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Review
The system of cerebrospinal
fluid-contacting neurons. Its supposed role in the nonsynaptic
signal transmission of the brain
B. Vígh1, M.J. Manzano e Silva2,
C.L. Frank1, C. Vincze1, S.J. Czirok1, A. Szabó1, A. Lukáts1
and A. Szél1
1Department of Human Morphology and Developmental
Biology, Semmelweis University, Budapest, Hungary and 2Occupational
Health Service, Hospital Santo António dos Capuchos, Lisbon,
Portugal
Offprint requests to: Prof. Dr. B. Vígh, Laboratory
of Photoneuro-endocrinology, Department of Human Morphology and
Developmental Biology, Semmelweis Medical University, Tüzoltó
u. 58. H-1094, Budapest, Hungary. Fax: 36-1-215-3064. e-mail:
vigh@ana2.sote.hu
Summary. Recent
investigations confirm the importance of nonsynaptic signal tranmission
in several functions of the nervous tissue. Present in various
periventricular brain regions of vertebrates, the system of cerebrospinal
fluid (CSF)-contacting neurons seems to have a special role in
taking up, transforming and emitting nonsynaptic signals mediated
by the internal and external CSF and intercellular fluid of the
brain.
Most of the CSF-contacting nerve cells send dendritic processes
into the internal CSF of the brain ventricles or central canal
where they form terminals bearing stereocilia and a 9+0-, or
9+2-type cilium. Some of these neurons resemble known sensory
cells of chemoreceptor-type, others may be sensitive to the pressure
or flow of the CSF, or to the illumination of the brain tissue.
The axons of the CSF-contacting neurons transmit information
taken up by dendrites and perikarya to synaptic zones of various
brain areas. By forming neurohormonal terminals, axons also contact
the external CSF space and release various bioactive substances
there. Some perikarya send their axons into the internal CSF,
and form free endings there, or synapses on intraventricular
dendrites, perikarya and/or on the ventricular surface of ependymal
cells. Contacting the intercellular space, sensory-type cilia
were also demonstrated on nerve cells situated in the brain tissue
subependymally or farther away from the ventricles.
Among neuronal elements entering the internal CSF-space, the
hypothalamic CSF-contacting neurons are present in the magnocellular
and parvicellular nuclei and in some circumventricular organs
like the paraventricular organ and the vascular sac. The CSF-contacting
dendrites of all these areas bear a solitary 9x2+0-type cilium
and resemble chemoreceptors 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 terminate not only in the hypothalamic
synaptic zones but also in tel-, mes- and rhombencephalic nuclei
and reach the spinal cord as well. The supposed chemical information
taken up by the CSF-contacting neurons from the ventricular CSF
may influence the function of these areas of the central nervous
system.
Some nerve cells of the photoreceptor areas form sensory terminals
similar to those of the hypothalamic CSF-contacting neurons.
Special secondary neurons of the retina and pineal organ contact
the retinal photoreceptor space and pineal recess respectively,
both cavities being embryologically derived from the 3rd ventricle.
The composition of these photoreceptor spaces is important in
the photochemical transduction and may modify the activity of
the secondary neurons. Septal and preoptic CSF-contacting neurons
contain various opsins and other compounds of the phototransduction
cascade and represent deep encephalic photoreceptors detecting
the illumination of the brain tissue and play a role in the regulation
of circadian and reproductive responses to light.
The medullo-spinal CSF-contacting neurons present in the oblongate
medulla, spinal cord and terminal filum, send their dendrites
into the fourth ventricle and central canal. Resembling mechanoreceptors
of the lateral line organ, the spinal CSF-contacting neurons
may be sensitive to the pressure or flow of the CSF. The axons
of these neurons terminate at the external CSF-space of the oblongate
medulla and spinal cord and form neurohormonal nerve endings.
Based on information taken up from the CSF, a regulatory effect
on the production or composition of CSF was supposed for bioactive
materials released by these terminals. Most of the axons of the
medullospinal CSF-contacting neurons and the magno- and parvicellular
neurosecretory nuclei running to neurohemal areas (neurohypophysis,
median eminence, terminal lamina, vascular sac and urophysis)
do not terminate directly on vessels, instead they form neurohormonal
nerve terminals attached by half-desmosomes on the basal lamina
of the external and vascular surface of the brain tissue. Therefore,
the bioactive materials released from these terminals primarily
enter the external CSF and secondarily, by diffusion into vessels
and the composition of the external CSF, may have a modulatory
effect on the bioactive substances released by the neurohormonal
terminals.
Contacting the intercellular space, sensory-type cilia were also
demonstrated on nerve cells situated subependymally or farther
away from the ventricles, among others in the neurosecretory
nuclei. Since tight-junctions are lacking between ependymal cells
of the ventricular wall, not only CSF-contacting but also subependymal
ciliated neurons may be influenced by the actual composition
of the CSF besides that of the intercellular fluid of the brain
tissue.
According to the comparative histological data summarised in
this review, the ventricular CSF-contacting neurons represent
the phylogenetically oldest component detecting the internal
fluid milieu of the brain. The neurohormonal terminals on the
external surface of the brain equally represent an ancient form
of nonsynaptic signal transmission. Histol. Histopathol. 19,
607-628 (2004)
Key words: CSF-receptors,
Nonsynaptic signal tranmission, Neurohormonal terminals, Deep
brain photoreceptors, Various vertebrates, Comparative fine structure,
Immunocytochemistry
DOI: 10.14670/HH-19.607
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