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01-12-2020 | Original Article

Concurrent changes in photoperiod-induced seasonal phenotypes and hypothalamic CART peptide-containing systems in night-migratory redheaded buntings

Authors: Omprakash Singh, Neha Agarwal, Anupama Yadav, Sumela Basu, Shalie Malik, Sangeeta Rani, Vinod Kumar, Praful S. Singru

Published in: Brain Structure and Function | Issue 9/2020

Abstract

This study tested the hypothesis whether hypothalamic cocaine-and amphetamine-regulated transcript (CART)-containing systems were involved in photoperiod-induced responses associated with spring migration (hyperphagia and weight gain) and reproduction (gonadal maturation) in migratory songbirds. We specifically chose CART to examine neural mechanism(s) underlying photoperiod-induced responses, since it is a potent anorectic neuropeptide and involved in the regulation of changes in the body mass and reproduction in mammals. We first studied the distribution of CART-immunoreactivity in the hypothalamus of migratory redheaded buntings (Emberiza bruniceps). CART-immunoreactive neurons were found extensively distributed in the preoptic, lateral hypothalamic (LHN), anterior hypothalamic (AN), suprachiasmatic (SCN), paraventricular (PVN), dorsomedialis hypothalami (DMN), inferior hypothalamic (IH), and infundibular (IN) nuclei. Then, we correlated hypothalamic CART-immunoreactivity in buntings with photostimulated seasonal states, particularly winter non-migratory/non-breeding (NMB) state under short days, and spring premigratory/pre-breeding (PMB) and migratory/breeding (MB) states under long days. There were significantly increased CART-immunoreactive cells, and percent fluorescent area of CART-immunoreactivity was significantly increased in all mapped hypothalamic areas, except the SCN, PVN, AN, and DMN in photostimulated PMB and MB states, as compared to the non-stimulated NMB state. In particular, CART was richly expressed in the medial preoptic nucleus, LHN, IH and IN during MB state in which buntings showed reduced food intake and increased night-time activity. These results suggest that changes in the activity of the CART-containing system in different brain regions were associated with heightened energy needs of the photoperiod-induced seasonal responses during spring migration and reproduction in migratory songbirds.

Abercrombie M (1946) Estimation of nuclear population from microtome sections. Anat Rec 94:239–247. https://doi.org/10.1002/ar.1090940210CrossRefPubMed

Agatsuma R, Ramenofsky M (2006) Migratory behaviour of captive white-crowned sparrows, Zonotrichia leucophrys gambelii, differs during autumn and spring migration. Behaviour 143:1219–1240. https://doi.org/10.1163/156853906778691586CrossRef

Akash G, Kaniganti T, Tiwari NK et al (2014) Differential distribution and energy status-dependent regulation of the four CART neuropeptide genes in the zebrafish brain. J Comp Neurol 522:2266–2285. https://doi.org/10.1002/cne.23532CrossRefPubMed

Ali S, Dillon RS (1974) Handbook of the Birds of India and Pakistan. Oxford University Press, Bombay London New York

Bairlein F (2002) How to get fat: nutritional mechanisms of seasonal fat accumulation in migratory songbirds. Naturwissenschaften 89:1–10. https://doi.org/10.1007/s00114-001-0279-6CrossRefPubMed

Barsh GS, Schwartz MW (2002) Genetic approaches to studying energy balance: perception and integration. Nat Rev Genet 3:589–600. https://doi.org/10.1038/nrg862CrossRefPubMed

Bellinger LL, Bernardis LL (2002) The dorsomedial hypothalamic nucleus and its role in ingestive behavior and body weight regulation: Lessons learned from lesioning studies. Physiol Behav 76:431–442. https://doi.org/10.1016/S0031-9384(02)00756-4CrossRefPubMed

Bons N (1980) The topography of mesotocin and vasotocin systems in the brain of the domestic mallard and Japanese quail: immunocytochemical identification. Cell Tissue Res 213:37–51. https://doi.org/10.1007/BF00236919CrossRefPubMed

