Abstract
The paraventricular nucleus (PVN) of the hypothalamus harbors diverse neurosecretory cells with critical physiological roles for the homeostasis. Decades of research in rodents have provided a large amount of information on the anatomy, development, and function of this important hypothalamic nucleus. However, since the hypothalamus lies deep within the brain in mammals and is difficult to access, many questions regarding development and plasticity of this nucleus still remain. In particular, how different environmental conditions, including stress exposure, shape the development of this important nucleus has been difficult to address in animals that develop in utero. To address these open questions, the transparent larval zebrafish with its rapid external development and excellent genetic toolbox offers exciting opportunities. In this review, we summarize recent information on the anatomy and development of the neurosecretory preoptic area (NPO), which represents a similar structure to the mammalian PVN in zebrafish. We will then review recent studies on the development of different cell types in the neurosecretory hypothalamus both in mouse and in fish. Lastly, we discuss stress-induced plasticity of the PVN mainly discussing the data obtained in rodents, but pointing out tools and approaches available in zebrafish for future studies. This review serves as a primer for the currently available information relevant for studying the development and plasticity of this important brain region using zebrafish.
Abbreviations
- ac :
-
anterior commissure
- ACTH:
-
adrenocorticotropic hormone
- AgRP :
-
agouti-related protein
- AMPA :
-
α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid–glutamate receptor agonist
- aPV:
-
anterior periventricular nucleus
- ARC:
-
arcuate nucleus
- ARNT2:
-
aryl hydrocarbon receptor nuclear translocator-2
- Arx :
-
aristaless-related homeodomain transcription factor
- AVP :
-
arginine vasopressin
- bHLH:
-
basic helix loop helix
- CCK :
-
cholecystokinin
- CRH :
-
corticotropin-releasing hormone
- d:
-
dorsal
- Dlx:
-
distal less homeodomain transcription factor
- DMH:
-
dorsomedial hypothalamus
- ECR:
-
evolutionarily conserved region in the enhancer
- ENK:
-
enkephalin
- Fezf2:
-
forebrain embryonic zinc finger-like protein
- H:
-
hypothalamus
- Ha:
-
habenula
- HPA:
-
hypothalamo-pituitary-adrenal axis
- IR:
-
interrenal gland
- Isl-1:
-
islet-1 homeodomain transcription factor
- lENK:
-
leucine enkephalin
- LHA:
-
lateral hypothalamic area
- MA:
-
mammillary area
- mENK:
-
Methionine enkephalin
- MSH:
-
Melanocyte-stimulating hormone
- MTZ:
-
Metronidazole (drug for nitroreductase cell ablation system)
- NMDA:
-
N-methyl-d-aspartate–glutamate receptor agonist
- NPO:
-
neurosecretory preoptic area/preoptic nucleus
- NTS:
-
neurotensin
- oc:
-
optic chiasm
- Otp:
-
Orthopedia homeodomain transcription factor
- OXT:
-
oxytocin
- penka:
-
proenkephalin a
- penkb:
-
proenkephalin b
- Pit:
-
pituitary
- PM:
-
magnocellular preoptic nucleus
- PNC:
-
parvocellular neuroendocrine cells
- PO:
-
preoptic area
- poc:
-
postoptic commissure
- pomc:
-
proopiomelanocortin
- PPa:
-
anterior parvocellular preoptic nucleus
- PPp:
-
posterior parvocellular preoptic nucleus
- PT:
-
posterior tuberculum
- PTh:
-
prethalamus
- PVN:
-
paraventricular nucleus
- r:
-
rostral
- SIM1:
-
single minded-1
- SCN:
-
suprachiasmatic nucleus
- SON:
-
supraoptic nucleus
- SPV:
-
supraoptoparaventricular region
- SST/sst1.:
-
1 somatostatin
- STAR:
-
steroidogenic acute regulatory protein
- Tel:
-
telencephalon
- TeO:
-
optic tectum
- Th:
-
thalamus
- TRH:
-
thyrotropin-releasing hormone
- VIP:
-
vasoactive intestinal peptide
- VMH:
-
ventromedial hypothalamus
References
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. https://doi.org/10.1101/gad.13.21.2787
Akana SF, Dallman MF, Bradbury MJ, Scribner KA, Strack AM, Walker CD (1992a) Feedback and facilitation in the adrenocortical system: unmasking facilitation by partial inhibition of the glucocorticoid response to prior stress. Endocrinology 131:57–68. https://doi.org/10.1210/endo.131.1.1319329
Akana SF, Scribner KA, Bradbury MJ, Strack AM, Dominique Walker C, Dallman MF (1992b) Feedback sensitivity of the rat hypothalamo-pituitary-adrenal axis and its capacity to adjust to exogenous corticosterone. Endocrinology 131:585–594. https://doi.org/10.1210/endo.131.2.1322275
Albadri S, Del Bene F, Revenu C (2017) Genome editing using CRISPR/Cas9-based knock-in approaches in zebrafish. Methods. https://doi.org/10.1016/j.ymeth.2017.03.005
Albeck DS, McKittrick CR, Blanchard DC, Blanchard RJ, Nikulina J, McEwen BS, Sakai RR (1997) Chronic social stress alters levels of corticotropin-releasing factor and arginine vasopressin mRNA in rat brain. J Neurosci 17:4895–4903
Allalou A, Wu Y, Ghannad-Rezaie M, Eimon PM, Yanik MF (2017) Automated deep-phenotyping of the vertebrate brain. eLife 6. https://doi.org/10.7554/eLife.23379
Alsop D, Vijayan M (2009) The zebrafish stress axis: molecular fallout from the teleost-specific genome duplication event. Gen Comp Endocrinol 161:62–66. https://doi.org/10.1016/j.ygcen.2008.09.011
Alvarez-Bolado G (2018) Development of neuroendocrine neurons in the mammalian hypothalamus. Cell Tissue Res 1–17. https://doi.org/10.1007/s00441-018-2859-1
