Skip to main content
SpringerLink
Log in

Ontogenesis of Hypothalamic Neurons in Mammals

  • Chapter
  • First Online:
Neuroanatomy of Neuroendocrine Systems

Part of the book series: Masterclass in Neuroendocrinology ((MANEURO,volume 12))

Abstract

The hypothalamus is an essential component of brain circuits that control critical physiological functions. It plays a particularly important role in regulating energy balance and feeding behaviors. Accumulating evidence suggests that perturbations in hypothalamic development greatly contribute to obesity and metabolic diseases in later life. This chapter will discuss the timelines during which hypothalamic neurons develop, paying particular attention to neurons producing agouti-related peptide/neuropeptide Y, pro-opiomelanocortin, and oxytocin, because of their documented role in feeding regulation. It will also describe hormonal, molecular, and cellular factors related to the development of these neuronal systems. Finally, it will review the role of genetic and nutritional factors in hypothalamic development.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 189.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 249.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 249.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Similar content being viewed by others

Abbreviations

AgRP:

agouti-related peptide

AN:

accessory nucleus

ARH:

arcuate nucleus of the hypothalamus

ATG:

autophagy-related protein

AVP:

arginine vasopressin

BNST:

bed nucleus of the stria terminalis

CTR:

calcitonin receptor

DIO:

diet-induced obesity

DMH:

dorsomedial nucleus of the hypothalamus

E:

embryonic day

ERK:

extracellular signal-regulated kinase

GHSR:

growth hormone secretagogue receptor

GLP1:

glucagon-like peptide 1

GLP1-R:

glucagon-like peptide 1 receptor

HFD:

high-fat diet

LepR:

leptin receptor

LHA:

lateral hypothalamic area

MC4-R:

melanocortin 4 receptor

MRI:

magnetic resonance imaging

MTII:

melanotan II

NPY:

neuropeptide Y

OT:

oxytocin

OTR:

oxytocin receptor

P:

postnatal day

POMC:

pro-opiomelanocortin

PVH:

paraventricular nucleus of the hypothalamus

PWS:

Prader-Willi Syndrome

RAMP:

receptor activity-modifying protein

SCN:

suprachiasmatic nucleus

SON:

supraoptic nucleus

STAT:

signal transducer and activator of transcription

VMH:

ventromedial nucleus of the hypothalamus

Y1R:

neuropeptide Y receptor 1

αMSH:

alpha melanocyte-stimulating hormone

References

  • Abegg K, Hermann A, Boyle CN, Bouret SG, Lutz TA, Riediger T (2017) Involvement of amylin and leptin in the development of projections from the area postrema to the nucleus of the solitary tract. Front Endocrinol (Lausanne) 8:324

    Article  PubMed  PubMed Central  Google Scholar 

  • Acampora D, Postiglione MP, Avantaggiato V, Di Bonito M, Vaccarino FM, Michaud J, Simeone A (1999) Progressive impairment of developing neuroendocrine cell lineages in the hypothalamus of mice lacking the Orthopedia gene. Genes Dev 13:2787–2800

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ackland J, Ratter S, Bourne GL, Rees LH (1983) Characterization of immunoreactive somatostatin in human fetal hypothalamic tissue. Regul Pept 5:95–101

    Article  CAS  PubMed  Google Scholar 

  • Ahima RS, Hileman SM (2000) Postnatal regulation of hypothalamic neuropeptide expression by leptin: implications for energy balance and body weight regulation. Regul Pept 92:1–7

    Article  CAS  PubMed  Google Scholar 

  • Ahima R, Prabakaran D, Flier J (1998) Postnatal leptin surge and regulation of circadian rhythm of leptin by feeding. Implications for energy homeostasis and neuroendocrine function. J Clin Invest 101:1020–1027

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Alstein M, Whitnall MH, House S, Key S, Gainer H (1988) An immunochemical analysis of oxytocin and vasopressin prohormone processing in vivo. Peptides 9:87–105

    Article  CAS  PubMed  Google Scholar 

  • Althammer F, Grinevich V (2017) Diversity of oxytocin neurons: beyond magno- and parvocellular cell types? J Neuroendocrinol

    Google Scholar 

  • Altman J, Bayer SA (1986) The development of the rat hypothalamus. Adv Anat Embryol Cell Biol 100:1–178

    Article  CAS  PubMed  Google Scholar 

  • Anthwal N, Pelling M, Claxton S, Mellitzer G, Collin C, Kessaris N, Richardson WD, Gradwohl G, Ang SL (2013) Conditional deletion of neurogenin-3 using Nkx2.1iCre results in a mouse model for the central control of feeding, activity and obesity. Dis Model Mech 6:1133–1145

    CAS  PubMed  PubMed Central  Google Scholar 

  • Atasoy D, Betley JN, Su HH, Sternson SM (2012) Deconstruction of a neural circuit for hunger. Nature 488:172–177

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Aujla PK, Naratadam GT, Xu L, Raetzman LT (2013) Notch/Rbpjκ signaling regulates progenitor maintenance and differentiation of hypothalamic arcuate neurons. Development 140:3511–3521

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bochukova EG, Lawler K, Croizier S, Keogh JM, Patel N, Strohbehn G, Lo KK, Humphrey J, Hokken-Koelega A, Damen L, Donze S, Bouret SG, Plagnol V, Farooqi IS (2018) A transcriptomic signature of the hypothalamic response to fasting and BDNF deficiency in Prader-Willi syndrome. Cell Rep 22:3401–3408

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bouret S, Simerly RB (2007) Development of leptin-sensitive circuits. J Neuroendocrinol 19:575–582

    Article  CAS  PubMed  Google Scholar 

  • Bouret SG, Draper SJ, Simerly RB (2004a) Formation of projection pathways from the arcuate nucleus of the hypothalamus to hypothalamic regions implicated in the neural control of feeding behavior in mice. J Neurosci 24:2797–2805

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bouret SG, Draper SJ, Simerly RB (2004b) Trophic action of leptin on hypothalamic neurons that regulate feeding. Science 304:108–110

    Article  CAS  PubMed  Google Scholar 

  • Bouret SG, Gorski JN, Patterson CM, Chen S, Levin BE, Simerly RB (2008) Hypothalamic neural projections are permanently disrupted in diet-induced obese rats. Cell Metab 7:179–185

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bouret SG, Bates SH, Chen S, Myers MG, Simerly RB (2012) Distinct roles for specific leptin receptor signals in the development of hypothalamic feeding circuits. J Neurosci 32:1244–1252

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bray GA, York DA (1979) Hypothalamic and genetic obesity in experimental animals: an autonomic and endocrine hypothesis. Physiol Rev 59

