Cerebrospinal fluid-contacting neurons of the central canal and terminal ventricle in various vertebrates

Vígh, B.; Vigh-Teichmann, I.; Silva, M. J. Manzano e; Pol, Anthony N. van den

doi:10.1007/bf00218119

Cited by 47 publications

(37 citation statements)

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“…Those settled in the lateral wall account for 73±6% of CSF-cNs at P0 (Fig. 1J,K Although spinal CSF-cNs have been described in a wide number of vertebrate species (Vigh and Vigh-Teichmann, 1971;Vigh et al, 1977Vigh et al, , 1983Stoeckel et al, 2003;Marichal et al, 2009;Huang et al, 2006;Djenoune et al, 2014;Jalalvand et al, 2014), their characteristics remain to be fully clarified. We evaluated the expression of distinct cellular markers and found that CSF-cNs express high levels of Nkx6-1 and Sox2 ( Fig.…”

Section: Resultsmentioning

confidence: 99%

“…The ependyma is composed of a layer of ciliated mural ependymocytes interspersed with tanycytes and CSF-contacting neurons (Bruni, 1998;Meletis et al, 2008;Sabourin et al, 2009;Marichal et al, 2012). Our genetic-tracing experiments with Gata3 Cre and Gata2 GFP selectively identified spinal CSF-cNs, which exhibit a unique morphology with a prominent dendritic process through the ependymal layer Vigh-Teichmann, 1971, 1998;Vigh et al, 1983) and express Pkd2l1 (Huang et al, 2006;Orts-Del'Immagine et al, 2014, 2016Djenoune et al, 2014).…”

Section: Csf-cns Are Late-born Gata2/3 + Neuronsmentioning

confidence: 86%

“…On the physiological properties and the role of CSF-cNs CSF-cNs have been found in every vertebrate species examined so far, from lamprey to primates (Vigh and Vigh-Teichmann, 1971;Vigh et al, 1977Vigh et al, , 1983Barber et al, 1982;Dale et al, 1987b;Stoeckel et al, 2003;Jalalvand et al, 2014;Djenoune et al, 2014;Reali et al, 2011). However, despite this evolutionary conservation, their function has not yet been fully elucidated.…”

Section: Heterochronic Development Of Csf-cns In Vertebratesmentioning

confidence: 99%

“…CSF-cNs are an intriguing cell type located around the spinal central canal. CSFcNs exhibit a peculiar morphology with a prominent dendritic extension through the ependymal layer terminating in a wide end bulb in the central canal Vigh-Teichmann, 1971, 1998;Vigh et al, 1983). More recently, CSF-cNs have been shown to express selectively the polycystic kidney disease 2-like 1 channel, Pkd2l1, which belongs to the transient receptor potential superfamily and has been proposed to serve mechano-and chemoreceptive functions (Huang et al, 2006;Djenoune et al, 2014;Orts-Del'Immagine et al, 2014).…”

Section: Introductionmentioning

confidence: 99%

“…More recently, CSF-cNs have been shown to express selectively the polycystic kidney disease 2-like 1 channel, Pkd2l1, which belongs to the transient receptor potential superfamily and has been proposed to serve mechano-and chemoreceptive functions (Huang et al, 2006;Djenoune et al, 2014;Orts-Del'Immagine et al, 2014). Although CSF-cNs were discovered a century ago and are present in all major groups of vertebrates, from cyclostomes to mammals (Vigh et al, 1983), their developmental origin and functions are only beginning to be unraveled.…”

Section: Introductionmentioning

confidence: 99%

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The late and dual origin of cerebrospinal fluid-contacting neurons in the mouse spinal cord