Amer S, Brown JA (1995) Glomerular actions of arginine vasotocin in the in situ perfused trout kidney. Am J Phys 269:R775–R780
Amir-Zilberstein L, Blechman J, Sztainberg Y, Norton WHJ, Reuveny A, Borodovsky N, Tahor M, Bonkowsky JL, Bally-Cuif L, Chen A, Levkowitz G (2012) Homeodomain protein Otp and activity-dependent splicing modulate neuronal adaptation to stress. Neuron 73:279–291. https://doi.org/10.1016/j.neuron.2011.11.019
Arima H, House SB, Gainer H, Aguilera G (2001) Direct stimulation of arginine vasopressin gene transcription by cAMP in parvocellular neurons of the paraventricular nucleus in organotypic cultures. Endocrinology 142:5027–5030. https://doi.org/10.1210/en.142.11.5027
Armario A, Martí O, Vallès A, Dal-Zotto S, Ons S (2004) Long-term effects of a single exposure to immobilization on the hypothalamic-pituitary-adrenal axis: neurobiologic mechanisms. Ann N Y Acad Sci 1018:162–172
Armario A, Escorihuela RM, Nadal R (2008) Long-term neuroendocrine and behavioural effects of a single exposure to stress in adult animals. Neurosci Biobehav Rev 32:1121–1135. https://doi.org/10.1016/j.neubiorev.2008.04.003
Arrenberg AB, Driever W (2013) Integrating anatomy and function for zebrafish circuit analysis. Front Neural Circuits 7:74. https://doi.org/10.3389/fncir.2013.00074
Bains JS, Cusulin JIW, Inoue W (2015) Stress-related synaptic plasticity in the hypothalamus. Nat Rev Neurosci 16:377–388. https://doi.org/10.1038/nrn3881
Bardet SM, Martinez-de-la-Torre M, Northcutt RG, Rubenstein JLR, Puelles L (2008) Conserved pattern of OTP-positive cells in the paraventricular nucleus and other hypothalamic sites of tetrapods. Brain Res Bull 75:231–235. https://doi.org/10.1016/j.brainresbull.2007.10.037
Béracochéa D (2005) Interaction between emotion and memory: importance of mammillary bodies damage in a mouse model of the alcoholic Korsakoff syndrome. Neural Plast 12:275–287. https://doi.org/10.1155/NP.2005.275
Bhargava HN (1969) Hypothalamo-hypophyseal system in the minnow, Phoxinus phoxinus L. with a note on the effects of hypophysectomy. J Comp Neurol 137:89–119. https://doi.org/10.1002/cne.901370106
Biran J, Tahor M, Wircer E, Levkowitz G (2015) Role of developmental factors in hypothalamic function. Front Neuroanat 9:1–11. https://doi.org/10.3389/fnana.2015.00047
Blechman J, Borodovsky N, Eisenberg M, Nabel-Rosen H, Grimm J, Levkowitz G (2007) Specification of hypothalamic neurons by dual regulation of the homeodomain protein Orthopedia. Development 134:4417–4426. https://doi.org/10.1242/dev.011262
Borodovsky N, Ponomaryov T, Frenkel S, Levkowitz G (2009) Neural protein olig2 acts upstream of the transcriptional regulator sim1 to specify diencephalic dopaminergic neurons. Dev Dyn 238:826–834. https://doi.org/10.1002/dvdy.21894
Braak H (1962) Uber die Gestalt des neurosekretorischen Zwischenhirn-Hypophysen-Systems von Spinax niger. Z Zellforsch Mikrosk Anat 58:265–276. https://doi.org/10.1007/BF00320188
Braford M, Northcutt R (1983) Organization of the diencephalon and pretectum of the ray-finned fishes. In: Davis RE, Northcutt RG (eds) Fish neurobiology. University of Michigan Press, Ann Arbor, pp 117–163
Burbridge S, Stewart I, Placzek M (2016) Development of the neuroendocrine hypothalamus. Compr Physiol 6:623–643. https://doi.org/10.1002/cphy.c150023
Burlet A, Tonon MC, Tankosic P, Coy D, Vaudry H (1983) Comparative immunocytochemical localization of corticotropin releasing factor (CRF-41) and neurohypophysial peptides in the brain of Brattleboro and Long-Evans rats. Neuroendocrinology 37:64–72. https://doi.org/10.1159/000123517
Caqueret A, Yang C, Duplan S, Boucher F, Michaud JL (2005) Looking for trouble: a search for developmental defects of the hypothalamus. Horm Res 64:222–230
Carraway R, Leeman SE (1973) The isolation of a new hypotensive peptide, neurotensin, from bovine hypothalami. J Biol Chem 248:6854–6861
Ceccatelli S, Eriksson M, Hokfelt T (1989) Distribution and coexistence of corticotropin-releasing factor-, neurotensin-, enkephalin-, cholecystokinin-, galanin- and vasoactive intestinal polypeptide/peptide histidine isoleucine-like peptides in the parvocellular part of the paraventricular nucleus. Neuroendocrinology 49:309–323. https://doi.org/10.1159/000125133
Chan DKO (1977) Comparative physiology of the vasomotor effects of neurohypophyseal peptides in the vertebrates. Am Zool 751–761
Chandrasekar G, Lauter G, Hauptmann G (2007) Distribution of corticotropin-releasing hormone in the developing zebrafish brain. J Comp Neurol 505:337–351. https://doi.org/10.1002/cne.21496
Charmandari E, Tsigos C, Chrousos G (2005) Endocrinology of the stress response. Annu Rev Physiol 67:259–284. https://doi.org/10.1146/annurev.physiol.67.040403.120816
Chen B, Schaevitz LR, McConnell SK (2005a) Fezl regulates the differentiation and axon targeting of layer 5 subcortical projection neurons in cerebral cortex. Proc Natl Acad Sci 102:17184–17189. https://doi.org/10.1073/pnas.0508732102
Chen J-G, Rasin M-R, Kwan KY, Sestan N (2005b) Zfp312 is required for subcortical axonal projections and dendritic morphology of deep-layer pyramidal neurons of the cerebral cortex. Proc Natl Acad Sci U S A 102:17792–17797. https://doi.org/10.1073/pnas.0509032102
