Skip to main content
Key Specialties
Cardiology Diabetology Endocrinology Gastroenterology Geriatrics and Gerontology Gynecology and Obstetrics Hematology Infectious Disease Internal Medicine Nephrology Neurology Oncology Pediatrics Respiratory Medicine Rheumatology Surgery
Congress Coverage
2024 ACC Congress 2023 ESMO Congress 2023 EASD Congress 2023 ERS Congress 2023 ESC Congress 2023 EHA Congress 2023 ASCO Annual Meeting
Clinical Collections
Advances in Alzheimer’s

At a glance: The ONWARDS insulin icodec trials

A round-up of the ONWARDS phase 3 clinical trials evaluating the novel weekly insulin icodec in people with diabetes.
ADVANCED SEARCH
Log in
Top
Brain Structure and Function
Published in: Brain Structure and Function 1/2018

01-01-2018 | Original Article

Seasonal reorganization of hypothalamic neurogenic niche in adult sheep

Authors: Lucile Butruille, Martine Batailler, Danièle Mazur, Vincent Prévot, Martine Migaud

Published in: Brain Structure and Function | Issue 1/2018

Login to get access

Abstract

Neurogenesis is the process by which new neurons are generated. This process, well established during development, persists in adulthood owing to the presence of neural stem cells (NSCs) localized in specific brain areas called neurogenic niches. Adult neurogenesis has recently been shown to occur in the hypothalamus, a structure involved in the neuroendocrine regulation of reproduction and metabolism, among others. In the adult sheep—a long-lived mammalian model—we have previously reported the existence of such a neurogenic niche located in the hypothalamic arcuate nucleus and the median eminence. In addition, in this seasonal species, the proliferation as well as neuroblasts production varies depending on the time of the year. In the present study, we provide a better characterization of the hypothalamic neurogenic niche by identifying the main components (NSCs, migrating cells, glial cells and blood vessels) using immunohistochemistry for validated markers. Then, we demonstrate the strong sensitivity of these various neurogenic niche components to the season, particularly in the arcuate nucleus. Further, using an electron microscopic approach, we reveal the cellular and cytoarchitectural reorganization of the arcuate nucleus niche following exposure to contrasting seasons. This study provides evidence that the arcuate nucleus and the median eminence contain two independent niches that react differently to the season. In addition, our results support the view that the cytoarchitectural organization of the sheep arcuate nucleus share comparable features with the structure of the subventricular zone in humans and non-human primates.
Literature
Aarum J, Sandberg K, Haeberlei S, Persson M (2003) Migration and differentiation of neural precursor cells can be directed by microglia. Proc Natl Acad Sci USA 100(26):15983–15988PubMedPubMedCentralCrossRef
Akmayev IG, Fidelina OV, Kabolova Z, Popov A, Schitkova T (1973) Morphological aspects of the hypothalamic-hypophyseal system. IV. Medial basal hypothalamus. An experimental morphological study. Z Zellforsch Mik Anat 137(4):493–512CrossRef
Alonso G, Prieto M, Chauvet N (1999) Tangential migration of young neurons arising from the subventricular zone of adult rats is impaired by surgical lesions passing through their natural migratory pathway. J Comp Neurol 405(4):508–528PubMedCrossRef
Alvarez-Buylla A, Theelen M, Nottebohm F (1990) Proliferation “hot spots” in adult avian ventricular zone reveal radial cell division. Neuron 5(1):101–109PubMedCrossRef
Alvarez-Buylla A, Garcia-Verdugo JM, Tramontin AD (2001) A unified hypothesis on the lineage of neural stem cells. Nat Rev Neurosci 2(4):287–293PubMedCrossRef