et al. 2016

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Considerable progress has been made in understanding the mechanisms that control the production of specialized neuronal types. However, how the timing of differentiation contributes to neuronal diversity in the developing spinal cord is still a pending question. In this study, we show that cerebrospinal fluid-contacting neurons (CSF-cNs), an anatomically discrete cell type of the ependymal area, originate from surprisingly late neurogenic events in the ventral spinal cord. CSF-cNs are identified by the expression of the transcription factors Gata2 and Gata3, and the ionic channels Pkd2l1 and Pkd1l2. Contrasting with Gata2/3 + V2b interneurons, differentiation of CSF-cNs is independent of Foxn4 and takes place during advanced developmental stages previously assumed to be exclusively gliogenic. CSF-cNs are produced from two distinct dorsoventral regions of the mouse spinal cord. Most CSF-cNs derive from progenitors circumscribed to the late-p2 and the oligodendrogenic ( pOL) domains, whereas a second subset of CSF-cNs arises from cells bordering the floor plate. The development of these two subgroups of CSF-cNs is differentially controlled by Pax6, they adopt separate locations around the postnatal central canal and they display electrophysiological differences. Our results highlight that spatiotemporal mechanisms are instrumental in creating neural cell diversity in the ventral spinal cord to produce distinct classes of interneurons, motoneurons, CSF-cNs, glial cells and ependymal cells.

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Section: Resultsmentioning

confidence: 99%

Section: Csf-cns Are Late-born Gata2/3 + Neuronsmentioning

confidence: 86%

Section: Heterochronic Development Of Csf-cns In Vertebratesmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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The late and dual origin of cerebrospinal fluid-contacting neurons in the mouse spinal cord

et al. 2016

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Synaptic and nonsynaptic monoaminergic neuron systems in the lamprey spinal cord

et al. 1996

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In the lamprey spinal cord, dopamine- (DA) and 5-hydroxytryptamine-(5-HT) containing cells appear to play an important role in controlling the firing properties of motoneurons and interneurons and, thereby, in modulating the efferent motor pattern. To determine the detailed morphology and synaptic connectivity of the intraspinal DA and 5-HT systems in Lampetra fluviatilis and Ichthyomyzon unicuspis, DA and 5-HT antisera were used in light and electron microscopic immunocytochemical experiments. Two main groups of labeled cells were distinguished: DA-containing liquor-contacting (LC) cells distributed along the central canal, and 5-HT+DA-containing multipolar cells located near the midline ventral to the central canal. Both types were synaptically connected with other neuronal elements. The DA-immunoreactive LC cells, which extended a ciliated process into the central canal, received symmetrical synapses from unlabeled terminals containing small synaptic vesicles. The distal process of the LC cells could be traced to the lateral cell column, to the ventral aspect of the dorsal column, or to the ventromedial area. Ultrastructural analysis of DA fibers in these regions showed the presence of labeled terminals containing numerous small synaptic vesicles and a few dense-core vesicles. These terminals formed symmetrical synapses with unlabeled cell bodies and dendrites, with GABA-immunopositive LC cells, and with the multipolar DA+5-HT cells. The multipolar DA+5-HT cells also received input from unlabeled synapses. Intracellular recording from these cells showed that they received excitatory postsynaptic potentials in response to stimulation of fibers in the ventromedial tracts and dorsal roots. The terminals of the multipolar DA+5-HT neurons in the ventromedial spinal cord contained numerous dense-core vesicles and small synaptic vesicles, but no synaptic specializations could be detected. In addition, a small number of larger DA-immunoreactive cells were observed in the lateral cell column at rostral levels. The lamprey spinal cord thus contains distinct populations of synaptically interconnected monoaminergic neurons. Dopamine-containing LC cells synapse onto DA+5-HT-containing multipolar cells, in addition to GABAergic LC cells and unidentified spinal neurons. In contrast, the multipolar cells appear to exert their influence by nonsynaptic mechanisms.

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Actual problems of the cerebrospinal fluid-contacting neurons

Vígh

Vigh-Teichmann

1998

Microsc. Res. Tech.

132

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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‐contacti...

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Cerebrospinal fluid-contacting neurons of the central canal and terminal ventricle in various vertebrates

Cited by 47 publications

References 4 publications

The late and dual origin of cerebrospinal fluid-contacting neurons in the mouse spinal cord

The late and dual origin of cerebrospinal fluid-contacting neurons in the mouse spinal cord

Synaptic and nonsynaptic monoaminergic neuron systems in the lamprey spinal cord

Actual problems of the cerebrospinal fluid-contacting neurons

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