    Google Scholar 

  • Brischoux F, Fellman D, Risold P-Y (2001a) Ontogenetic development of the diencephalic MCH neurons: a hypothalamic ‘MCH area’ hypothesis. Eur J Neurosci 13:1733–1744

    Article  CAS  PubMed  Google Scholar 

  • Brischoux F, Fellmann D, Risold PY (2001b) Ontogenetic development of the diencephalic MCH neurons: a hypothalamic ‘MCH area’ hypothesis. Eur J Neurosci 13:1733–1744

    Article  CAS  PubMed  Google Scholar 

  • Buffington SA, Di Prisco GV, Auchtung TA, Ajami NJ, Petrosino JF, Costa-Mattioli M (2016) Microbial reconstitution reverses maternal diet-induced social and synaptic deficits in offspring. Cell 165:1762–1775

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bugnon C, Fellmann D, Bresson JL, Clavequin MC (1982) Immunocytochemical study of the ontogenesis of the CRH-containing neuroglandular system in the human hypothalamus. CR Acad Sci 294

    Google Scholar 

  • Burford GD, Robinson IC (1982) Oxytocin, vasopressin and neurophysins in the hypothalamo-neurohypophysial system of the human fetus. J Endocrinol 95:403–408

    Article  CAS  PubMed  Google Scholar 

  • Campfield LA, Smith FJ, Guisez Y, Devos R, Burn P (1995) Recombinant mouse OB protein: evidence for a peripheral signal linking adiposity and central neural networks. Science 269:546–549

    Article  CAS  PubMed  Google Scholar 

  • Capuano CA, Leibowitz SF, BARR GA (1993) Effect of paraventricular injection of neuropeptide Y on milk and water intake of preweanling rat. Neuropeptides 24:177–182

    Article  CAS  PubMed  Google Scholar 

  • Caqueret A, Boucher F, Michaud JL (2006) Laminar organization of the early developing anterior hypothalamus. Dev Biol 298:95–106

    Article  CAS  PubMed  Google Scholar 

  • Caron E, Sachot C, Prevot V, Bouret SG (2010) Distribution of leptin-sensitive cells in the postnatal and adult mouse brain. J Comp Neurol 518:459–476

    Article  CAS  PubMed  Google Scholar 

  • Carreno G, Apps JR, Lodge EJ, Panousopoulos L, Haston S, Gonzalez-Meljem JM, Hahn H, Andoniadou CL, Martinez-Barbera JP (2017) Hypothalamic sonic hedgehog is required for cell specification and proliferation of LHX3/LHX4 pituitary embryonic precursors. Development 144:3289–3302

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chen H, Charlat O, Tartaglia LA, Woolf EA, Weng X, Ellis SJ, Lakey ND, Culpepper J, More KJ, Breitbart RE (1996) Evidence that the diabetes gene encodes the leptin receptor: identification of a mutation in the leptin receptor gene in db/db mice. Cell 84:491–495

    Article  CAS  PubMed  Google Scholar 

  • Chen H, Simar D, Morris MJ (2009) Hypothalamic neuroendocrine circuitry is programmed by maternal obesity: interaction with postnatal nutritional environment. PLoS One 4:e6259

    Article  PubMed  PubMed Central  Google Scholar 

  • Coggeshall RE (1964) A study of diencephalic development in the albino rat. J Comp Neurol 122:241–269

    Article  CAS  PubMed  Google Scholar 

  • Cohen P, Zhao C, Cai X, Montez JM, Rohani SC, Feinstein P, Mombaerts P, Friedman JM (2001) Selective deletion of leptin receptor in neurons leads to obesity. J Clin Invest 108:1113–1121

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Coleman DL (1973) Effects of parabiosis of obese with diabetes and normal mice. Diabetologia 9:294–298

    Article  CAS  PubMed  Google Scholar 

  • Coleman DL, Hummel KP (1969) Effects of parabiosis of normal with genetically diabetic mice. Diabetologia Am J Physiol:1298–1304

    Google Scholar 

  • Coupe B, Ishii Y, Dietrich MO, Komatsu M, Horvath TL, Bouret SG (2012) Loss of autophagy in pro-opiomelanocortin neurons perturbs axon growth and causes metabolic dysregulation. Cell Metab 15:247–255

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cowley MA, Smith RG, Diano S, Tschop M, Pronchuk N, Grove K, Strasburger G, Bidlingmaier M, Esterman M, Heiman ML, Garcia-Segura LM, Nillni EA, Mendez P, Low MJ, Sotonyi P, Friedman JM, Liu H, Pinto S, Colmers WF, Cone RD, Horvath T (2003) The distribution and mechanism of action of ghrelin in the CNS demonstrates a novel hypothalamic circuits regulating energy homeostasis. Neuron 37:649–661

    Article  CAS  PubMed  Google Scholar 

  • Croizier S, Franchi-Bernard G, Colard C, Poncet F, La Roche A, Risold P-Y (2010) A comparative analysis shows morphofunctional differences between the rat and mouse melanin-concentrating hormone systems. PLoS One 5:e15471

    Article  PubMed  PubMed Central  Google Scholar 

  • Croizier S, Amiot C, Chen X, Presse Fß, Nahon J-L, Wu JY, Fellmann D, Risold P-Y (2011) Development of posterior hypothalamic neurons enlightens a switch in the prosencephalic basic plan. PLoS One 6:e28574

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Croizier S, Park S, Maillard J, Bouret SG (2018) Central dicer-miR-103/107 controls developmental switch of POMC progenitors into NPY neurons and impacts glucose homeostasis. elife 7

    Google Scholar 

  • Daikoku S, Okamura Y, Kawano H, Tsuruo Y, Maegawa M, Shibasaki T (1984) Immunohistochemical study on the development of CRF-containing neurons in the hypothalamus of the rat. Cell Tissue Res 238:539–544

    Article  CAS  PubMed  Google Scholar 

  • de Luca C, Kowalski TJ, Zhang Y, Elmquist JK, Lee C, Kilimann MW, Ludwig T, Liu S-M, Chua SC Jr (2005) Complete rescue of obesity, diabetes, and infertility in db/db mice by neuron-specific LEPR-B transgenes. J Clin Invest 115:3484–3493

    Article  PubMed  PubMed Central  Google Scholar 

  • Dearden L, Buller S, Furigo IC, Fernandez-Twinn DS, Ozanne SE (2020) Maternal obesity causes fetal hypothalamic insulin resistance and disrupts development of hypothalamic feeding pathways. Mol Metab 42:101079