Chen L, Zheng J, Yang N, Li H, Guo S (2011) Genomic selection identifies vertebrate transcription factor fezf2 binding sites and target genes. J Biol Chem 286:18641–18649. https://doi.org/10.1074/jbc.M111.236471
Chrousos GP (1998) Stressors, stress, and neuroendocrine integration of the adaptive response: the 1997 Hans Selye Memorial Lecture. Ann N Y Acad Sci 851:311–335. https://doi.org/10.1111/j.1749-6632.1998.tb09006.x
Cole RL, Sawchenko PE (2002) Neurotransmitter regulation of cellular activation and neuropeptide gene expression in the paraventricular nucleus of the hypothalamus. J Neurosci 22:959–969
Cullinan WE, Wolfe TJ (2000) Chronic stress regulates levels of mRNA transcripts encoding β subunits of the GABAA receptor in the rat stress axis. Brain Res 887:118–124. https://doi.org/10.1016/S0006-8993(00)03000-6
Cusulin JIW, Füzesi T, Inoue W, Bains JS (2013) Glucocorticoid feedback uncovers retrograde opioid signaling at hypothalamic synapses. Nat Neurosci 16:596–604. https://doi.org/10.1038/nn.3374
Dabrowska J, Hazra R, Ahern TH, Guo JD, McDonald AJ, Mascagni F, Muller JF, Young LJ, Rainnie DG (2011) Neuroanatomical evidence for reciprocal regulation of the corticotrophin-releasing factor and oxytocin systems in the hypothalamus and the bed nucleus of the stria terminalis of the rat: implications for balancing stress and affect. Psychoneuroendocrinology 36:1312–1326. https://doi.org/10.1016/j.psyneuen.2011.03.003
Darlington DN, Miyamoto M, Keil LC, Dallman MF (1989) Paraventricular stimulation with glutamate elicits bradycardia and pituitary responses. Am J Physiol 256:R112–R119. https://doi.org/10.1152/ajpregu.1989.256.1.R112
De Marco RJ, Groneberg AH, Yeh C-M, Castillo Ramírez LA, Ryu S (2013) Optogenetic elevation of endogenous glucocorticoid level in larval zebrafish. Front Neural Circuits 7:82. https://doi.org/10.3389/fncir.2013.00082
De Marco RJ, Thiemann T, Groneberg AH, Herget U, Ryu S (2016) Optogenetically enhanced pituitary corticotroph cell activity post-stress onset causes rapid organizing effects on behaviour. Nat Commun 7:12620. https://doi.org/10.1038/ncomms12620
Del Giacco L, Sordino P, Pistocchi A, Andreakis N, Tarallo R, Di Benedetto B, Cotelli F (2006) Differential regulation of the zebrafish orthopedia1 gene during fate determination of diencephalic neurons. BMC Dev Biol. https://doi.org/10.1186/1471-213X-6-50
Denver RJ (2009) Structural and functional evolution of vertebrate neuroendocrine stress systems. Ann N Y Acad Sci 1163:1–16
Diaz ML, Becerra M, Manso MJ, Anadon R (2002) Distribution of thyrotropin-releasing hormone (TRH) immunoreactivity in the brain of the zebrafish (Danio rerio). J Comp Neurol 450:45–60. https://doi.org/10.1002/cne.10300
Domínguez L, Morona R, González A, Moreno N (2013) Characterization of the hypothalamus of Xenopus laevis during development. I. The alar regions. J Comp Neurol 521:725–759. https://doi.org/10.1002/cne.23222
Domínguez L, González A, Moreno N (2015) Patterns of hypothalamic regionalization in amphibians and reptiles: common traits revealed by a genoarchitectonic approach. Front Neuroanat 9:3. https://doi.org/10.3389/fnana.2015.00003
Duplan SM, Boucher F, Alexandrov L, Michaud JL (2009) Impact of Sim1 gene dosage on the development of the paraventricular and supraoptic nuclei of the hypothalamus. Eur J Neurosci 30:2239–2249. https://doi.org/10.1111/j.1460-9568.2009.07028.x
Eaton JL, Glasgow E (2006) The zebrafish bHLH PAS transcriptional regulator, single-minded 1 (sim1), is required for isotocin cell development. Dev Dyn 235:2071–2082. https://doi.org/10.1002/dvdy.20848
Eaton JL, Glasgow E (2007) Zebrafish orthopedia (otp) is required for isotocin cell development. Dev Genes Evol 217:149–158. https://doi.org/10.1007/s00427-006-0123-2
Eaton JL, Holmqvist B, Glasgow E (2008) Ontogeny of vasotocin-expressing cells in zebrafish: selective requirement for the transcriptional regulators orthopedia and single-minded 1 in the preoptic area. Dev Dyn 237:995–1005. https://doi.org/10.1002/dvdy.21503
Ferguson AV, Latchford KJ, Samson WK (2008) The paraventricular nucleus of the hypothalamus—a potential target for integrative treatment of autonomic dysfunction. Expert Opin Ther Targets 12:717–727. https://doi.org/10.1517/14728222.12.6.717
Fernandes AM, Beddows E, Filippi A, Driever W (2013) Orthopedia transcription factor otpa and otpb paralogous genes function during dopaminergic and neuroendocrine cell specification in larval zebrafish. PLoS One. https://doi.org/10.1371/journal.pone.0075002
Forlano PM, Cone RD (2007) Conserved neurochemical pathways involved in hypothalamic control of energy homeostasis. J Comp Neurol 505:235–248. https://doi.org/10.1002/cne.21447
García-Moreno F, Pedraza M, Di Giovannantonio LG, Di Salvio M, López-Mascaraque L, Simeone A, De Carlos JA (2010) A neuronal migratory pathway crossing from diencephalon to telencephalon populates amygdala nuclei. Nat Neurosci 13:680–689. https://doi.org/10.1038/nn.2556
Gillies G, Lowry P (1979) Corticotrophin releasing factor may be modulated vasopressin. Nature 278:463–464
