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Relationships between radial glial progenitors and 5‐HT neurons in the paraventricular organ of adult zebrafish – potential effects of serotonin on adult neurogenesis

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Relationships between radial glial progenitors and 5‐HT neurons in the paraventricular organ of adult zebrafish – potential effects of serotonin on adult neurogenesis

Auteurs : María Rita Pérez [France, Argentine] ; Elisabeth Pellegrini [France] ; Joel Cano-Nicolau [France] ; Marie-Madeleine Gueguen [France] ; Dounia Menouer-Le Guillou [France] ; Yohann Merot [France] ; Colette Vaillant [France] ; Gustavo M. Somoza [Argentine] ; Olivier Kah [France]

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Abstract

In non‐mammalian vertebrates, serotonin (5‐HT)‐producing neurons exist in the paraventricular organ (PVO), a diencephalic structure containing cerebrospinal fluid (CSF)‐contacting neurons exhibiting 5‐HT or dopamine (DA) immunoreactivity. Because the brain of the adult teleost is known for its neurogenic activity supported, for a large part, by radial glial progenitors, this study addresses the origin of newborn 5‐HT neurons in the hypothalamus of adult zebrafish. In this species, the PVO exhibits numerous radial glial cells (RGCs) whose somata are located at a certain distance from the ventricle. To study relationships between RGCs and 5‐HT CSF‐contacting neurons, we performed 5‐HT immunohistochemistry in transgenic tg(cyp19a1b‐GFP) zebrafish in which RGCs are labelled with GFP under the control of the cyp19a1b promoter. We show that the somata of the 5‐HT neurons are located closer to the ventricle than those of RGCs. RGCs extend towards the ventricle cytoplasmic processes that form a continuous barrier along the ventricular surface. In turn, 5‐HT neurons contact the CSF via processes that cross this barrier through small pores. Further experiments using proliferating cell nuclear antigen or 5‐bromo‐2′‐deoxyuridine indicate that RGCs proliferate and give birth to 5‐HT neurons migrating centripetally instead of centrifugally as in other brain regions. Furthermore, treatment of adult zebrafish with tryptophan hydroxylase inhibitor causes a significant decrease in the number of proliferating cells in the PVO, but not in the mediobasal hypothalamus. These data point to the PVO as an intriguing region in which 5‐HT appears to promote genesis of 5‐HT neurons that accumulate along the brain ventricles and contact the CSF.

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DOI: 10.1111/ejn.12348

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<div type="abstract">In non‐mammalian vertebrates, serotonin (5‐HT)‐producing neurons exist in the paraventricular organ (PVO), a diencephalic structure containing cerebrospinal fluid (CSF)‐contacting neurons exhibiting 5‐HT or dopamine (DA) immunoreactivity. Because the brain of the adult teleost is known for its neurogenic activity supported, for a large part, by radial glial progenitors, this study addresses the origin of newborn 5‐HT neurons in the hypothalamus of adult zebrafish. In this species, the PVO exhibits numerous radial glial cells (RGCs) whose somata are located at a certain distance from the ventricle. To study relationships between RGCs and 5‐HT CSF‐contacting neurons, we performed 5‐HT immunohistochemistry in transgenic tg(cyp19a1b‐GFP) zebrafish in which RGCs are labelled with GFP under the control of the cyp19a1b promoter. We show that the somata of the 5‐HT neurons are located closer to the ventricle than those of RGCs. RGCs extend towards the ventricle cytoplasmic processes that form a continuous barrier along the ventricular surface. In turn, 5‐HT neurons contact the CSF via processes that cross this barrier through small pores. Further experiments using proliferating cell nuclear antigen or 5‐bromo‐2′‐deoxyuridine indicate that RGCs proliferate and give birth to 5‐HT neurons migrating centripetally instead of centrifugally as in other brain regions. Furthermore, treatment of adult zebrafish with tryptophan hydroxylase inhibitor causes a significant decrease in the number of proliferating cells in the PVO, but not in the mediobasal hypothalamus. These data point to the PVO as an intriguing region in which 5‐HT appears to promote genesis of 5‐HT neurons that accumulate along the brain ventricles and contact the CSF.</div>
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