Boswell T (2005) Regulation of energy balance in birds by the neuroendocrine hypothalamus. J Poult Sci 42:161–181. https://doi.org/10.2141/jpsa.42.161CrossRef

Boswell T, Dunn IC (2017) Regulation of agouti-related protein and pro-opiomelanocortin gene expression in the avian arcuate nucleus. Front Endocrinol (Lausanne) 8:75. https://doi.org/10.3389/fendo.2017.00075CrossRef

Boswell T, Li Q, Takeuchi S (2002) Neurons expressing neuropeptide Y mRNA in the infundibular hypothalamus of Japanese quail are activated by fasting and co-express agouti-related protein mRNA. Brain Res Mol Brain Res 100:31–42. https://doi.org/10.1016/S0169-328X(02)00145-6CrossRefPubMed

Bottjer SW (1993) The distribution of tyrosine hydroxylase immunoreactivity in the brains of male and female zebra finches. J Neurobiol. https://doi.org/10.1002/neu.480240105CrossRefPubMed

Brandstätterr R, Abraham U (2003) Hypothalamic circadian organization in birds. I. Anatomy, functional morphology, and terminology of the suprachiasmatic region. Chronobiol Int 20:637–655. https://doi.org/10.1081/cbi-120023343CrossRef

Budki P, Rani S, Kumar V (2009) Food deprivation during photosensitive and photorefractory life-history stages affects the reproductive cycle in the migratory red-headed bunting, Emberiza bruniceps. J Exp Biol 212:225–230. https://doi.org/10.1242/jeb.024190CrossRefPubMed

Cai G, Mo C, Huang L et al (2015) Characterization of the two CART genes (CART1 and CART2) in chickens (Gallus gallus). PLoS ONE 10:e0127107. https://doi.org/10.1371/journal.pone.0127107CrossRefPubMedPubMedCentral

Calle M, Kozicz T, van der Linden E et al (2006) Effect of starvation on Fos and neuropeptide immunoreactivities in the brain and pituitary gland of Xenopus laevis. Gen Comp Endocrinol 147:237–246. https://doi.org/10.1016/j.ygcen.2006.01.007CrossRefPubMed

Cardot J, Griffond B, Risold P-Y et al (1999) Melanin-concentrating hormone-producing neurons in birds. J Comp Neurol 411:239–256. https://doi.org/10.1002/(SICI)1096-9861(19990823)411:2%3c239::AID-CNE5%3e3.0.CO;2-7CrossRefPubMed

Caughey SD, Wilson PW, Mukhtar N et al (2018) Sex differences in basal hypothalamic anorectic and orexigenic gene expression and the effect of quantitative and qualitative food restriction. Biol Sex Differ 9:20. https://doi.org/10.1186/s13293-018-0178-6CrossRefPubMedPubMedCentral

Chokchaloemwong D, Prakobsaeng N, Sartsoongnoen N et al (2013) Mesotocin and maternal care of chicks in native Thai hens (Gallus domesticus). Horm Behav. https://doi.org/10.1016/j.yhbeh.2013.04.010CrossRefPubMed

Chou TC, Scammell TE, Gooley JJ et al (2003) Critical role of dorsomedial hypothalamic nucleus in a wide range of behavioral circadian rhythms. J Neurosci 23:10691–10702. https://doi.org/10.1523/JNEUROSCI.23-33-10691.2003CrossRefPubMedPubMedCentral

Chronwall BM, DiMaggio DA, Massari VJ et al (1985) The anatomy of neuropeptide-Y-containing neurons in rat brain. Neuroscience 15:1159–1181. https://doi.org/10.1016/0306-4522(85)90260-XCrossRefPubMed

Coons EE, Levak M, Miller NE (1965) Lateral hypothalamus: learning of food-seeking response motivated by electrical stimulation. Science 80(150):1320–1321. https://doi.org/10.1126/science.150.3701.1320CrossRef