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Diaz C, Puelles L (2020) Developmental genes and malformations in the hypothalamus. Front Neuroanat 14:607111

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dongen VPAM, Nieuwenhuys R (1989) Diencephalon. In: Dubbeldam JL, Van Dongen PAM, Voogd J (eds) The central nervous system of vertebrates, vol 3. Springer, Berlin, pp 1844–1871

    Google Scholar 

  • Drucker DJ (1998) Glucagon-like peptides. Diabetes 47:159–169

    Article  CAS  PubMed  Google Scholar 

  • Eliava M, Melchior M, Knobloch-Bollmann HS, Wahis J, da Silva Gouveia M, Tang Y, Ciobanu AC, Triana del Rio R, Roth LC, Althammer F, Chavant V, Goumon Y, Gruber T, Petit-Demouliere N, Busnelli M, Chini B, Tan LL, Mitre M, Froemke RC, Chao MV, Giese G, Sprengel R, Kuner R, Poisbeau P, Seeburg PH, Stoop R, Charlet A, Grinevich V (2016) A new population of parvocellular oxytocin neurons controlling magnocellular neuron activity and inflammatory pain processing. Neuron 89:1291–1304

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fuchs JL, Schwark HD (2004) Neuronal primary cilia: a review. Cell Biol Int 28:111–118

    Article  CAS  PubMed  Google Scholar 

  • Geng X, Speirs C, Lagutin O, Inbal A, Liu W, Solnica-Krezel L, Jeong Y, Epstein DJ, Oliver G (2008) Haploinsufficiency of Six3 fails to activate Sonic hedgehog expression in the ventral forebrain and causes holoprosencephaly. Dev Cell 15:236–247

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gervais M, Labouèbe G, Picard A, Thorens B, Croizier S (2020) EphrinB1 modulates glutamatergic inputs into POMC-expressing progenitors and controls glucose homeostasis. PLoS Biol 18:e3000680

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gimpl G, Fahrenholz F (2001) The oxytocin receptor system: structure, function, and regulation. Physiol Rev 81:629–683

    Article  CAS  PubMed  Google Scholar 

  • Glavas MM, Joachim SE, Draper SJ, Smith MS, Grove KL (2007) Melanocortinergic activation by melanotan II inhibits feeding and increases uncoupling protein 1 messenger ribonucleic acid in the developing rat. Endocrinology 148:3279–3287

    Article  CAS  PubMed  Google Scholar 

  • Glendining KA, Jasoni CL (2019) Maternal high fat diet-induced obesity modifies histone binding and expression of Oxtr in offspring hippocampus in a sex-specific manner. Int J Mol Sci 20

    Google Scholar 

  • Godefroy D, Dominici C, Hardin-Pouzet H, Anouar Y, Melik-Parsadaniantz S, Rostene W, Reaux-Le Goazigo A (2017) Three-dimensional distribution of tyrosine hydroxylase, vasopressin and oxytocin neurones in the transparent postnatal mouse brain. J Neuroendocrinol 29

    Google Scholar 

  • Goldstone AP, Unmehopa UA, Bloom SR, Swaab DF (2002) Hypothalamic NPY and agouti-related protein are increased in human illness but not in Prader-Willi syndrome and other obese subjects. J Clin Endocrinol Metabol 87:927–937

    Article  CAS  Google Scholar 

  • Goldstone AP, Unmehopa UA, Swaab DF (2003) Hypothalamic growth hormone-releasing hormone (GHRH) cell number is increased in human illness, but is not reduced in Prader-Willi syndrome or obesity. 58:8

    Google Scholar 

  • Goudsmit E, Neijmeijer-Leloux A, Swaab DF (1992) The human hypothalamo-neurohypophyseal system in relation to development, aging and Alzheimer’s disease. Prog Brain Res 93:237–247; discussion 247–238

    Google Scholar 

  • Grayson BE, Allen SE, Billes SK, Williams SM, Smith MS, Grove KL (2006) Prenatal development of hypothalamic neuropeptide systems in the nonhuman primate. Neuroscience 143:975–986

    Article  CAS  PubMed  Google Scholar 

  • Greenwood MA, Hammock EA (2017) Oxytocin receptor binding sites in the periphery of the neonatal mouse. PLoS One 12:e0172904

    Article  PubMed  PubMed Central  Google Scholar 

  • Grinevich V, Desarménien MG, Chini B, Tauber M, Muscatelli F (2015) Ontogenesis of oxytocin pathways in the mammalian brain: late maturation and psychosocial disorders. Front Neuroanat 8

    Google Scholar 

  • Grove KL, Allen S, Grayson BE, Smith MS (2003) Postnatal development of the hypothalamic neuropeptide Y system. Neuroscience 116:393–406

    Article  CAS  PubMed  Google Scholar 

  • Gutnick A, Blechman J, Kaslin J, Herwig L, Belting HG, Affolter M, Bonkowsky JL, Levkowitz G (2011) The hypothalamic neuropeptide oxytocin is required for formation of the neurovascular interface of the pituitary. Dev Cell 21:642–654

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Haddad-Tóvolli R, Altirriba J, Obri A, Sánchez EE, Chivite I, Milà-Guasch M, Ramírez S, Gómez-Valadés AG, Pozo M, Burguet J, Velloso LA, Claret M (2020) Pro-opiomelanocortin (POMC) neuron translatome signatures underlying obesogenic gestational malprogramming in mice. Mol Metab 36:100963

    Article  PubMed  PubMed Central  Google Scholar 

  • Halaas JL, Gajiwala KS, Maffei M, Cohen SL, Chait BT, Rabinowitz D, Lallone RL, Burley SK, Friedman JM (1995) Weight-reducing effects of the plasma protein encoded by the obese gene. Science 269:543–546

    Article  CAS  PubMed  Google Scholar 

  • Halaas JL, Boozer C, Blair-West J, Fidahusein N, Denton DA, Friedman JM (1997) Physiological response to long-term peripheral and central leptin infusion in lean and obese mice. PNAS 94:8878–8883

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hammock EA, Levitt P (2013) Oxytocin receptor ligand binding in embryonic tissue and postnatal brain development of the C57BL/6J mouse. Front Behav Neurosci 7:195

    Article  PubMed  PubMed Central  Google Scholar 

  • Hoffiz YC, Castillo-Ruiz A, Hall MAL, Hite TA, Gray JM, Cisternas CD, Cortes LR, Jacobs AJ, Forger NG (2021) Birth elicits a conserved neuroendocrine response with implications for perinatal osmoregulation and neuronal cell death. Sci Rep 11:2335