Alvarez-Buylla A, Seri B, Doetsch F (2002) Identification of neural stem cells in the adult vertebrate brain. Brain Res Bull 57(6):751–758PubMedCrossRef
Andreu-Agullo C, Morante-Redolat JM, Delgado AC, Farinas I (2009) Vascular niche factor PEDF modulates Notch-dependent stemness in the adult subependymal zone. Nat Neurosci 12(12):1514–1523PubMedCrossRef
Barnea A, Pravosudov V (2011) Birds as a model to study adult neurogenesis: bridging evolutionary, comparative and neuroethological approches. Eur J Neurosci 34(6):884–907PubMedPubMedCentralCrossRef
Batailler M, Droguerre M, Baroncini M, Fontaine C, Prevot V, Migaud M (2014) DCX-expressing cells in the vicinity of the hypothalamic neurogenic niche: a comparative study between mouse, sheep, and human tissues. J Comp Neurol 522(8):1966–1985PubMedCrossRef
Batailler M, Derouet L, Butruille L, Migaud M (2016) Sensitivity to the photoperiod and potential migratory features of neuroblasts in the adult sheep hypothalamus. Brain Struct Funct 221(6):3301–3314PubMedCrossRef
Baumann N, Pham-Dinh D (2001) Biology of oligodendrocyte and myelin in the mammalian central nervous system. Physiol Rev 81(2):871–927PubMedCrossRef
Beltramo M, Dardente H, Cayla X, Caraty A (2014) Cellular mechanisms and integrative timing of neuroendocrine control of GnRH secretion by kisspeptin. Mol Cell Endocrinol 382(1):387–399PubMedCrossRef
Belvindrah R, Hankel S, Walker J, Patton BL, Müller U (2007) β1 integrins control the formation of cell chains in the adult rostral migratory stream. J Neurosci 27(10):2704–2717PubMedCrossRef
Bennett L, Yang M, Enikolopov G, Iacovitti L (2009) Circumventricular organs: a novel site of neural stem cells in the adult brain. Mol Cell Neurosci 41(3):337–347PubMedPubMedCentralCrossRef
Bolborea M, Laran-Chich MP, Rasri K, Hildebrandt H, Govitrapong P, Simonneaux V, Pévet P, Steinlechner S, Klosen P (2011) Melatonin controls photoperiodic changes in tanycyte vimentin and neural cell adhesion molecule expression in the Djungarian hamster (Phodopus sungorus). Endocrinology 152(10):3871–3883PubMedCrossRef
Bonfanti L (2006) PSA-NCAM in mammalian structural plasticity and neurogenesis. Prog Neurobiol 80(3):129–164PubMedCrossRef
Bonfanti L, Theodosis DT (1994) Expression of polysialylated neural cell adhesion molecule by proliferating cells in the subependymal layer of the adult rat, in its rostral extension and in the olfactory bulb. Neuroscience 62(1):291–305PubMedCrossRef
Bonfanti L, Olive S, Poulain DA, Theodosis DT (1992) Mapping of the distribution of polysialylated neural cell adhesion molecule throughout the central nervous system of the adult rat: an immunohistochemical study. Neuroscience 49(2):419–436PubMedCrossRef
Brus M, Meurisse M, Franceschini I, Keller M, Levy F (2010) Evidence for cell proliferation in the sheep brain and its down-regulation by parturition and interactions with the young. Horm Behav 58(5):737–746PubMedCrossRef
Brus M, Meurisse M, Gheusi G, Keller M, Lledo PM, Levy F (2013) Dynamics of olfactory and hippocampal neurogenesis in adult sheep. J Comp Neurol 521(1):169–188PubMedCrossRef
Cameron HA, Woolley CS, Mcewen BS, Gould E (1993) Differentiation of newly born neurons and glia in the dentate gyrus of the adult rat. Neuroscience 56(2):337–344PubMedCrossRef
Chalivoix S, Guillaume D, Cognié J, Thiéry JC, Malpaux B, Dufourny L (2013) Photoperiodic variations of the polysialylated form of neural cell adhesion molecule within the hypothalamus and related reproductive output in the ewe. Cell Tissue Res 352(2):387–399PubMedCrossRef
Chemineau P, Guillaume D, Migaud M, Thiéry J, Pellicer-Rubio M, Malpaux B (2008) Seasonality of reproduction in mammals: intimate regulatory mechanisms and practical implications. Reprod Domest Anim 43:40–47PubMedCrossRef