Givalois L, Arancibia S, Tapia-Arancibia L (2000) Concomitant changes in CRH mRNA levels in rat hippocampus and hypothalamus following immobilization stress. Mol Brain Res 75:166–171
Goshu E, Jin H, Lovejoy J, Marion J-F, Michaud JL, Fan C-M (2004) Sim2 contributes to neuroendocrine hormone gene expression in the anterior hypothalamus. Mol Endocrinol 18:1251–1262. https://doi.org/10.1210/me.2003-0372
Grunwald DJ, Eisen JS (2002) Headwaters of the zebrafish—emergence of a new model vertebrate. Nat Rev Genet 3:717–724. https://doi.org/10.1038/nrg892
Guo S, Wilson SW, Cooke S, Chitnis AB, Driever W, Rosenthal A (1999) Mutations in the zebrafish unmask shared regulatory pathways controlling the development of catecholaminergic neurons. Dev Biol 208:473–487. https://doi.org/10.1006/dbio.1999.9204
Gutierrez-Triana JA, Herget U, Lichtner P, Castillo-Ramírez LA, Ryu S (2014) A vertebrate-conserved cis-regulatory module for targeted expression in the main hypothalamic regulatory region for the stress response. BMC Dev Biol 14:41. https://doi.org/10.1186/s12861-014-0041-x
Gutierrez-Triana JA, Herget U, Castillo-Ramirez LA, Lutz M, Yeh C-M, De Marco RJ, Ryu S (2015) Manipulation of Interrenal cell function in developing zebrafish using genetically targeted ablation and an optogenetic tool. Endocrinology 156:3394–3401. https://doi.org/10.1210/EN.2015-1021
Harbuz MS, Lightman SL (1989) Responses of hypothalamic and pituitary mRNA to physical and psychological stress in the rat. J Endocrinol 122:705–711
Hashimoto H, Yabe T, Hirata T, Shimizu T, Bae Y, Yamanaka Y, Hirano T, Hibi M (2000) Expression of the zinc finger gene fez-like in zebrafish forebrain. Mech Dev 97:191–195. https://doi.org/10.1016/S0925-4773(00)00418-4
Herget U (2015) The molecular neuroanatomy, chemoarchitecture and projectome of the hypothalamic center regulating the stress response in larval zebrafish. Dissertation, Heidelberg University
Herget U, Ryu S (2015) Coexpression analysis of nine neuropeptides in the neurosecretory preoptic area of larval zebrafish. Front Neuroanat 9:2. https://doi.org/10.3389/fnana.2015.00002
Herget U, Wolf A, Wullimann MF, Ryu S (2014) Molecular neuroanatomy and chemoarchitecture of the neurosecretory preoptic-hypothalamic area in zebrafish larvae. J Comp Neurol 522:1542–1564. https://doi.org/10.1002/cne.23480
Herget U, Gutierrez-Triana JA, Salazar Thula O, Knerr B, Ryu S (2017) Single-cell reconstruction of oxytocinergic neurons reveals separate hypophysiotropic and encephalotropic subtypes in larval zebrafish. eNeuro 4. https://doi.org/10.1523/ENEURO.0278-16.2016
Herman JP, Tasker JG (2016) Paraventricular hypothalamic mechanisms of chronic stress adaptation. Front Endocrinol (Lausanne) 7:1–10. https://doi.org/10.3389/fendo.2016.00137
Herman JP, Schafer MK, Thompson RC, Watson SJ (1992) Rapid regulation of corticotropin-releasing hormone gene transcription in vivo. Mol Endocrinol 6:1061–1069
Herman JP, Adams D, Prewitt C (1995) Regulatory changes in neuroendocrine stress-integrative circuitry produced by a variable stress paradigm. Neuroendocrinology 61:180–190
Herman JP, Cullinan WE, Ziegler DR, Tasker JG (2002) Role of the paraventricular nucleus microenvironment in stress integration. Eur J Neurosci 16(3):381–385
Herman JP, McKlveen JM, Ghosal S, Kopp B, Wulsin A, Makinson R, Scheimann J, Myers B (2016) Regulation of the hypothalamic-pituitary-adrenocortical stress response. Compr Physiol 6:603–621. https://doi.org/10.1002/cphy.c150015
Hirata T, Suda Y, Nakao K, Narimatsu M, Hirano T, Hibi M (2004) Zinc finger gene fez-like functions in the formation of subplate neurons and thalamocortical axons. Dev Dyn 230:546–556. https://doi.org/10.1002/dvdy.20068
Hirata T, Nakazawa M, Muraoka O, Nakayama R, Suda Y, Hibi M (2006) Zinc-finger genes Fez and Fez-like function in the establishment of diencephalon subdivisions. Development 133:3993–4004. https://doi.org/10.1242/dev.02585
Hökfelt T, Fahrenkrug J, Tatemoto K, Mutt V, Werner S, Hulting AL, Terenius L, Chang KJ (1983) The PHI (PHI-27)/corticotropin-releasing factor/enkephalin immunoreactive hypothalamic neuron: possible morphological basis for integrated control of prolactin, corticotropin, and growth hormone secretion. Proc Natl Acad Sci U S A 80:895–898
Holtzman NG, Iovine MK, Liang JO, Morris J (2016) Learning to fish with genetics: a primer on the vertebrate model Danio rerio. Genetics 203:1069–1089. https://doi.org/10.1534/genetics.116.190843
Imaki T, Nahan JL, Rivier C, Sawchenko PE, Vale W (1991) Differential regulation of corticotropin-releasing factor mRNA in rat brain regions by glucocorticoids and stress. J Neurosci 11:585–599
Inoue W, Baimoukhametova DV, Füzesi T, Cusulin JIW, Koblinger K, Whelan PJ, Pittman QJ, Bains JS (2013) Noradrenaline is a stress-associated metaplastic signal at GABA synapses. Nat Neurosci 16:605–612. https://doi.org/10.1038/nn.3373
Jeong J-Y, Einhorn Z, Mercurio S, Lee S, Lau B, Mione M, Wilson SW, Guo S (2006) Neurogenin1 is a determinant of zebrafish basal forebrain dopaminergic neurons and is regulated by the conserved zinc finger protein Tof/Fezl. Proc Natl Acad Sci 103:5143–5148. https://doi.org/10.1073/pnas.0600337103
Jeong J-Y, Einhorn Z, Mathur P, Chen L, Lee S, Kawakami K, Guo S (2007) Patterning the zebrafish diencephalon by the conserved zinc-finger protein Fezl. Development 134:127–136. https://doi.org/10.1242/dev.02705