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Holm VA, Cassidy SB, Butler MG, Hanchett JM, Greenswag LR, Whitman BY, Greenberg F (1993) Prader-Willi syndrome: consensus diagnostic criteria. Pediatrics 91:398–402

    Article  CAS  PubMed  Google Scholar 

  • Holsen LM, Zarcone JR, Brooks WM, Butler MG, Thompson TI, Ahluwalia JS, Nollen NL, Savage CR (2006) Neural mechanisms underlying hyperphagia in Prader-Willi syndrome. Obesity 14:1028–1037

    Article  PubMed  Google Scholar 

  • Horvath TL, Sarman B, García-Cáceres C, Enriori PJ, Sotonyi P, Shanabrough M, Borok E, Argente J, Chowen JA, Perez-Tilve D, Pfluger PT, Brönneke HS, Levin BE, Diano S, Cowley MA, Tschöp MH (2010) Synaptic input organization of the melanocortin system predicts diet-induced hypothalamic reactive gliosis and obesity. Proc Natl Acad Sci USA 107:14875–14880

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hosoya T, Oda Y, Takahashi S, Morita M, Kawauchi S, Ema M, Yamamoto M, Fujii-Kuriyama Y (2001) Defective development of secretory neurones in the hypothalamus of Arnt2-knockout mice. Genes Cells 6:361–374

    Article  CAS  PubMed  Google Scholar 

  • Hu Y, Li J, Zhu Y, Li M, Lin J, Yang L, Wang C, Lu Z (2020) Development and characterization of an Otp conditional loss of function allele. Genesis (New York: 2000) 58, e23370

    Google Scholar 

  • Hyyppä M (1969) Differentiation of the hypothalamic nuclei during ontogenetic development in the rat. Z Anat Entwicklungsgesch 129:41–52

    Article  PubMed  Google Scholar 

  • Ifft JD (1972) An autoradiographic study of the time of final division of neurons in rat hypothalamic nuclei. J Comp Neurol 144:193–204

    Article  CAS  PubMed  Google Scholar 

  • Ishii Y, Bouret SG (2012) Embryonic birthdate of hypothalamic leptin-activated neurons in mice. Endocrinology 153:3657–3667

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Johnson K, Posner SF, Biermann J, Cordero JF, Atrash HK, Parker CS, Boulet S, Curtis MG, and Care, C.A.P.C.W.G.S.P.o.P (2006) Recommendations to improve preconception health and health care—United States. A report of the CDC/ATSDR Preconception Care Work Group and the Select Panel on Preconception Care MMWR Recomm Rep 55, 1–23

    Google Scholar 

  • Johnson MD, Bouret SG, Dunn-Meynell AA, Boyle CN, Lutz TA, Levin BE (2016) Early postnatal amylin treatment enhances hypothalamic leptin signaling and neural development in the selectively bred diet-induced obese rat. Am J Physiol Regul Integr Comp Physiol 311:R1032–r1044

    Article  PubMed  PubMed Central  Google Scholar 

  • Jurado MPMVaS (2020) Specification of oxytocinergic and vasopressinergic circuits in the developing mouse brain. BioRxiv https://doi.org/10.1101/2020.08.07.241364

  • Jurek B, Neumann ID (2018) The oxytocin receptor: from intracellular signaling to behavior. Physiol Rev 98:1805–1908

    Article  CAS  PubMed  Google Scholar 

  • Kamitakahara A, Bouyer K, Wang CH, Simerly R (2017) A critical period for the trophic actions of leptin on AgRP neurons in the arcuate nucleus of the hypothalamus. J Comp Neurol

    Google Scholar 

  • Keyser A (1979) Development of the hypothalamus in mammals. (New York)

    Google Scholar 

  • Khachaturian H, Alessi NE, Lewis ME, Munfakh N, Fitzsimmons MD, Watson SJ (1985) Development of hypothalamic opioid neurons: a combined immunocytochemical and [3H]thymidine autoradiographic study. Neuropeptides 5:477–480

    Article  CAS  PubMed  Google Scholar 

  • Kimura S, Hara Y, Pineau T, Fernandez-Salguero P, Fox CH, Ward JM, Gonzalez FJ (1996) The T/ebp null mouse: thyroid-specific enhancer-binding protein is essential for the organogenesis of the thyroid, lung, ventral forebrain, and pituitary. Genes Dev 10:60–69

    Article  CAS  PubMed  Google Scholar 

  • Kirk SL, Samuelsson A-M, Argenton M, Dhonye H, Kalamatianos T, Poston L, Taylor PD, Coen CW (2009) Maternal obesity induced by diet in rats permanently influences central processes regulating food intake in offspring. PLoS One 4:e5870

    Article  PubMed  PubMed Central  Google Scholar 

  • Klionsky DJ (2007) Autophagy: from phenomenology to molecular understanding in less than a decade. Nat Rev Mol Cell Biol 8:931–937

    Article  CAS  PubMed  Google Scholar 

  • Kojima M, Hosoda H, Date Y, Nakazato M, Matsuo H, Kangawa K (1999) Ghrelin is a growth-hormone-releasing acylated peptide from stomach. Nature 402:656–660

    Article  CAS  PubMed  Google Scholar 

  • Kokoeva MV, Yin H, Flier JS (2005) Neurogenesis in the hypothalamus of adult mice: potential role in energy balance. Science 310:679–683

    Article  CAS  PubMed  Google Scholar 

  • Kokoeva MV, Yin H, Flier JS (2007) Evidence for constitutive neural cell proliferation in the adult murine hypothalamus. J Comp Neurol 505:209–220

    Article  PubMed  Google Scholar 

  • Koutcherov Y, Mai JK, Ashwell KW, Paxinos G (2002) Organization of human hypothalamus in fetal development. J Comp Neurol 446:301–324

    Article  PubMed  Google Scholar 

  • Kowalski, T.J., Liu, S.-M., Leibel, R.L., and Chua, S.C., Jr. (2001). Transgenic complementation of leptin-receptor deficiency: I. Rescue of the obesity/diabetes phenotype of LEPR-null mice expressing a LEPR-B transgene diabetes 50, 425-435

    Google Scholar 

  • Kozlov SV, Bogenpohl JW, Howell MP, Wevrick R, Panda S, Hogenesch JB, Muglia LJ, Van Gelder RN, Herzog ED, Stewart CL (2007) The imprinted gene Magel2 regulates normal circadian output. Nat Genet 39:1266–1272

    Article  CAS  PubMed  Google Scholar 

  • Lagutin OV, Zhu CC, Kobayashi D, Topczewski J, Shimamura K, Puelles L, Russell HRC, McKinnon PJ, Solnica-Krezel L, Oliver G (2003) Six3 repression of Wnt signaling in the anterior neuroectoderm is essential for vertebrate forebrain development. Genes Dev 17:368–379