Codega P, Silva-Vargas V, Paul A, Maldonado-Soto AR, Deleo AM, Pastrana E, Doetsch F (2014) Prospective identification and purification of quiescent adult neural stem cells from their in vivo niche. Neuron 82(3):545–559PubMedPubMedCentralCrossRef
Degendorfer G, Chuang CY, Hammer A, Malle E, Davies MJ (2015) Peroxynitrous acid induces structural and functional modifications to basement membranes and its key component, laminin. Free Radic Biol Med 89:721–733PubMedCrossRef
Djogo T, Robins SC, Schneider S, Kryzskaya D, Liu X, Mingay A, Gillon CJ, Kim JH, Storch K-F, Boehm U, Bourque CW, Stroh T, Dimou L, Kokoeva MV (2016) Adult NG2-glia are required for median eminence-mediated leptin sensing and body weight control. Cell Metab 23(5):797–810PubMedCrossRef
Doetsch F, Caille I, Lim DA, Garcia-Verdugo JM, Alvarez-Buylla A (1999a) Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell 97(6):703–716PubMedCrossRef
Doetsch F, García-Verdugo JM, Alvarez-Buylla A (1999b) Regeneration of a germinal layer in the adult mammalian brain. Proc Natl Acad Sci USA 96(20):11619–11624PubMedPubMedCentralCrossRef
Eriksdotter-Nilsson M, Björklund H, Olson L (1986) Laminin immunohistochemistry: a simple method to visualize and quantitate vascular structures in the mammalian brain. J Neurosci Methods 17(4):275–286PubMedCrossRef
Eriksson PS, Perfilieva E, Björk-Eriksson T, Alborn AM, Nordborg C, Peterson DA, Gage FH (1998) Neurogenesis in the adult human hippocampus. Nat Med 4(11):1313–1317PubMedCrossRef
Faissner A, Reinhard J (2015) The extracellular matrix compartment of neural stem and glial progenitor cells. Glia 63:1330–1349PubMedCrossRef
Ferri ALM, Cavallaro M, Braida D, Di Cristofano A, Canta A, Vezzani A, Ottolenghi S, Pandolfi PP, Sala M, Debiasi S, Nicolis SK (2004) Sox2 deficiency causes neurodegeneration and impaired neurogenesis in the adult mouse brain. Development 131(15):3805–3819PubMedCrossRef
Fowler C, Johnson F, Wang Z (2005) Estrogen regulation of cell proliferation and distribution of estrogen receptor-alpha in the brains of adult female prairie and meadow voles. J Comp Neurol 489(2):166–179PubMedPubMedCentralCrossRef
Gil-Perotin S, Duran-Moreno M, Belzunegui S, Luquin MR, Garcia-Verdugo JM (2009) Ultrastructure of the subventricular zone in Macaca fascicularis and evidence of a mouse-like migratory stream. J Comp Neurol 514:533–554PubMedCrossRef
Goldman SA, Nottebohm F (1983) Neuronal production, migration, and differentiation in a vocal control nucleus of the adult female canary brain. Proc Natl Acad Sci USA 80(8):2390–2394PubMedPubMedCentralCrossRef
Gould E, Tanapat P, Mcewen BS, Flügge G, Fuchs E (1998) Proliferation of granule cell precursors in the dentate gyrus of adult monkeys is diminished by stress. Proc Natl Acad Sci USA 95(6):3168–3171PubMedPubMedCentralCrossRef
Graham V, Khudyakov J, Ellis P, Pevny L (2003) SOX2 functions to maintain neural progenitor identity. Neuron 39(5):749–765PubMedCrossRef
Haan N, Goodman T, Najdi-Samiei A, Stratford CM, Rice R, El Agha E, Bellusci S, Hajihosseini MK (2013) Fgf10-expressing tanycytes add new neurons to the appetite/energy-balance regulating centers of the postnatal and adult hypothalamus. J Neurosci 33(14):6170–6180PubMedPubMedCentralCrossRef
Hawken PaR, Jorre TJDS, Rodger J, Esmaili T, Blache D, Martin GB (2009) Rapid induction of cell proliferation in the adult female ungulate brain (Ovis aries) associated with activation of the reproductive axis by exposure to unfamiliar males. Biol Reprod 80(6):1146–1151PubMedCrossRef
Huang L, Devries GJ, Bittman EL (1998) Photoperiod regulates neuronal bromodeoxyuridine labeling in the brain of a seasonally breeding mammal. J Neurobiol 36:410–420PubMedCrossRef
