Actual problems of the cerebrospinal fluid-contacting neurons

B. Vígh, Ingeborg Vigh-Teichmann

Research output: Contribution to journalArticle

102 Citations (Scopus)

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 x 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 x 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 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 neural areas were outlined during the last decades by morphological studies. The comparative neurohistology of this neurons shows a relatively conservative organizations of the CSF-contacting neural system in the evolution.

Original languageEnglish
Pages (from-to)57-83
Number of pages27
JournalMicroscopy Research and Technique
Volume41
Issue number1
DOIs
Publication statusPublished - Apr 1 1998

Fingerprint

cerebrospinal fluid
Cerebrospinal fluid
neurons
Neurons
Cerebrospinal Fluid
axons
photoreceptors
Axons
organs
vertebrates
nuclei
cells
dendrites
Dendrites
Vertebrates
spinal cord
Vertebrate Photoreceptor Cells
central nervous system
canals
Presynaptic Terminals

Keywords

  • Circumventricular organs
  • Comparative histology
  • Immunocytochemistry
  • Pineal organ
  • Retina

ASJC Scopus subject areas

  • Agricultural and Biological Sciences(all)
  • Anatomy
  • Instrumentation

Cite this

Actual problems of the cerebrospinal fluid-contacting neurons. / Vígh, B.; Vigh-Teichmann, Ingeborg.

In: Microscopy Research and Technique, Vol. 41, No. 1, 01.04.1998, p. 57-83.

Research output: Contribution to journalArticle

Vígh, B. ; Vigh-Teichmann, Ingeborg. / Actual problems of the cerebrospinal fluid-contacting neurons. In: Microscopy Research and Technique. 1998 ; Vol. 41, No. 1. pp. 57-83.
@article{fcbc7b2c136843a09ccbc4a97c37d0e5,
title = "Actual problems of the cerebrospinal fluid-contacting neurons",
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 x 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 x 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 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 neural areas were outlined during the last decades by morphological studies. The comparative neurohistology of this neurons shows a relatively conservative organizations of the CSF-contacting neural system in the evolution.",
keywords = "Circumventricular organs, Comparative histology, Immunocytochemistry, Pineal organ, Retina",
author = "B. V{\'i}gh and Ingeborg Vigh-Teichmann",
year = "1998",
month = "4",
day = "1",
doi = "10.1002/(SICI)1097-0029(19980401)41:1<57::AID-JEMT6>3.0.CO;2-R",
language = "English",
volume = "41",
pages = "57--83",
journal = "Microscopy Research and Technique",
issn = "1059-910X",
publisher = "Wiley-Liss Inc.",
number = "1",

}

TY - JOUR

T1 - Actual problems of the cerebrospinal fluid-contacting neurons

AU - Vígh, B.

AU - Vigh-Teichmann, Ingeborg

PY - 1998/4/1

Y1 - 1998/4/1

N2 - 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 x 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 x 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 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 neural areas were outlined during the last decades by morphological studies. The comparative neurohistology of this neurons shows a relatively conservative organizations of the CSF-contacting neural system in the evolution.

AB - 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 x 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 x 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 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 neural areas were outlined during the last decades by morphological studies. The comparative neurohistology of this neurons shows a relatively conservative organizations of the CSF-contacting neural system in the evolution.

KW - Circumventricular organs

KW - Comparative histology

KW - Immunocytochemistry

KW - Pineal organ

KW - Retina

UR - http://www.scopus.com/inward/record.url?scp=0032054699&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=0032054699&partnerID=8YFLogxK

U2 - 10.1002/(SICI)1097-0029(19980401)41:1<57::AID-JEMT6>3.0.CO;2-R

DO - 10.1002/(SICI)1097-0029(19980401)41:1<57::AID-JEMT6>3.0.CO;2-R

M3 - Article

C2 - 9550137

AN - SCOPUS:0032054699

VL - 41

SP - 57

EP - 83

JO - Microscopy Research and Technique

JF - Microscopy Research and Technique

SN - 1059-910X

IS - 1

ER -