Elias CF, Lee CE, Kelly JF et al (2001) Characterization of CART neurons in the rat and human hypothalamus. J Comp Neurol 432:1–19. https://doi.org/10.1002/cne.1085CrossRefPubMed

Elmquist JK, Maratos-Flier E, Saper CB, Flier JS (1998) Unraveling the central nervous system pathways underlying responses to leptin. Nat Neurosci 1:445–450. https://doi.org/10.1038/2164CrossRefPubMed

Elmquist JK, Elias CF, Saper CB (1999) From lesions to leptin: hypothalamic control of food intake and body weight. Neuron 22:221–232. https://doi.org/10.1016/S0896-6273(00)81084-3CrossRef

Farzi A, Lau J, Ip CK et al (2018) Arcuate nucleus and lateral hypothalamic CART neurons in the mouse brain exert opposing effects on energy expenditure. Elife 7:e36494. https://doi.org/10.7554/eLife.36494CrossRefPubMedPubMedCentral

García-Fernández JM, Cernuda-Cernuda R, Davies WIL et al (2015) The hypothalamic photoreceptors regulating seasonal reproduction in birds: a prime role for VA opsin. Front Neuroendocrinol 37:13–28. https://doi.org/10.1016/j.yfrne.2014.11.001CrossRefPubMed

Gombash SE, Manfredsson FP, Mandel RJ et al (2014) Neuroprotective potential of pleiotrophin overexpression in the striatonigral pathway compared with overexpression in both the striatonigral and nigrostriatal pathways. Gene Ther 21:682–693CrossRef

Goodson JL, Kelly AM, Kingsbury MA (2012) Evolving nonapeptide mechanisms of gregariousness and social diversity in birds. Horm Behav 61:239–250. https://doi.org/10.1016/j.yhbeh.2012.01.005CrossRefPubMedPubMedCentral

Gooley JJ, Schomer A, Saper CB (2006) The dorsomedial hypothalamic nucleus is critical for the expression of food-entrainable circadian rhythms. Nat Neurosci 9:398–407. https://doi.org/10.1038/nn1651CrossRefPubMed

Gutekunst C-A, Stewart EN, Gross RE (2010) Immunohistochemical distribution of plexinA4 in the adult rat central nervous system. Front Neuroanat 4:1–17. https://doi.org/10.3389/fnana.2010.00025CrossRef

Gutierrez-Ibanez C, Iwaniuk AN, Jensen M et al (2016) Immunohistochemical localization of cocaine- and amphetamine-regulated transcript peptide (CARTp) in the brain of the pigeon (Columba livia) and zebra finch (Taeniopygia guttata). J Comp Neurol 524:3747–3773. https://doi.org/10.1002/cne.24028CrossRefPubMed

Gwinner E, Czeschlik D (1978) On the significance of spring migratory restlessness in caged birds. Oikos 30:364–372. https://doi.org/10.2307/3543485CrossRef

Hall ZJ, Healy SD, Meddle SL (2015) A role for nonapeptides and dopamine in nest-building behaviour. J Neuroendocrinol 27:158–165. https://doi.org/10.1111/jne.12250CrossRefPubMedPubMedCentral

Higgins SE, Ellestad LE, Trakooljul N et al (2010) Transcriptional and pathway analysis in the hypothalamus of newly hatched chicks during fasting and delayed feeding. BMC Genomics 11:162. https://doi.org/10.1186/1471-2164-11-162CrossRefPubMedPubMedCentral

Ho T, Jobling AI, Greferath U et al (2015) Vesicular expression and release of ATP from dopaminergic neurons of the mouse retina and midbrain. Front Cell Neurosci 9:389. https://doi.org/10.3389/fncel.2015.00389CrossRefPubMedPubMedCentral

Honda K, Kamisoyama H, Saneyasu T et al (2007) Central administration of insulin suppresses food intake in chicks. Neurosci Lett 423:153–157. https://doi.org/10.1016/j.neulet.2007.07.004CrossRefPubMed