Kameda Y (1996) Immunoelectron microscopic localization of vimentin in sustentacular cells of the carotid body and the adrenal medulla of guinea pigs. J Histochem Cytochem 44(12):1439–1449PubMedCrossRef
Kameda Y, Arai Y, Nishimaki T (2003) Ultrastructural localization of vimentin immunoreactivity and gene expression in tanycytes and their alterations in hamsters kept under different photoperiods. Cell Tissue Res 314(2):251–262PubMedCrossRef
Kaplan M, Bell D (1984) Mitotic neuroblasts in the 9-day-old and 11-month-old rodent hippocampus. J Neurosci 4(6):1429–1441PubMed
Kaplan M, Hinds J (1977) Neurogenesis in the adult rat: electron microscopic analysis of light radioautographs. Science 197(4308):1092–1094PubMedCrossRef
Kazanis I, Lathia JD, Vadakkan TJ, Raborn E, Wan R, Mughal MR, Eckley DM, Sasaki T, Patton B, Mattson MP, Hirschi KK, Dickinson ME, Ffrench-Constant C (2010) Quiescence and activation of stem and precursor cell populations in the subependymal zone of the mammalian brain are associated with distinct cellular and extracellular matrix signals. J Neurosci 30(29):9771–9781PubMedPubMedCentralCrossRef
Kerever A, Schnack J, Vellinga D, Ichikawa N, Moon C, Arikawa-Hirasawa E, Efird JT, Mercier F (2007) Novel extracellular matrix structures in the neural stem cell niche capture the neurogenic factor fibroblast growth factor 2 from the extracellular milieu. Stem cells 25:2146–2157PubMedCrossRef
Kleinman HK, Cannon FB, Laurie GW, Hassell JR, Aumailley M, Terranova VP, Martin GR, Dubois-Dalcq M (1985) Biological activities of laminin. J Cell Biochem 27:317–325PubMedCrossRef
Knigge KM, Scott DE (1970) Structure and function of the median eminence. Am J Anat 129(2):223–243PubMedCrossRef
Kokoeva MV, Yin H, Flier JS (2005) Neurogenesis in the hypothalamus of adult mice: potential role in energy balance. Science 310(5748):679–683PubMedCrossRef
Kokoeva MV, Yin H, Flier JS (2007) Evidence for constitutive neural cell proliferation in the adult murine hypothalamus. J Comp Neurol 505(2):209–220PubMedCrossRef
Kuhn H, Dickinson-Anson H, Gage F (1996) Neurogenesis in the dentate gyrus of the adult rat: age-related decrease of neuronal progenitor proliferation. J Neurosci 16(6):2027–2033PubMed
Langlet F (2014) Tanycytes: a gateway to the metabolic hypothalamus. J Neuroendocrinol 26(11):753–760PubMedCrossRef
Laywell ED, Rakic P, Kukekov VG, Holland EC, Steindler DA (2000) Identification of a multipotent astrocytic stem cell in the immature and adult mouse brain. Proc Natl Acad Sci USA 97(25):13883–13888PubMedPubMedCentralCrossRef
Lee DA, Bedont JL, Pak T, Wang H, Song J, Miranda-Angulo A, Takiar V, Charubhumi V, Balordi F, Takebayashi H, Aja S, Ford E, Fishell G, Blackshaw S (2012) Tanycytes of the hypothalamic median eminence form a diet-responsive neurogenic niche. Nat Neurosci 15(5):700–702PubMedPubMedCentralCrossRef
Li J, Tang Y, Cai D (2012) IKKbeta/NF-kappaB disrupts adult hypothalamic neural stem cells to mediate a neurodegenerative mechanism of dietary obesity and pre-diabetes. Nat Cell Biol 14(10):999–1012PubMedPubMedCentralCrossRef
Lois C, Alvarez-Buylla A (1993) Proliferating subventricular zone cells in the adult mammalian forebrain can differentiate into neurons and glia. Proc Natl Acad Sci USA 90(5):2074–2077PubMedPubMedCentralCrossRef
Lopez-Garcia C, Molowny A, Garcia-Verdugo JM, Ferrer I (1988) Delayed postnatal neurogenesis in the cerebral cortex of lizards. Brain Res 43(2):167–174CrossRef
Lugert S, Basak O, Knuckles P, Haussler U, Fabel K, Götz M, Haas CA, Kempermann G, Taylor V, Giachino C (2010) Quiescent and active hippocampal neural stem cells with distinct morphologies respond selectively to physiological and pathological stimuli and aging. Cell Stem Cell 6(5):445–456PubMedCrossRef