Joëls M, Baram TZ (2009) The neuro-symphony of stress. Nat Rev Neurosci 10:459–466. https://doi.org/10.1038/nrn2632
Juster R, Mcewen BS, Lupien SJ (2010) Neuroscience and biobehavioral reviews allostatic load biomarkers of chronic stress and impact on health and cognition. Neurosci Biobehav Rev 35:2–16. https://doi.org/10.1016/j.neubiorev.2009.10.002
Keeney A, Jessop DS, Harbuz MS, Marsden CA, Hogg S, Blackburn-Munro RE (2006) Differential effects of acute and chronic social defeat stress on hypothalamic-pituitary-adrenal axis function and hippocampal serotonin release in mice. J Neuroendocrinol 18:330–338
Keith B, Adelman DM, Simon MC (2001) Targeted mutation of the murine arylhydrocarbon receptor nuclear translocator 2 (Arnt2) gene reveals partial redundancy with Arnt. Proc Natl Acad Sci 98:6692–6697. https://doi.org/10.1073/pnas.121494298
Khan AM, Watts AG (2004) Intravenous 2-deoxy-D-glucose injection rapidly elevates levels of the phosphorylated forms of p44/42 mitogen-activated protein kinases (extracellularly regulated kinases 1/2) in rat hypothalamic parvicellular paraventricular neurons. Endocrinology 145:351–359
Kiss JZ (1988) Dynamism of chemoarchitecture in the hypothalamic paraventricular nucleus. Brain Res Bull 20:699–708
Kobayashi D, Kobayashi M, Matsumoto K, Ogura T, Nakafuku M, Shimamura K (2002) Early subdivisions in the neural plate define distinct competence for inductive signals. Development 129:83–93
Kovacs KJ, Sawchenko PE (1996) Sequence of stress-induced alterations in indices of synaptic and transcriptional activation in parvocellular neurosecretory neurons. J Neurosci 16:262–273
Kurrasch DM, Nevin LM, Wong JS, Baier H, Ingraham HA (2009) Neuroendocrine transcriptional programs adapt dynamically to the supply and demand for neuropeptides as revealed in NSF mutant zebrafish. Neural Dev 4:22. https://doi.org/10.1186/1749-8104-4-22
Kuzmiski JB, Marty V, Baimoukhametova DV, Bains JS (2010) Stress-induced priming of glutamate synapses unmasks associative short-term plasticity. Nat Neurosci 13:1257–1264. https://doi.org/10.1038/nn.2629
Landgraf R, Neumann ID (2004) Vasopressin and oxytocin release within the brain: a dynamic concept of multiple and variable modes of neuropeptide communication. Front Neuroendocrinol 25:150–176
Lee S, Rivier C, Torres G (1994) Induction of c-fos and CRF mRNA by MK-801 in the parvocellular paraventricular nucleus of the rat hypothalamus. Mol Brain Res 24:192–198. https://doi.org/10.1016/0169-328X(94)90132-5
Levin MC, Sawchenko PE (1993) Neuropeptide co-expression in the magnocellular neurosecretory system of the female rat: evidence for differential modulation by estrogen. Neuroscience 54:1001–1018. https://doi.org/10.1016/0306-4522(93)90591-3
Levkowitz G, Zeller J, Sirotkin HI, French D, Schilbach S, Hashimoto H, Hibi M, Talbot WS, Rosenthal A (2003) Zinc finger protein too few controls the development of monoaminergic neurons. Nat Neurosci 6:28–33. https://doi.org/10.1038/nn979
Li M, Zhao L, Page-McCaw PS, Chen W (2016) Zebrafish genome engineering using the CRISPR–Cas9 system. Trends Genet 32:815–827. https://doi.org/10.1016/j.tig.2016.10.005
Lichtman JW, Livet J, Sanes JR (2008) A technicolour approach to the connectome. Nat Rev Neurosci 9:417–422. https://doi.org/10.1038/nrn2391
Lin X, State MW, Vaccarino FM, Greally J, Hass M, Leckman JF (1999) Identification, chromosomal assignment, and expression analysis of the human homeodomain-containing gene Orthopedia (OTP). Genomics 60:96–104. https://doi.org/10.1006/geno.1999.5882
Liu N-A, Huang H, Yang Z, Herzog W, Hammerschmidt M, Lin S, Melmed S (2003) Pituitary corticotroph ontogeny and regulation in transgenic zebrafish. Mol Endocrinol 17:959–966. https://doi.org/10.1210/me.2002-0392
Livet J, Weissman TA, Kang H, Draft RW, Lu J, Bennis RA, Sanes JR, Lichtman JW (2007) Transgenic strategies for combinatorial expression of fluorescent proteins in the nervous system. Nature 450:56–62. https://doi.org/10.1038/nature06293
Löhr H, Hammerschmidt M (2011) Zebrafish in endocrine systems: recent advances and implications for human disease. Annu Rev Physiol 73:183–211. https://doi.org/10.1146/annurev-physiol-012110-142320
Löhr H, Ryu S, Driever W (2009) Zebrafish diencephalic A11-related dopaminergic neurons share a conserved transcriptional network with neuroendocrine cell lineages. Development 136:1007–1017. https://doi.org/10.1242/dev.033878
Machluf Y, Gutnick A, Levkowitz G (2011) Development of the zebrafish hypothalamus. Ann N Y Acad Sci 1220:93–105. https://doi.org/10.1111/j.1749-6632.2010.05945.x
Makino S, Schulkin J, Smith MA, Pacak K, Palkovits M, Gold PW (1995) Regulation of corticotropin-releasing hormone receptor messenger ribonucleic acid in the rat brain and pituitary by glucocorticoids and stress. Endocrinology 136:4517–4525
Markakis EA (2002) Development of the neuroendocrine hypothalamus. Front Neuroendocrinol 23:257–291. https://doi.org/10.1016/S0091-3022(02)00003-1
Martin R, Voigt KH (1981) Enkephalins co-exist with oxytocin and vasopressin in nerve terminals of rat neurohypophysis. Nature 289:502–504. https://doi.org/10.1038/289502a0