Kabelik D, Schrock SE, Ayres LC, Goodson JL (2011) Estrogenic regulation of dopaminergic neurons in the opportunistically breeding zebra finch. Gen Comp Endocrinol 173:96–104. https://doi.org/10.1016/j.ygcen.2011.04.026CrossRefPubMedPubMedCentral

Kádár A, Sánchez E, Wittmann G et al (2010) Distribution of hypophysiotropic thyrotropin-releasing hormone (TRH)-synthesizing neurons in the hypothalamic paraventricular nucleus of the mouse. J Comp Neurol 518:3948–3961. https://doi.org/10.1002/cne.22432CrossRefPubMedPubMedCentral

Koylu EO, Couceyro PR, Lambert PD et al (1997) Immunohistochemical localization of novel CART peptides in rat hypothalamus, pituitary and adrenal gland. J Neuroendocrinol 9:823–833. https://doi.org/10.1046/j.1365-2826.1997.00651.xCrossRefPubMed

Kristensen P, Judge ME, Thim L et al (1998) Hypothalamic CART is a new anorectic peptide regulated by leptin. Nature 393:72–76. https://doi.org/10.1038/29993CrossRef

Kuenzel WJ (2000) Central nervous system regulation of gonadal development in the avian male. Poult Sci. https://doi.org/10.1093/ps/79.11.1679CrossRefPubMed

Kuenzel WJ, van Tienhoven A (1982) Nomenclature and location of avian hypothalamic nuclei and associated circumventricular organs. J Comp Neurol 206:293–313. https://doi.org/10.1002/cne.902060309CrossRefPubMed

Kumar V, Wingfield JC, Dawson A et al (2010) Biological clocks and regulation of seasonal reproduction and migration in birds. Physiol Biochem Zool 83:827–835. https://doi.org/10.1086/652243CrossRefPubMed

Lambert PD, Couceyro PR, McGirr KM et al (1998) CART peptides in the central control of feeding and interactions with neuropeptide Y. Synapse 29:293–298. https://doi.org/10.1002/(SICI)1098-2396(199808)29:4%3c293::AID-SYN1%3e3.0.CO;2-0CrossRefPubMed

Lau J, Herzog H (2014) CART in the regulation of appetite and energy homeostasis. Front Neurosci 8:313. https://doi.org/10.3389/fnins.2014.00313CrossRefPubMedPubMedCentral

Lau J, Farzi A, Qi Y et al (2018) CART neurons in the arcuate nucleus and lateral hypothalamic area exert differential controls on energy homeostasis. Mol Metab 7:102–118. https://doi.org/10.1016/j.molmet.2017.10.015CrossRefPubMed

Lázár G, Calle M, Roubos EW, Kozicz T (2004) Immunohistochemical localization of cocaine- and amphetamine-regulated transcript peptide in the central nervous system of the frog, Rana esculenta. J Comp Neurol 477:324–339. https://doi.org/10.1002/cne.20264CrossRefPubMed

Loh K, Herzog H, Shi Y-C (2015) Regulation of energy homeostasis by the NPY system. Trends Endocrinol Metab 26:125–135. https://doi.org/10.1016/j.tem.2015.01.003CrossRefPubMed

Majumdar G, Yadav G, Rani S, Kumar V (2014) A photoperiodic molecular response in migratory redheaded bunting exposed to a single long day. Gen Comp Endocrinol 204:104–113. https://doi.org/10.1016/j.ygcen.2014.04.013CrossRefPubMed

Malik S, Rani S, Kumar V (2004) Wavelength dependency of light-induced effects on photoperiodic clock in the migratory blackheaded bunting, Emberiza melanocephala. Chronobiol Int 21:367–384. https://doi.org/10.1081/CBI-120038742CrossRefPubMed

Meddle SL, Follett BK (1997) Photoperiodically driven changes in Fos expression within the basal tuberal hypothalamus and median eminence of Japanese quail. J Neurosci 17:8909–8918. https://doi.org/10.1523/JNEUROSCI.17-22-08909.1997CrossRefPubMedPubMedCentral