Luzzati F, Bonfanti L, Fasolo A, Peretto P (2009) DCX and PSA-NCAM expression identifies a population of neurons preferentially distributed in associative areas of different pallial derivatives and vertebrate species. Cereb Cortex 19(5):1028–1041PubMedCrossRef
Marques S, Zeisel A, Codeluppi S, Van Bruggen D, Mendanha Falcão A, Xiao L, Li H, Häring M, Hochgerner H, Romanov RA, Gyllborg D, Muñoz-Manchado AB, La Manno G, Lönnerberg P, Floriddia EM, Rezayee F, Ernfors P, Arenas E, Hjerling-Leffler J, Harkany T, Richardson WD, Linnarsson S, Castelo-Branco G (2016) Oligodendrocyte heterogeneity in the mouse juvenile and adult central nervous system. Science 352(6291):1326–1329PubMedPubMedCentralCrossRef
Mckinley MJ, Rm Mcallen, Fao Mendelsohn, Am Allen, Sy Chai, Bj Oldfield (1990) Circumventricular organs: neuroendocrine interfaces between the brain and the hemal milieu. Front Neuroendocrinol 11(2):91–127
Mcnay DEG, Briançon N, Kokoeva MV, Maratos-Flier E, Flier JS (2012) Remodeling of the arcuate nucleus energy-balance circuit is inhibited in obese mice. J Clin Investig 122(1):142–152PubMedCrossRef
Mercier F, Hatton GI (2001) Connexin 26 and basic fibroblast growth factor are expressed primarily in the subpial and subependymal layers in adult brain parenchyma: roles in stem cell proliferation and morphological plasticity? J Comp Neurol 431:88–104PubMedCrossRef
Mercier F, Cho Kwon Y, Kodama R (2011) Meningeal/vascular alterations and loss of extracellular matrix in the neurogenic zone of adult BTBR T + tf/J mice, animal model for autism. Neurosci Lett 498(3):173–178PubMedCrossRef
Merkle FT, Tramontin AD, García-Verdugo JM, Alvarez-Buylla A (2004) Radial glia give rise to adult neural stem cells in the subventricular zone. Proc Natl Acad Sci USA 101(50):17528–17532PubMedPubMedCentralCrossRef
Messager S, Chatzidaki EE, Ma D, Hendrick AG, Zahn D, Dixon J, Thresher RR, Malinge I, Lomet D, Carlton MBL, Colledge WH, Caraty A, SaJR Aparicio (2005) Kisspeptin directly stimulates gonadotropin-releasing hormone release via G protein-coupled receptor 54. Proc Natl Acad Sci USA 102(5):1761–1766PubMedPubMedCentralCrossRef
Migaud M, Batailler M, Segura S, Duittoz A, Franceschini I, Pillon D (2010) Emerging new sites for adult neurogenesis in the mammalian brain: a comparative study between the hypothalamus and the classical neurogenic zones. Eur J Neurosci 32(12):2042–2052PubMedCrossRef
Migaud M, Batailler M, Pillon D, Franceschini I, Malpaux B (2011) Seasonal changes in cell proliferation in the adult sheep brain and pars tuberalis. J Biol Rhythms 26(6):486–496PubMedCrossRef
Migaud M, Butruille L, Batailler M (2015) Seasonal regulation of structural plasticity and neurogenesis in the adult mammalian brain: focus on the sheep hypothalamus. Front Neuroendocrinol 37:146–157PubMedCrossRef
Migaud M, Butruille L, Duittoz A, Pillon D, Batailler M (2016) Adult neurogenesis and reproductive functions in mammals. Theriogenology 86(1):313–323PubMedCrossRef
Miller FD, Gauthier-Fisher A (2009) Home at last: neural stem cell niches defined. Cell Stem Cell 4(6):507–510PubMedCrossRef
Mirzadeh Z, Merkle FT, Soriano-Navarro M, García-Verdugo JM, Alvarez-Buylla A (2008) Neural stem cells confer unique pinwheel architecture to the ventricular surface in neurogenic regions of the adult brain. Cell Stem Cell 3(3):265–278PubMedPubMedCentralCrossRef
Morshead CM, Reynolds BA, Craig CG, Mcburney MW, Staines WA, Morassutti D, Weiss S, Van Der Kooy D (1994) Neural stem cells in the adult mammalian forebrain: a relatively quiescent subpopulation of subependymal cells. Neuron 13(5):1071–1082PubMedCrossRef