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee G-H, Proenca R, Montez JM, Carroll KM, Darvishzadeh JG, Lee JI, Friedman JM (1996) Abnormal splicing of the leptin receptor in diabetic mice. Nature 379:632–635

    Article  CAS  PubMed  Google Scholar 

  • Lee S, Kozlov S, Hernandez L, Chamberlain SJ, Brannan CI, Stewart CL, Wevrick R (2000) Expression and imprinting of MAGEL2 suggest a role in Prader–Willi syndrome and the homologous murine imprinting phenotype. Hum Mol Genet 9:1813–1819

    Article  CAS  PubMed  Google Scholar 

  • Lee S, Walker CL, Wevrick R (2003) Prader–Willi syndrome transcripts are expressed in phenotypically significant regions of the developing mouse brain. Gene Expr Patterns 3:599–609

    Article  CAS  PubMed  Google Scholar 

  • Lee HJ, Macbeth AH, Pagani JH, Young WS 3rd (2009) Oxytocin: the great facilitator of life. Prog Neurobiol 88:127–151

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lee B, Lee S, Lee SK, Lee JW (2016) The LIM-homeobox transcription factor Isl1 plays crucial roles in the development of multiple arcuate nucleus neurons. Development 143:3763–3773

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lee B, Kim J, An T, Kim S, Patel EM, Raber J, Lee SK, Lee S, Lee JW (2018) Dlx1/2 and Otp coordinate the production of hypothalamic GHRH- and AgRP-neurons. Nat Commun 9:2026

    Article  PubMed  PubMed Central  Google Scholar 

  • Lee CH, Song DK, Park CB, Choi J, Kang GM, Shin SH, Kwon I, Park S, Kim S, Kim JY, Dugu H, Park JW, Choi JH, Min SH, Sohn JW, Kim MS (2020) Primary cilia mediate early life programming of adiposity through lysosomal regulation in the developing mouse hypothalamus. Nat Commun 11:5772

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Levin BE, Dunn-Meynell AA, Balkan B, Keesey RE (1997) Selective breeding for diet-induced obesity and resistance in Sprague-Dawley rats. Am J Physiol Regul Integr Comp Physiol 273:R725–R730

    Article  CAS  Google Scholar 

  • Li C, Xu JJ, Hu HT, Shi CY, Yu CJ, Sheng JZ, Wu YT, Huang HF (2020) Amylin receptor insensitivity impairs hypothalamic POMC neuron differentiation in the male offspring of maternal high-fat diet-fed mice. Mol Metab 44:101135

    Article  PubMed  PubMed Central  Google Scholar 

  • Lu F, Kar D, Gruenig N, Zhang ZW, Cousins N, Rodgers HM, Swindell EC, Jamrich M, Schuurmans C, Mathers PH, Kurrasch DM (2013) Rax is a selector gene for mediobasal hypothalamic cell types. J Neurosci 33:259–272

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lutz TA, Coester B, Whiting L, Dunn-Meynell AA, Boyle CN, Bouret SG, Levin BE, Le Foll C (2018) Amylin selectively signals onto POMC neurons in the arcuate nucleus of the hypothalamus. Diabetes 67:805–817

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mai JK, Lensing-Hohn S, Ende AA, Safroniew MV (1997) Developmental organization of neurophysin neurons in the human brain. J Comp Neurol 385:477–489

    Article  CAS  PubMed  Google Scholar 

  • Maillard J, Park S, Croizier S, Vanacker C, Cook JH, Prevot V, Tauber M, Bouret SG (2016) Loss of Magel2 impairs the development of hypothalamic Anorexigenic circuits. Hum Mol Genet 25:3208–3215

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Makarenko IG, Ugrumov MV, Derer P, Calas A (2000) Projections from the hypothalamus to the posterior lobe in rats during ontogenesis: 1,1?-dioctadecyl-3,3,3?,3?-tetramethylindocarbocyanine perchlorate tracing study. J Comp Neurol 422:327–337

    Article  CAS  PubMed  Google Scholar 

  • Manning L, Ohyama K, Saeger B, Hatano O, Wilson SA, Logan M, Placzek M (2006) Regional morphogenesis in the hypothalamus: a BMP-Tbx2 pathway coordinates fate and proliferation through Shh downregulation. Dev Cell 11:873–885

    Article  CAS  PubMed  Google Scholar 

  • Marín O, Baker J, Puelles L, Rubenstein JLR (2002) Patterning of the basal telencephalon and hypothalamus is essential for guidance of cortical projections. Development 129:761–773

    Article  PubMed  Google Scholar 

  • Matsumoto A, Arai Y (1976) Developmental changes in synaptic formation in the hypothalamic arcuate nucleus of female rats. Cell Tissue Res 14:143–156

    Google Scholar 

  • McClellana KM, Parker KL, Tobet SA (2006) Development of the ventromedial nucleus of the hypothalamus. Front Neuroendocrinol 27:193–209

    Article  Google Scholar 

  • McMinn JE, Liu S-M, Liu H, Dragatsis I, Dietrich P, Ludwig T, Boozer CN, Chua SC Jr (2005) Neuronal deletion of Lepr elicits diabesity in mice without affecting cold tolerance or fertility. Am J Physiol Endocrinol Metab 289:E403–E411

    Article  CAS  PubMed  Google Scholar 

  • McNay DEG, Pelling M, Claxton S, Guillemot Fß, Ang S-L (2006) Mash1 is required for generic and subtype differentiation of hypothalamic neuroendocrine cells. Mol Endocrinol 20:1623–1632

    Article  CAS  PubMed  Google Scholar 

  • 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 Invest 122:142–152

    Article  CAS  PubMed  Google Scholar 

  • Melnick I, Pronchuck N, Cowley MA, Grove KL, Colmers WF (2007) Developmental switch in neuropeptide Y and melanocortin effects in the paraventricular nucleus of the hypothalamus. Neuron 56:1103–1115

    Article  CAS  PubMed  Google Scholar 

  • Mercer RE, Kwolek EM, Bischof JM, van Eede M, Henkelman RM, Wevrick R (2009) Regionally reduced brain volume, altered serotonin neurochemistry, and abnormal behavior in mice null for the circadian rhythm output gene Magel2. Am J Med Genet B Neuropsychiatr Genet 150B:1085–1099