Mercer JG, Tups A (2003) Neuropeptides and anticipatory changes in behaviour and physiology: seasonal body weight regulation in the siberian hamster. Eur J Pharmacol 480:43–50. https://doi.org/10.1016/j.ejphar.2003.08.091CrossRefPubMed

Mishra I, Singh D, Kumar V (2017) Seasonal alterations in the daily rhythms in hypothalamic expression of genes involved in the photoperiodic transduction and neurosteroid-dependent processes in migratory blackheaded buntings. J Neuroendocrinol. https://doi.org/10.1111/jne.12469CrossRefPubMed

Mishra I, Singh D, Kumar V (2018) Temporal expression of c-fos and genes coding for neuropeptides and enzymes of amino acid and amine neurotransmitter biosynthesis in retina, pineal and hypothalamus of a migratory songbird: evidence for circadian rhythm-dependent seasonal responses. Neuroscience 371:309–324. https://doi.org/10.1016/j.neuroscience.2017.12.016CrossRefPubMed

Okumura T, Yamada H, Motomura W, Kohgo Y (2000) Cocaine-amphetamine-regulated transcript (CART) acts in the central nervous system to inhibit gastric acid secretion via brain corticotropin-releasing factor system. Endocrinology 141:2854–2860. https://doi.org/10.1210/endo.141.8.7588CrossRefPubMed

Petrovich GD (2018) Lateral hypothalamus as a motivation-cognition interface in the control of feeding behavior. Front Syst Neurosci. https://doi.org/10.3389/fnsys.2018.00014CrossRefPubMedPubMedCentral

Phillips-Singh D, Li Q, Takeuchi S et al (2003) Fasting differentially regulates expression of agouti-related peptide, pro-opiomelanocortin, prepro-orexin, and vasoactive intestinal polypeptide mRNAs in the hypothalamus of Japanese quail. Cell Tissue Res 313:217–225. https://doi.org/10.1007/s00441-003-0755-8CrossRefPubMed

Rani S, Singh S, Misra M et al (2005) Daily light regulates seasonal responses in the migratory male redheaded bunting, Emberiza bruniceps. J Exp Zool A Comp Exp Biol 303:541–550. https://doi.org/10.1002/jez.a.187CrossRefPubMed

Rani S, Malik S, Trivedi AK et al (2006) A circadian clock regulates migratory restlessness in the blackheaded bunting, Emberiza melanocephala. Curr Sci 91:1093–1096

Raptis S, Fekete C, Sarkar S et al (2004) Cocaine- and amphetamine-regulated transcript co-contained in thyrotropin-releasing hormone (TRH) neurons of the hypothalamic paraventricular nucleus modulates TRH-induced prolactin secretion. Endocrinology 145:1695–1699. https://doi.org/10.1210/en.2003-1576CrossRefPubMed

Rastogi A, Kumari Y, Rani S, Kumar V (2011) Phase inversion of neural activity in the olfactory and visual systems of a night-migratory bird during migration. Eur J Neurosci 34:99–109. https://doi.org/10.1111/j.1460-9568.2011.07737.xCrossRefPubMed

Rastogi A, Kumari Y, Rani S, Kumar V (2013) Neural correlates of migration: activation of hypothalamic clock(s) in and out of migratory state in the blackheaded bunting Emberiza melanocephala. PLoS ONE 8:e70065. https://doi.org/10.1371/journal.pone.0070065CrossRefPubMedPubMedCentral

Rondini TA, Baddini SP, Sousa LF et al (2004) Hypothalamic cocaine- and amphetamine-regulated transcript neurons project to areas expressing gonadotropin releasing hormone immunoreactivity and to the anteroventral periventricular nucleus in male and female rats. Neuroscience 125:735–748. https://doi.org/10.1016/j.neuroscience.2003.12.045CrossRefPubMed

Sen S, Parishar P, Pundir AS et al (2019) The expression of tyrosine hydroxylase and DARPP-32 in the house crow (Corvus splendens) brain. J Comp Neurol 527:1–36. https://doi.org/10.1002/cne.24649CrossRef