Mullier A, Bouret SG, Prevot V, Dehouck B (2010) Differential distribution of tight junction proteins suggests a role for tanycytes in blood–hypothalamus barrier regulation in the adult mouse brain. J Comp Neurol 518(7):943–962PubMedPubMedCentralCrossRef
Palmer TD, Willhoite AR, Gage FH (2000) Vascular niche for adult hippocampal neurogenesis. J Comp Neurol 425(4):479–494PubMedCrossRef
Pencea V, Bingaman KD, Wiegand SJ, Luskin MB (2001) Infusion of brain-derived neurotrophic factor into the lateral ventricle of the adult rat leads to new neurons in the parenchyma of the striatum, septum, thalamus, and hypothalamus. J Neurosci 21(17):6706–6717PubMed
Perera AD, Lagenaur CF, Plant TM (1993) Postnatal expression of polysialic acid-neural cell adhesion molecule in the hypothalamus of the male rhesus monkey (Macaca mulatta). Endocrinology 133(6):2729–2735PubMedCrossRef
Pérez-Martín M, Cifuentes M, Grondona JM, López-Ávalos MD, Gómez-Pinedo U, García-Verdugo JM, Fernández-Llebrez P (2010) IGF-I stimulates neurogenesis in the hypothalamus of adult rats. Eur J Neurosci 31:1533–1548PubMed
Prevot V, Dutoit S, Croix D, Tramu G, Beauvillain JC (1998) Semi-quantitative ultrastructural analysis of the localization and neuropeptide content of gonadotropin releasing hormone nerve terminals in the median eminence throughout the estrous cycle of the rat. Neuroscience 84(1):177–191PubMedCrossRef
Prevot V, Croix D, Bouret S, Dutoit S, Tramu G, Stefano GB, Beauvillain JC (1999) Definitive evidence for the existence of morphological plasticity in the external zone of the median eminence during the rat estrous cycle: implication of neuro-glio-endothelial interactions in gonadotropin-releasing hormone release. Neuroscience 94(3):809–819PubMedCrossRef
Prevot V, Bellefontaine N, Baroncini M, Sharif A, Hanchate NK, Parkash J, Campagne C, De Seranno S (2010) Gonadotrophin-releasing hormone nerve terminals, tanycytes and neurohaemal junction remodelling in the adult median eminence: functional consequences for reproduction and dynamic role of vascular endothelial cells. J Neuroendocrinol 22(7):639–649PubMedPubMedCentral
Rinne UK (1966) Ultrastructure of the median eminence of the rat. Z Zellforsch Mik Anat 74(1):98–122CrossRef
Robins SC, Stewart I, Mcnay DE, Taylor V, Giachino C, Goetz M, Ninkovic J, Briancon N, Maratos-Flier E, Flier JS, Kokoeva MV, Placzek M (2013) α-Tanycytes of the adult hypothalamic third ventricle include distinct populations of FGF-responsive neural progenitors. Nat Commun 4:2049PubMedCrossRef
Rodríguez EM, González CB, Delannoy L (1979) Cellular organization of the lateral and postinfundibular regions of the median eminence in the rat. Cell Tissue Res 201(3):377–408PubMedCrossRef
Rodríguez EM, Blázquez JL, Pastor FE, Peláez B, Peña P, Peruzzo B, Amat P (2005) Hypothalamic tanycytes: a key component of brain–endocrine interaction. Int Rev Cytol 247:89–164PubMedCrossRef
Sanai N, Tramontin AD, Quinones-Hinojosa A, Barbaro NM, Gupta N, Kunwar S, Lawton MT, Mcdermott MW, Parsa AT, Manuel-Garcia Verdugo J, Berger MS, Alvarez-Buylla A (2004) Unique astrocyte ribbon in adult human brain contains neural stem cells but lacks chain migration. Nature 427(6976):740–744PubMedCrossRef
Sawamoto K, Hirota Y, Alfaro-Cervello C, Soriano-Navarro M, He X, Hayakawa-Yano Y, Yamada M, Hikishima K, Tabata H, Iwanami A, Nakajima K, Toyama Y, Itoh T, Alvarez-Buylla A, Garcia-Verdugo JM, Okano H (2011) Cellular composition and organization of the subventricular zone and rostral migratory stream in the adult and neonatal common marmoset brain. J Comp Neurol 519(4):690–713PubMedPubMedCentralCrossRef