    Article  CAS  PubMed  Google Scholar 

  • Mercer RE, Michaelson SD, Chee MJS, Atallah TA, Wevrick R, Colmers WF (2013) Magel2 Is required for leptin-mediated depolarization of POMC neurons in the hypothalamic arcuate nucleus in mice. PLoS Genet 9:e1003207

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Meziane H, Schaller F, Bauer S, Villard C, Matarazzo V, Riet F, Guillon G, Lafitte D, Desarmenien MG, Tauber M, Muscatelli F (2015) An early postnatal oxytocin treatment prevents social and learning deficits in adult mice deficient for Magel2, a gene involved in Prader-Willi syndrome and autism. Biol Psychiatry 78:85–94

    Article  CAS  PubMed  Google Scholar 

  • Michaud JL, DeRossi C, May NR, Holdener BC, Fan CM (2000) ARNT2 acts as the dimerization partner of SIM1 for the development of the hypothalamus. Mech Dev 90:253–261

    Article  CAS  PubMed  Google Scholar 

  • Miller JL, Couch JA, Schmalfuss I, He G, Liu Y, Driscoll DJ (2007) Intracranial abnormalities detected by three-dimensional magnetic resonance imaging in Prader–Willi syndrome. Am J Med Genet A 143A:476–483

    Article  PubMed  Google Scholar 

  • Miriam Altstein MHW, House S, Key S, Gainer H (1988) An immunochemical analysis of oxytocin and vasopressin prohormone processing in vivo. Peptides 9:87–105

    Article  Google Scholar 

  • Mistry A, Swick A, Romsos D (1999) Leptin alters metabolic rates before acquisition of its anorectic effect in developing neonatal mice. Am J Phys 277:R742–R747

    CAS  Google Scholar 

  • Mountjoy KG, Wild JM (1998) Melanocortin-4 receptor mRNA expression in the developing autonomic and central nervous systems. Dev Brain Res 107:309–314

    Article  CAS  Google Scholar 

  • Nakai S, Kawano H, Yudate T, Nishi M, Kuno J, Nagata A, Jishage K, Hamada H, Fujii H, Kawamura K et al (1995) The POU domain transcription factor Brn-2 is required for the determination of specific neuronal lineages in the hypothalamus of the mouse. Genes Dev 9:3109–3121

    Article  CAS  PubMed  Google Scholar 

  • Nakazato M, Murakami N, Date Y, Kojima M, Matsuo H, Kangawa K, Matsukura S (2001) A role for ghrelin in the central regulation of feeding. Nature 409:194–198

    Article  CAS  PubMed  Google Scholar 

  • Nasif S, de Souza FS, González LE, Yamashita M, Orquera DP, Low MJ, Rubinstein M (2015) Islet 1 specifies the identity of hypothalamic melanocortin neurons and is critical for normal food intake and adiposity in adulthood. Proc Natl Acad Sci USA 112:E1861–E1870

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Newmaster KT, Nolan ZT, Chon U, Vanselow DJ, Weit AR, Tabbaa M, Hidema S, Nishimori K, Hammock EAD, Kim Y (2020) Quantitative cellular-resolution map of the oxytocin receptor in postnatally developing mouse brains. Nat Commun 11:1885

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nilsson I, Johansen JE, Schalling M, Hˆkfelt T, Fetissov SO (2005a) Maturation of the hypothalamic arcuate agouti-related protein system during postnatal development in the mouse. Dev Brain Res 155:147–154

    Article  CAS  Google Scholar 

  • Nilsson I, Johansen JE, Schalling M, Hokfelt T, Fetissov SO (2005b) Maturation of the hypothalamic arcuate agouti-related protein system during postnatal development in the mouse. Dev Brain Res 155:147–154

    Article  CAS  Google Scholar 

  • Orquera DP, Tavella MB, de Souza FSJ, Nasif S, Low MJ, Rubinstein M (2019) The homeodomain transcription factor NKX2.1 is essential for the early specification of melanocortin neuron identity and activates Pomc expression in the developing hypothalamus. J Neurosci 39:4023–4035

    Article  PubMed  PubMed Central  Google Scholar 

  • Padilla SL, Carmody JS, Zeltser LM (2010) Pomc-expressing progenitors give rise to antagonistic neuronal populations in hypothalamic feeding circuits. Nat Med 16:403–405

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Park S, Aintablian A, Coupe B, Bouret SG (2020a) The endoplasmic reticulum stress-autophagy pathway controls hypothalamic development and energy balance regulation in leptin-deficient neonates. Nat Commun 11:1914

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Park S, Jang A, Bouret SG (2020b) Maternal obesity-induced endoplasmic reticulum stress causes metabolic alterations and abnormal hypothalamic development in the offspring. PLoS Biol 18:e3000296

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pelleymounter M, Cullen M, Baker M, Hecht R, Winters D, Boone T, F, C. (1995) Effects of the obese gene product on body weight regulation in ob/ob mice. Science 269:540–543

    Article  CAS  PubMed  Google Scholar 

  • Pelling M, Anthwal N, McNay D, Gradwohl G, Leiter AB, Guillemot F, Ang SL (2011) Differential requirements for neurogenin 3 in the development of POMC and NPY neurons in the hypothalamus. Dev Biol 349:406–416

    Article  CAS  PubMed  Google Scholar 

  • Peng CY, Mukhopadhyay A, Jarrett JC, Yoshikawa K, Kessler JA (2012) BMP receptor 1A regulates development of hypothalamic circuits critical for feeding behavior. J Neurosci 32:17211–17224

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Piao H, Hosoda H, Kangawa K, Murata T, Narita K, Higuchi T (2008) Ghrelin stimulates milk intake by affecting adult type feeding behaviour in postnatal rats. J Neuroendocrinol 20:330–334

    Article  CAS  PubMed  Google Scholar 

  • Pinto S, Roseberry AG, Liu H, Diano S, Shanabrough M, Cai X, Friedman JM, Horvath TL (2004) Rapid rewiring of arcuate nucleus feeding circuits by leptin. Science 304:110–115

    Article  CAS  PubMed  Google Scholar 

  • Prader A, Labhart A, Willi H (1956) Ein syndrom von adipositas, kleinwuchskryptorchismus und oligophrenie nach myatonieartigem zustand im neugeborenenalter. Scweiz Med Wochenschr 86:1260–1261

    Google Scholar 

  • Pravdivyi I, Ballanyi K, Colmers WF, Wevrick R (2015) Progressive postnatal decline in leptin sensitivity of arcuate hypothalamic neurons in the Magel2-null mouse model of Prader–Willi syndrome. Hum Mol Genet 24:4276–4283