Sharma A, Singh D, Malik S et al (2018) Difference in control between spring and autumn migration in birds: insight from seasonal changes in hypothalamic gene expression in captive buntings. Biol Sci. https://doi.org/10.1098/rspb.2018.1531CrossRef

Singh D, Kumari Y, Rastogi A et al (2013) Neuropeptide Y mRNA and peptide in the night-migratory redheaded bunting brain. Cell Tissue Res 354:551–562. https://doi.org/10.1007/s00441-013-1667-xCrossRef

Singh D, Trivedi AK, Rani S et al (2015) Circadian timing in central and peripheral tissues in a migratory songbird: dependence on annual life-history states. FASEB J 29:4248–4255. https://doi.org/10.1096/fj.15-275339CrossRefPubMedPubMedCentral

Singh O, Kumar S, Singh U et al (2016a) Cocaine- and amphetamine-regulated transcript peptide (CART) in the brain of zebra finch, Taeniopygia guttata: Organization, interaction with neuropeptide Y, and response to changes in energy status. J Comp Neurol 524:3014–3041. https://doi.org/10.1002/cne.24004CrossRefPubMed

Singh O, Kumar S, Singh U et al (2016b) Role of isotocin in the regulation of the hypophysiotropic dopamine neurones in the preoptic area of the catfish Clarias batrachus. J Neuroendocrinol. https://doi.org/10.1111/jne.12441CrossRefPubMed

Singh O, Pradhan D, Nagalakashmi B et al (2019) Thyrotropin-releasing hormone (TRH) in the brain and pituitary of the teleost, Clarias batrachus and its role in regulation of hypophysiotropic dopamine neurons. J Comp Neurol 527:1070–1101. https://doi.org/10.1002/cne.24570CrossRefPubMed

Singru PS, Mazumdar M, Sakharkar AJ et al (2007) Immunohistochemical localization of cocaine- and amphetamine-regulated transcript peptide in the brain of the catfish, Clarias batrachus (Linn.). J Comp Neurol 502:215–235. https://doi.org/10.1002/cne.21295CrossRefPubMed

Song Z, Liu L, Yue Y et al (2012) Fasting alters protein expression of AMP-activated protein kinase in the hypothalamus of broiler chicks (Gallus gallus domesticus). Gen Comp Endocrinol 178:546–555. https://doi.org/10.1016/j.ygcen.2012.06.026CrossRefPubMed

Stevenson TJ, Kumar V (2017) Neural control of daily and seasonal timing of songbird migration. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 203:399–409. https://doi.org/10.1007/s00359-017-1193-5CrossRefPubMed

Stuber GD, Wise RA (2016) Lateral hypothalamic circuits for feeding and reward. Nat Neurosci 19:198–205. https://doi.org/10.1038/nn.4220CrossRefPubMedPubMedCentral

Subhedar N, Barsagade VG, Singru PS et al (2011) Cocaine- and amphetamine-regulated transcript peptide (CART) in the telencephalon of the catfish, Clarias gariepinus: Distribution and response to fasting, 2-deoxy-d-glucose, glucose, insulin, and leptin treatments. J Comp Neurol 519:1281–1300. https://doi.org/10.1002/cne.22569CrossRefPubMed

Subhedar NK, Nakhate KT, Upadhya MA, Kokare DM (2014) CART in the brain of vertebrates: circuits, functions and evolution. Peptides 54:108–130. https://doi.org/10.1016/j.peptides.2014.01.004CrossRefPubMed

Surbhi KV (2015) Avian photoreceptors and their role in the regulation of daily and seasonal physiology. Gen Comp Endocrinol 220:13–22. https://doi.org/10.1016/j.ygcen.2014.06.001CrossRefPubMed