Scott DE, Sladek JR (1981) Age related changes in the endocrine hypothalamus: I. Tanycytes and the blood–brain–cerebrospinal fluid barrier. Neurobiol Aging 2(2):89–94PubMedCrossRef
Shen Q, Wang Y, Kokovay E, Lin G, Chuang S-M, Goderie SK, Roysam B, Temple S (2008) Adult SVZ stem cells lie in a vascular niche: a quantitative analysis of niche cell–cell interactions. Cell Stem Cell 3(3):289–300PubMedPubMedCentralCrossRef
Simmoneaux V, Ancel C, Poirel VJ, Gauer F (2013) Kisspeptins and RFRP-3 act in concert to synchronize rodent reproduction with seasons. Front Neurosci 7:22
Sousa-Ferreira L, Álvaro AR, Aveleira C, Santana M, Brandão I, Kügler S, Pereira De Almeida L, Cavadas C (2011) Proliferative hypothalamic neurospheres express NPY, AGRP, POMC, CART and orexin-A and differentiate to functional neurons. PLoS One 6(5):e19745PubMedPubMedCentralCrossRef
Tanti A, Rainer Q, Minier F, Surget A, Belzung C (2012) Differential environmental regulation of neurogenesis along the septo-temporal axis of the hippocampus. Neuropharmacology 63(3):374–384PubMedCrossRef
Taupin P, Gage FH (2002) Adult neurogenesis and neural stem cells of the central nervous system in mammals. J Neurosci Res 69(6):745–749PubMedCrossRef
Viguié C, Jansen HT, Glass JD, Watanabe M, Billings HJ, Coolen L, Lehman MN, Karsch FJ (2001) Potential for polysialylated form of neural cell adhesion molecule-mediated neuroplasticity within the gonadotropin-releasing hormone neurosecretory system of the ewe. Endocrinology 142(3):1317–1324PubMedCrossRef
Walton NM, Sutter BM, Laywell ED, Levkoff LH, Kearns SM, Marshall GP, Scheffler B, Steindler DA (2006) Microglia instruct subventricular zone neurogenesis. Glia 54:815–825PubMedCrossRef
Wei LC, Shi M, Chen LW, Cao R, Zhang P, Chan YS (2002) Nestin-containing cells express glial fibrillary acidic protein in the proliferative regions of central nervous system of postnatal developing and adult mice. Dev Brain Res 139(1):9–17CrossRef
Wiese C, Rolletschek A, Kania G, Blyszczuk P, Tarasov KV, Tarasova Y, Wersto RP, Boheler KR, Wobus AM (2004) Nestin expression—a property of multi-lineage progenitor cells? Cell Mol Life Sci 61(19):2510–2522PubMedCrossRef
Woodfill CJ, Robinson JE, Malpaux B, Karsch FJ (1991) Synchronization of the circannual reproductive rhythm of the ewe by discrete photoperiodic signals. Biol Reprod 45(1):110–121PubMedCrossRef
Xu Y, Tamamaki N, Noda T, Kimura K, Itokazu Y, Matsumoto N, Dezawa M, Ide C (2005) Neurogenesis in the ependymal layer of the adult rat 3rd ventricle. Exp Neurol 192(2):251–264PubMedCrossRef
Metadata
Title
Seasonal reorganization of hypothalamic neurogenic niche in adult sheep
Authors
Lucile Butruille
Martine Batailler
Danièle Mazur
Vincent Prévot
Martine Migaud
Publication date
01-01-2018
Publisher
Springer Berlin Heidelberg
Published in
Brain Structure and Function / Issue 1/2018
Print ISSN: 1863-2653
Electronic ISSN: 1863-2661
DOI
https://doi.org/10.1007/s00429-017-1478-z

Other articles of this Issue 1/2018

Brain Structure and Function 1/2018 Go to the issue

Original Article

Neuroanatomy of pain-deficiency and cross-modal activation in calcium channel subunit (CACN) α2δ3 knockout mice

Original Article

Keeping brains young with making music

Original Article

Long-term intensive gymnastic training induced changes in intra- and inter-network functional connectivity: an independent component analysis

Original Article

Neuronal connections of the central amygdalar nucleus with refeeding-activated brain areas in rats

Original Article

Sex differences in hippocampal damage, cognitive impairment, and trophic factor expression in an animal model of an alcohol use disorder

Original Article

Anatomo-functional correspondence in the superior temporal sulcus