Matsuo-Takasaki M, Lim JH, Beanan MJ, Sato SM, Sargent TD (2000) Cloning and expression of a novel zinc finger gene, Fez, transcribed in the forebrain of Xenopus and mouse embryos. Mech Dev 93:201–204. https://doi.org/10.1016/S0925-4773(00)00264-1
McEwen BS (2000) Allostasis and allostatic load: implications for neuropsychopharmacology. Neuropsychopharmacology 22:108–124. https://doi.org/10.1016/S0893-133X(99)00129-3
McEwen BS (2007) Physiology and neurobiology of stress and adaptation: central role of the brain. Physiol Rev 87:873–904. https://doi.org/10.1152/physrev.00041.2006
McEwen BS, Wingfield JC (2003) The concept of allostasis in biology and biomedicine. Horm Behav 43:2–15. https://doi.org/10.1016/S0018-506X(02)00024-7
Mezey E, Reisine TD, Skirboll L, Beinfeld M, Kiss JZ (1985) Cholecystokinin in the medial parvocellular subdivision of the paraventricular nucleus. Co-existence with corticotropin-releasing hormone. Ann N Y Acad Sci 448:152–156
Michaud JL, Rosenquist T, May NR, Fan CM (1998) Development of neuroendocrine lineages requires the bHLH-PAS transcription factor SIM1. Genes Dev 12:3264–3275. https://doi.org/10.1101/gad.12.20.3264
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
Miklos IH, Kovacs KJ (2002) GABAergic innervation of corticotropin-releasing hormone (CRH)-secreting parvocellular neurons and its plasticity as demonstrated by quantitative immunoelectron microscopy. Neuroscience 113:581–592
Miklos IH, Kovacs KJ (2012) Reorganization of synaptic inputs to the hypothalamic paraventricular nucleus during chronic psychogenic stress in rats. Biol Psychiatry 71:301–308. https://doi.org/10.1016/j.biopsych.2011.10.027
Miura H, Yanazawa M, Kato K, Kitamura K (1997) Expression of a novel aristaless related homeobox gene “Arx” in the vertebrate telencephalon, diencephalon and floor plate. Mech Dev 65:99–109. https://doi.org/10.1016/S0925-4773(97)00062-2
Molyneaux BJ, Arlotta P, Hirata T, Hibi M, Macklis JD (2005) Fezl is required for the birth and specification of corticospinal motor neurons. Neuron 47:817–831. https://doi.org/10.1016/j.neuron.2005.08.030
Morales-Delgado N, Merchan P, Bardet SM, Ferrán JL, Puelles L, Díaz C (2011) Topography of somatostatin gene expression relative to molecular progenitor domains during ontogeny of the mouse hypothalamus. Front Neuroanat 5:10. https://doi.org/10.3389/fnana.2011.00010
Moreno N, González A (2011) The non-evaginated secondary prosencephalon of vertebrates. Front Neuroanat. https://doi.org/10.3389/fnana.2011.00012
Moreno N, Domínguez L, Morona R, González A (2012) Subdivisions of the turtle Pseudemys scripta hypothalamus based on the expression of regulatory genes and neuronal markers. J Comp Neurol 520:453–478. https://doi.org/10.1002/cne.22762
Nakai S, Kawano H, Yudate T, Nishi M, Kuno J, Nagata A, Jishage KI, Hamada H, Fujii H, Kawamura K, Shiba K, Noda T (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. https://doi.org/10.1101/gad.9.24.3109
Nieuwenhuys R, Voogd J, van Huijzen C. (2008) The human central nervous system. Springer
Onaka T, Takayanagi Y, Yoshida M (2012) Roles of oxytocin neurones in the control of stress, energy metabolism, and social behaviour. J Neuroendocrinol 24:587–598
Orger MB, de Polavieja GG (2017) Zebrafish behavior: opportunities and challenges. Annu Rev Neurosci 40. https://doi.org/10.1146/annurev-neuro-071714-033857
Osório J, Mueller T, Rétaux S, Vernier P, Wullimann MF (2010) Phylotypic expression of the bHLH genes Neurogenin2, NeuroD, and Mash1 in the mouse embryonic forebrain. J Comp Neurol 518:851–871. https://doi.org/10.1002/cne.22247
Park JB, Skalska S, Son S, Stern JE (2007) Dual GABAA receptor-mediated inhibition in rat presympathetic paraventricular nucleus neurons. J Physiol 582:539–551. https://doi.org/10.1113/jphysiol.2007.133223
Pechnick RN, Bresee CJ, Poland RE (2006) The role of antagonism of NMDA receptor-mediated neurotransmission and inhibition of the dopamine reuptake in the neuroendocrine effects of phencyclidine. Life Sci 78:2006–2011. https://doi.org/10.1016/j.lfs.2005.09.018
Piekut DT, Joseph SA (1986) Co-existence of CRF and vasopressin immunoreactivity in parvocellular paraventricular neurons of rat hypothalamus. Peptides 7:891–898. https://doi.org/10.1016/0196-9781(86)90111-7
Pistocchi A, Gaudenzi G, Carra S, Bresciani E, Del Giacco L, Cotelli F (2008) Crucial role of zebrafish prox1 in hypothalamic catecholaminergic neurons development. BMC Dev Biol. https://doi.org/10.1186/1471-213X-8-27
Portugues R, Severi KE, Wyart C, Ahrens MB (2013) Optogenetics in a transparent animal: circuit function in the larval zebrafish. Curr Opin Neurobiol 23:119–126. https://doi.org/10.1016/j.conb.2012.11.001
Pretel S, Piekut D (1990) Coexistence of corticotropin-releasing factor and enkephalin in the paraventricular nucleus of the rat. J Comp Neurol 294:192–201. https://doi.org/10.1002/cne.902940204
Puelles L, Medina L (2002) Field homology as a way to reconcile genetic and developmental variability with adult homology. Brain Res Bull 57(3–4):243–255
Puelles L, Rubenstein JLR (2003) Forebrain gene expression domains and the evolving prosomeric model. Trends Neurosci 26:469–476. https://doi.org/10.1016/S0166-2236(03)00234-0