    Article  CAS  PubMed  Google Scholar 

  • Proulx K, Richard D, Walker C-D (2002) Leptin regulates appetite-related neuropeptides in the hypothalamus of developing rats without affecting food intake. Endocrinology 143:4683–4692

    Article  CAS  PubMed  Google Scholar 

  • Quarta C, Fisette A, Xu Y, Colldén G, Legutko B, Tseng YT, Reim A, Wierer M, De Rosa MC, Klaus V, Rausch R, Thaker VV, Graf E, Strom TM, Poher AL, Gruber T, Le Thuc O, Cebrian-Serrano A, Kabra D, Bellocchio L, Woods SC, Pflugfelder GO, Nogueiras R, Zeltser L, Grunwald Kadow IC, Moon A, García-Cáceres C, Mann M, Treier M, Doege CA, Tschöp MH (2019) Functional identity of hypothalamic melanocortin neurons depends on Tbx3. Nat Metab 1:222–235

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rakic P, Cameron RS, Komuro H (1994) Recognition, adhesion, transmembrane signaling and cell motility in guided neuronal migration. Curr Opin Neurobiol 4:63–69

    Article  CAS  PubMed  Google Scholar 

  • Risold PY, Croizier S, Legagneux K, Brischoux F, Fellmann D, Griffond B (2009) The development of the MCH system. Peptides 30:1969–1972

    Article  CAS  PubMed  Google Scholar 

  • Rozo AV, Babu DA, Suen PA, Groff DN, Seeley RJ, Simmons RA, Seale P, Ahima RS, Stoffers DA (2017) Neonatal GLP1R activation limits adult adiposity by durably altering hypothalamic architecture. Mol Metab 6:748–759

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Saper CB, Swanson LW, Cowan WM (1979) An autoradiographic study of the efferent connections of the lateral hypothalamic area in the rat. J Comp Neurol 183:689–706

    Article  CAS  PubMed  Google Scholar 

  • Sauer FC (1935) Mitosis in the neural tube. J Comp Neurol 62:377–405

    Article  Google Scholar 

  • Sawchenko PE (1998) Toward a new neurobiology of energy balance, appetite, and obesity: the anatomists weigh in. J Comp Neurol 402:435–441

    Article  CAS  PubMed  Google Scholar 

  • Sawchenko PE, Swanson LW (1983) The organization of forebrain afferents to the paraventricular and supraoptic nuclei of the rat. J Comp Neurol 218:121–144

    Article  CAS  PubMed  Google Scholar 

  • Schaller F, Watrin F, Sturny R, Massacrier A, Szepetowski P, Muscatelli F (2010) A single postnatal injection of oxytocin rescues the lethal feeding behaviour in mouse newborns deficient for the imprinted Magel2 gene. Hum Mol Genet 19:4895–4905

    Article  CAS  PubMed  Google Scholar 

  • Schmidt I, Fritz A, Scholch C, Schneider D, Simon E, Plagemann A (2001) The effect of leptin treatment on the development of obesity in overfed suckling Wistar rats. Int J Obes Relat Metab Disorders 25:1168–1174

    Article  CAS  Google Scholar 

  • Schonemann MD, Ryan AK, McEvilly RJ, O'Connell SM, Arias CA, Kalla KA, Li P, Sawchenko PE, Rosenfeld MG (1995) Development and survival of the endocrine hypothalamus and posterior pituitary gland requires the neuronal POU domain factor Brn-2. Genes Dev 9:3122–3135

    Article  CAS  PubMed  Google Scholar 

  • Shapira NA, Lessig MC, He AG, James GA, Driscoll DJ, Liu Y (2005) Satiety dysfunction in Prader-Willi syndrome demonstrated by fMRI. J Neurol Neurosurg Psychiatry 76:260–262

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shimada M, Nakamura T (1973) Time of neuron origin in mouse hypothalamic nuclei. Exp Neurol 41:163–173

    Article  CAS  PubMed  Google Scholar 

  • Shimogori T, Lee DA, Miranda-Angulo A, Yang Y, Wang H, Jiang L, Yoshida AC, Kataoka A, Mashiko H, Avetisyan M, Qi L, Qian J, Blackshaw S (2010) A genomic atlas of mouse hypothalamic development. Nat Neurosci 13:767–775

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Silverman A-J, Goldstein R, Gadde CA (1980) The ontogenesis of neurophysin-containing neurons in the mouse hypothalamus. Peptides 1:27–44

    Article  CAS  Google Scholar 

  • Steculorum SM, Bouret SG (2011) Maternal diabetes compromises the organization of hypothalamic feeding circuits and impairs leptin sensitivity in offspring. Endocrinology 152:4171–4179

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Steculorum SM, Collden G, Coupe B, Croizier S, Andrews Z, Jarosch F, Klussmann S, Bouret SG (2015) Ghrelin programs development of hypothalamic feeding circuits. J Clin Invest 125:846–858

    Article  PubMed  PubMed Central  Google Scholar 

  • Sun L, Lizneva D, Ji Y, Colaianni G, Hadelia E, Gumerova A, Ievleva K, Kuo TC, Korkmaz F, Ryu V, Rahimova A, Gera S, Taneja C, Khan A, Ahmad N, Tamma R, Bian Z, Zallone A, Kim SM, New MI, Iqbal J, Yuen T, Zaidi M (2019) Oxytocin regulates body composition. Proc Natl Acad Sci USA 116:26808–26815

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sussel L, Marin O, Kimura S, Rubenstein JL (1999) Loss of Nkx2.1 homeobox gene function results in a ventral to dorsal molecular respecification within the basal telencephalon: evidence for a transformation of the pallidum into the striatum. Development 126:3359–3370

    Article  CAS  PubMed  Google Scholar 

  • Swaab DF, Purba JS, Hofman MA (1995) Alterations in the hypothalamic paraventricular nucleus and its oxytocin neurons (putative satiety cells) in Prader-Willi syndrome: a study of five cases. J Clin Endocrinol Metabol 80:573–579

    CAS  Google Scholar 

  • Swanson LW, Kuypers HG (1980) The paraventricular nucleus of the hypothalamus: cytoarchitectonic subdivisions and organization of projections to the pituitary, dorsal vagal complex, and spinal cord as demonstrated by retrograde fluorescence double-labeling methods. J Comp Neurol 194:555–570

    Article  CAS  PubMed  Google Scholar 

  • Takebayashi H, Yoshida S, Sugimori M, Kosako H, Kominami R, Nakafuku M, Nabeshima Y (2000) Dynamic expression of basic helix-loop-helix Olig family members: implication of Olig2 in neuron and oligodendrocyte differentiation and identification of a new member, Olig3. Mech Dev 99:143–148

