third ventricle. In addition to ciliated dendritic terminals, there are intraventricular axons and neuronal perikarya contacting the CSF. Part of the CSF‐contacting axons are serotoninergic; their perikarya are situated in the raphe nuclei. Intraventricular axons innervate the CSF‐contacting dendrites, intraventricular nerve cells, and/or the ventricular surface of the ependyma. The cytologic organization and the fiber connections of the CSF‐contacting neuronal areas were outlined during the last decades by morphological studies. The comparative neurohistology of these neurons shows a relatively conservative organization of the CSF‐contacting neuronal system in the evolution. Microsc. Res. Tech. 41:57–83, 1998.

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