Puelles L, Martinez-de-la-Torre M, Bardet S, Rubenstein J (2012) Hypothalamus. In: Watson C, Paxinos G, Puelles L (eds) The mouse nervous system. Academic Press, New York, pp 221–312
Raadsheer FC, Sluiter AA, Ravid R, Tilders FJ, Swaab DF (1993) Localization of corticotropin-releasing hormone (CRH) neurons in the paraventricular nucleus of the human hypothalamus; age-dependent colocalization with vasopressin. Brain Res 615:50–62
Rho JH, Swanson LW (1989) A morphometric analysis of functionally defined subpopulations of neurons in the paraventricular nucleus of the rat with observations on the effects of colchicine. J Neurosci 9:1375–1388
Rink E, Guo S (2004) The too few mutant selectively affects subgroups of monoaminergic neurons in the zebrafish forebrain. Neuroscience 127:147–154. https://doi.org/10.1016/j.neuroscience.2004.05.004
Rivier C, Vale W (1983) Interaction of corticotropin-releasing factor and arginine vasopressin on adrenocorticotropin secretion in vivo. Endocrinology 113:939–942. https://doi.org/10.1210/endo-113-3-939
Roland BL, Sawchenko PE (1993) Local origins of some GABAergic projections to the paraventricular and supraoptic nuclei of the hypothalamus in the rat. J Comp Neurol 332:123–143. https://doi.org/10.1002/cne.903320109
Rossier J, Liston D, Patey G, Chaminade M, Foutz AS, Cupo A, Giraud P, Roisin MP, Henry JP, Verbanck P (1983) The enkephalinergic neuron: implications of a polyenkephalin precursor. Cold Spring Harb Symp Quant Biol 48(Pt 1):393–404
Roth KA, Weber E, Barchas JD, Chang D, Chang JK (1983) Immunoreactive dynorphin-(1-8) and corticotropin- releasing factor in subpopulation of hypothalamic neurons. Science 219:189–191
Rupp B, Northcutt R (1998) The diencephalon and pretectum of the white sturgeon (Acipenser transmontanus): a cytoarchitectonic study. Brain Behav Evol 51:239–262. https://doi.org/10.1159/000006541
Russek-Blum N, Gutnick A, Nabel-Rosen H, Blechman J, Staudt N, Dorsky RI, Houart C, Levkowitz G (2008) Dopaminergic neuronal cluster size is determined during early forebrain patterning. Development 135:3401–3413. https://doi.org/10.1242/dev.024232
Ryu S, Mahler J, Acampora D, Holzschuh J, Erhardt S, Omodei D, Simeone A, Driever W (2007) Orthopedia homeodomain protein is essential for diencephalic dopaminergic neuron development. Curr Biol 17:873–880. https://doi.org/10.1016/j.cub.2007.04.003
Saper CB, Lowell BB (2014) The hypothalamus. Curr Biol 24:R1111–R1116. https://doi.org/10.1016/j.cub.2014.10.023
Sathyanesan AG (1969) An in situ study of the preoptico-neurohypophysial complex of the freshwater teleost Clarias batrachus (L.). Z Zellforsch Mikrosk Anat 98:202–216
Sawchenko PE (1987) Evidence for differential regulation of corticotropin-releasing factor and vasopressin immunoreactivities in parvocellular neurosecretory and autonomic-related projections of the paraventricular nucleus. Brain Res 437:253–263. https://doi.org/10.1016/0006-8993(87)91641-6
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
Sawchenko PE, Swanson LW, Vale WW (1984) Corticotropin-releasing factor: co-expression within distinct subsets of oxytocin-, vasopressin-, and neurotensin-immunoreactive neurons in the hypothalamus of the male rat. J Neurosci 4:1118–1129
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. https://doi.org/10.1101/gad.9.24.3122
Shimizu T, Hibi M (2009) Formation and patterning of the forebrain and olfactory system by zinc-finger genes Fezf1 and Fezf2. Develop Growth Differ 51:221–231
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. https://doi.org/10.1038/nn.2545
Simeone A, D’Apice MR, Nigro V, Casanova J, Graziani F, Acampora D, Avantaggiato V (1994) Orthopedia, a novel homeobox-containing gene expressed in the developing CNS of both mouse and drosophila. Neuron 13:83–101. https://doi.org/10.1016/0896-6273(94)90461-8
Simmons DM, Swanson LW (2008) High-resolution paraventricular nucleus serial section model constructed within a traditional rat brain atlas. Neurosci Lett 438:85–89. https://doi.org/10.1016/j.neulet.2008.04.057
Simmons DM, Swanson LW (2009) Comparison of the spatial distribution of seven types of neuroendocrine neurons in the rat paraventricular nucleus: toward a global 3D model. J Comp Neurol 516:423–441. https://doi.org/10.1002/cne.22126
Strand FL (1999) Neuropeptides: regulators of physiological processes. MIT Press
Swanson LW (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. 570:555–570
Swanson LW (1991) Biochemical switching in hypothalamic circuits mediating responses to stress. Prog Brain Res 87:181–200
Swanson LW, Sawchenko PE (1980) Paraventricular nucleus: a site for the integration of neuroendocrine and autonomic mechanisms. Neuroendocrinology 31:410–417. https://doi.org/10.1159/000123111
Swanson LW, Sawchenko PE (1983) Hypothalamic integration: organization of the paraventricular and supraoptic nuclei. Annu Rev Neurosci 6:269–324. https://doi.org/10.1146/annurev.ne.06.030183.001413
Swanson LW, Simmons DM (1989) Differential steroid hormone and neural influences on peptide mRNA levels in CRH cells of the paraventricular nucleus: a hybridization histochemical study in the rat. J Comp Neurol 285:413–435. https://doi.org/10.1002/cne.902850402