Surbhi RA, Rani S, Kumar V (2015) Seasonal plasticity in the peptide neuronal systems: potential roles of gonadotrophin-releasing hormone, gonadotrophin-inhibiting hormone, neuropeptide Y and vasoactive intestinal peptide in the regulation of the reproductive axis in subtropical Indian weaver birds. J Neuroendocrinol 27:357–369. https://doi.org/10.1111/jne.12274CrossRefPubMed

Surbhi RA, Malik S et al (2016) Changes in brain peptides associated with reproduction and energy homeostasis in photosensitive and photorefractory migratory redheaded buntings. Gen Comp Endocrinol 230–231:67–75. https://doi.org/10.1016/j.ygcen.2016.03.031CrossRefPubMed

Tachibana T, Takagi T, Tomonaga S et al (2003) Central administration of cocaine- and amphetamine-regulated transcript inhibits food intake in chicks. Neurosci Lett 337:131–134. https://doi.org/10.1016/S0304-3940(02)01321-6CrossRefPubMed

Tomaszuk A, Simpson C, Williams G (1996) Neuropeptide Y, the hypothalamus and the regulation of energy homeostasis. Horm Res 46:53–58. https://doi.org/10.1159/000184996CrossRefPubMed

Trivedi A, Kumar J, Rani S, Kumar V (2014) Annual life history-dependent gene expression in the hypothalamus and liver of a migratory songbird: insights into the molecular regulation of seasonal metabolism. J Biol Rhythms 29:332–345. https://doi.org/10.1177/0748730414549766CrossRefPubMed

True C, Verma S, Grove KL, Smith MS (2013) Cocaine- and amphetamine-regulated transcript is a potent stimulator of GnRH and kisspeptin cells and may contribute to negative energy balance-induced reproductive inhibition in females. Endocrinology 154:2821–2832. https://doi.org/10.1210/en.2013-1156CrossRefPubMedPubMedCentral

Vrang N (2006) Anatomy of hypothalamic CART neurons. Peptides 27:1970–1980. https://doi.org/10.1016/j.peptides.2005.10.029CrossRefPubMed

Vrang N, Larsen PJ, Clausen JT, Kristensen P (1999) Neurochemical characterization of hypothalamic cocaine- amphetamine-regulated transcript neurons. J Neurosci. https://doi.org/10.1523/JNEUROSCI.19-10-j0006.1999CrossRefPubMedPubMedCentral

Vrang N, Larsen PJ, Kristensen P, Tang-Christensen M (2000) Central administration of cocaine-amphetamine-regulated transcript activates hypothalamic neuroendocrine neurons in the rat. Endocrinology 141:794–801. https://doi.org/10.1210/endo.141.2.7295CrossRefPubMed

Yanik T, Dominguez G, Kuhar MJ et al (2006) The Leu34Phe ProCART mutation leads to cocaine- and amphetamine-regulated transcript (CART) deficiency: a possible cause for obesity in humans. Endocrinology 147:39–43. https://doi.org/10.1210/en.2005-0812CrossRefPubMed

Yoshimura T, Yasuo S, Suzuki Y et al (2001) Identification of the suprachiasmatic nucleus in birds. Am J Physiol Regul Integr Comp Physiol 280:R1185–R1189. https://doi.org/10.1152/ajpregu.2001.280.4.R1185CrossRefPubMed

Title: Concurrent changes in photoperiod-induced seasonal phenotypes and hypothalamic CART peptide-containing systems in night-migratory redheaded buntings
Authors: Omprakash Singh
Neha Agarwal
Anupama Yadav
Sumela Basu
Shalie Malik
Sangeeta Rani
Vinod Kumar
Praful S. Singru
Publication date: 01-12-2020
Publisher: Springer Berlin Heidelberg
Published in: Brain Structure and Function / Issue 9/2020
Print ISSN: 1863-2653
Electronic ISSN: 1863-2661
DOI: https://doi.org/10.1007/s00429-020-02154-y

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Concurrent changes in photoperiod-induced seasonal phenotypes and hypothalamic CART peptide-containing systems in night-migratory redheaded buntings

Abstract

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Abstract

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