    Article  CAS  PubMed  Google Scholar 

  • Tamborski S, Mintz EM, Caldwell HK (2016) Sex differences in the embryonic development of the central oxytocin system in mice. J Neuroendocrinol 28

    Google Scholar 

  • Tessier-Lavigne M, Goodman CS (1996) The molecular biology of axon guidance. Science 274:1123–1133

    Article  CAS  PubMed  Google Scholar 

  • Tolle V, Zizzari P, Tomasetto C, Rio MC, Epelbaum J, Bluet-Pajot MT (2001) In vivo and in vitro effects of ghrelin/motilin-related peptide on growth hormone secretion in the rat. Neuroendocrinology 73:54–61

    Article  CAS  PubMed  Google Scholar 

  • Tribollet E, Charpak S, Schmidt A, Dubois-Dauphin M, Dreifuss JJ (1989) Appearance and transient expression of oxytocin receptors in fetal, infant, and peripubertal rat brain studied by autoradiography and electrophysiology. J Neurosci 9:1764–1773

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tschöp M, Smiley DL, Heiman ML (2000) Ghrelin induces adiposity in rodent. Nature:908–913

    Google Scholar 

  • Vaidyanathan R, Hammock EA (2017) Oxytocin receptor dynamics in the brain across development and species. Dev Neurobiol 77:143–157

    Article  CAS  PubMed  Google Scholar 

  • van der Klaauw AA, Croizier S, Mendes de Oliveira E, Stadler LKJ, Park S, Kong Y, Banton MC, Tandon P, Hendricks AE, Keogh JM, Riley SE, Papadia S, Henning E, Bounds R, Bochukova EG, Mistry V, O'Rahilly S, Simerly RB, Minchin JEN, Barroso I, Jones EY, Bouret SG, Farooqi IS (2019) Human Semaphorin 3 variants link melanocortin circuit development and energy balance. Cell 176:729–742.e718

    Google Scholar 

  • van Eerdenburg FJ, Rakic P (1994) Early neurogenesis in the anterior hypothalamus of the rhesus monkey. Brain Res Dev Brain Res 79:290–296

    Article  PubMed  Google Scholar 

  • Vogt MC, Paeger L, Hess S, Steculorum SM, Awazawa M, Hampel B, Neupert S, Nicholls HT, Mauer J, Hausen AC, Predel R, Kloppenburg P, Horvath TL, Brüning JC (2014) Neonatal insulin action impairs hypothalamic neurocircuit formation in response to maternal high-fat feeding. Cell 156:495–509

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vuong HE, Pronovost GN, Williams DW, Coley EJL, Siegler EL, Qiu A, Kazantsev M, Wilson CJ, Rendon T, Hsiao EY (2020) The maternal microbiome modulates fetal neurodevelopment in mice. Nature 586:281–286

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang W, Lufkin T (2000) The murine Otp homeobox gene plays an essential role in the specification of neuronal cell lineages in the developing hypothalamus. Dev Biol 227:432–449

    Article  CAS  PubMed  Google Scholar 

  • Wasinski F, Furigo IC, Teixeira PDS, Ramos-Lobo AM, Peroni CN, Bartolini P, List EO, Kopchick JJ, Donato J Jr (2020) Growth hormone receptor deletion reduces the density of axonal projections from hypothalamic arcuate nucleus neurons. Neuroscience 434:136–147

    Article  CAS  PubMed  Google Scholar 

  • Whittington JE, Holland AJ, Webb T, Butler J, Clarke D, Boer H (2001) Population prevalence and estimated birth incidence and mortality rate for people with Prader-Willi syndrome in one UK Health Region. J Med Genet 38:792–798

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Widmer H, Amerdeil H, Fontanaud P, Desarménien MG (1997) Postnatal maturation of rat hypothalamoneurohypophysial neurons: evidence for a developmental decrease in calcium entry during action potentials. J Neurophysiol 77:260–271

    Article  CAS  PubMed  Google Scholar 

  • Wu TJ, Gibson MJ, Rogers MC, Silverman AJ (1997) New observations on the development of the gonadotropin-releasing hormone system in the mouse. J Neurobiol 33:983–998

    Article  CAS  PubMed  Google Scholar 

  • Yee CL, Wang Y, Anderson S, Ekker M, Rubenstein JLR (2009) Arcuate nucleus expression of NKX2.1 and DLX and lineages expressing these transcription factors in neuropeptide Y+, proopiomelanocortin+, and tyrosine hydroxylase+ neurons in neonatal and adult mice. J Comp Neurol 517:37–50

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yoshimura R, Kimura T, Watanabe D, Kiyama H (1996) Differential expression of oxytocin receptor mRNA in the developing rat brain. Neurosci Res 24:291–304

    Article  CAS  PubMed  Google Scholar 

  • Zhang Y, Proenca R, Maffel M, Barone M, Leopold L, Friedman JM (1994) Position cloning of the mouse obese gene and its human homologue. Nature 372:425

    Article  CAS  PubMed  Google Scholar 

  • Zhou Q, Wang S, Anderson DJ (2000) Identification of a novel family of oligodendrocyte lineage-specific basic helix-loop-helix transcription factors. Neuron 25:331–343

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Inserm, Laboratory of Development and Plasticity of the Neuroendocrine Brain, Lille Neuroscience & Cognition Research Center, Lille, France

    Sebastien G. Bouret

  2. University of Lille, FHU 1,000 Days for Health, Lille, France

    Sebastien G. Bouret

  3. Institut de Neurobiologie de la Méditerranée, INSERM, U1249, Aix Marseille University, Marseille, France

    Françoise Muscatelli

Authors
  1. Sebastien G. Bouret
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Françoise Muscatelli
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Sebastien G. Bouret or Françoise Muscatelli .

Editor information

Editors and Affiliations

  1. Department of Neuropeptide Research in Psychiatry, Central Institute of Mental Health, University of Heidelberg, Mannheim, Baden-Württemberg, Germany

    Valery Grinevich

  2. Department of Physiology & Neurobiology, Eötvös Loránd University, Budapest, Hungary

    Árpád Dobolyi

Rights and permissions

Reprints and permissions

Copyright information

© 2021 The Author(s), under exclusive license to Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Bouret, S.G., Muscatelli, F. (2021). Ontogenesis of Hypothalamic Neurons in Mammals. In: Grinevich, V., Dobolyi, Á. (eds) Neuroanatomy of Neuroendocrine Systems. Masterclass in Neuroendocrinology, vol 12. Springer, Cham. https://doi.org/10.1007/978-3-030-86630-3_1

Download citation

Publish with us

Policies and ethics

Search

Navigation