Swanson LW, Sawchenko PE, Lind RW (1986) Regulation of multiple peptides in CRF parvocellular neurosecretory neurons: implications for the stress response. Prog Brain Res 68:169–190
Szarek E, Cheah P-S, Schwartz J, Thomas P (2010) Molecular genetics of the developing neuroendocrine hypothalamus. Mol Cell Endocrinol 323:115–123. https://doi.org/10.1016/j.mce.2010.04.002
Tessmar-Raible K, Raible F, Christodoulou F, Guy K, Rembold M, Hausen H, Arendt D (2007) Conserved sensory-neurosecretory cell types in annelid and fish forebrain: insights into hypothalamus evolution. Cell 129:1389–1400. https://doi.org/10.1016/j.cell.2007.04.041
Ulrich-Lai YM, Herman JP (2009) Neural regulation of endocrine and autonomic stress responses. Nat Rev Neurosci 10:397–409
Umesono Y, Watanabe K, Agata K (1999) Distinct structural domains in the planarian brain defined by the expression of evolutionarily conserved homeobox genes. Dev Genes Evol 209:31–39. https://doi.org/10.1007/s004270050224
Unger JL, Glasgow E (2003) Expression of isotocin-neurophysin mRNA in developing zebrafish. Gene Expr Patterns 3:105–108. https://doi.org/10.1016/S1567-133X(02)00064-9
Vale W, Vaughan J, Smith M, Yamamoto G, Rivier J, Rivier C (1983) Effects of synthetic ovine corticotropin-releasing factor, glucocorticoids, catecholamines, neurohypophysial peptides, and other substances on cultured corticotropic cells. Endocrinology 113:1121–1131. https://doi.org/10.1210/endo-113-3-1121
Vanderhaeghen JJ, Lotstra F, Vandesande F, Dierickx K (1981) Coexistence of cholecystokinin and oxytocin-neurophysin in some magnocellular hypothalamo-hypophyseal neurons. Cell Tissue Res 221:227–231. https://doi.org/10.1007/BF00216585
Vann SD, Nelson AJD (2015) The mammillary bodies and memory. Prog Brain Res 219:163–185
Verkuyl JM, Hemby SE, Jöels M (2004) Chronic stress attenuates GABAergic inhibition and alters gene expression of parvocellular neurons in rat hypothalamus. Eur J Neurosci 20:1665–1673. https://doi.org/10.1111/j.1460-9568.2004.03568.x
Vom Berg-Maurer CM, Trivedi CA, Bollmann JH, De Marco RJ, Ryu S (2016) The severity of acute stress is represented by increased synchronous activity and recruitment of hypothalamic CRH neurons. J Neurosci 36:3350–3362. https://doi.org/10.1523/JNEUROSCI.3390-15.2016
Wamsteeker JI, Kuzmiski JB, Bains JS (2010) Repeated stress impairs endocannabinoid signaling in the paraventricular nucleus of the hypothalamus. J Neurosci 30:11188–11196. https://doi.org/10.1523/JNEUROSCI.1046-10.2010
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. https://doi.org/10.1006/dbio.2000.9902
Whitnall MH, Gainer H (1988) Major pro-vasopressin-expressing and pro-vasopressin-deficient subpopulations of corticotropin-releasing hormone neurons in normal rats: differential distributions within the paraventricular nucleus. Neuroendocrinology 47:176–180. https://doi.org/10.1159/000124910
Wircer E, Blechman J, Borodovsky N, Tsoory M, Nunes AR, Oliveira RF, Levkowitz G (2017) Homeodomain protein otp affects developmental neuropeptide switching in oxytocin neurons associated with a long-term effect on social behavior. elife. https://doi.org/10.7554/eLife.22170
Wolf A, Ryu S (2013) Specification of posterior hypothalamic neurons requires coordinated activities of Fezf2, Otp, Sim1a and Foxb1.2. Development 140:1762–1773. https://doi.org/10.1242/dev.085357
Woo K, Fraser SE (1995) Order and coherence in the fate map of the zebrafish nervous system. Development 121:2595–2609
Wullimann MF, Rupp B, Reichert H (1996) Neuroanatomy of the zebrafish brain: a topological atlas
Xi D, Gandhi N, Lai M, Kublaoui BM (2012) Ablation of Sim1 neurons causes obesity through hyperphagia and reduced energy expenditure. PLoS One. https://doi.org/10.1371/journal.pone.0036453
Xie Y, Dorsky RI (2017) Development of the hypothalamus: conservation, modification and innovation. Development 144:1588–1599. https://doi.org/10.1242/dev.139055
Xie Y, Kaufmann D, Moulton MJ, Panahi S, Gaynes JA, Watters HN, Zhou D, Xue HH, Fung CM, Levine EM, Letsou A, Brennan KC, Dorsky RI (2017) Lef1-dependent hypothalamic neurogenesis inhibits anxiety. PLoS Biol. https://doi.org/10.1371/journal.pbio.2002257
Yang Z, Liu N, Lin S (2001) A zebrafish forebrain-specific zinc finger gene can induce ectopic dlx2 and dlx6 expression. Dev Biol 231:138–148. https://doi.org/10.1006/dbio.2000.0139
Ziegler DR, Cullinan WE, Herman JP (2005) Organization and regulation of paraventricular nucleus glutamate signaling systems: N-methyl-D-aspartate receptors. J Comp Neurol 484:43–56
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This study was funded by the Max Planck Society, the University Medical Center of the Johannes Gutenberg University Mainz, the German Federal Office for Education and Research (Bundesministerium für Bildung und Forschung) grant number 01GQ1404 to S.R., and German Research Foundation (Deutsche Forschungsgemeinschaft) SPP1926 Next Generation Optogenetics grant to S.R.
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Nagpal, J., Herget, U., Choi, M.K. et al. Anatomy, development, and plasticity of the neurosecretory hypothalamus in zebrafish. Cell Tissue Res 375, 5–22 (2019). https://doi.org/10.1007/s00441-018-2900-4
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DOI: https://doi.org/10.1007/s00441-018-2900-4