Skip to main content
SpringerLink
Log in

Neuropeptide Y-induced feeding is dependent on GABAA receptors in neonatal chicks

  • Original Paper
  • Published:
Journal of Comparative Physiology A Aims and scope Submit manuscript

Abstract

In mammals and birds, neuropeptide Y (NPY) and gamma-aminobutyric acid (GABA) are found in brain areas known to be involved in the control of ingestive behavior and act to increase voluntary food intake. In rats, significant evidence suggest a functional and behavioral interaction between NPY and GABA mediated transmission in various brain regions, including the arcuate and paraventricular nuclei of the hypothalamus which can be important in the regulation of feeding behavior. In the present study, the effect of intracerebroventricular (ICV) administration of NPY and GABA receptor antagonists on food intake was examined in neonatal chicks. The ICV injection of NPY strongly stimulated food intake while co-administration of NPY and picrotoxin, a GABAA antagonist, (but not CGP54626, a GABAB antagonist) weakened food intake induced by NPY. These results suggest that central NPY stimulates food intake in neonatal chicks by interaction with the GABAergic system via GABAA receptors.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Abbreviations

AgRP:

Agouti-related protein

ANOVA:

Analysis of variance

ARC:

Arcuate nucleus

CRF:

Corticotrophin releasing factor

DMSO:

Dimethyl sulfoxide

GABA:

Gamma-aminobutyric acid

ICV:

Intracerebroventricular

NPY:

Neuropeptide Y

PVN:

Paraventricular nucleus

SEM:

Standard Error of the mean

SPSS:

Statistical Package for the Social Sciences

References

  • Ando R, Kawakami SI, Bungo T, Ohgushi A, Takagi T, Denbow DM, Furuse M (2001) Feeding responses to several neuropeptide Y receptor agonists in the neonatal chick. Eur J Pharmacol 427:53–59

    Article  PubMed  CAS  Google Scholar 

  • Backberg M, Collin M, Ovesjo ML, Meister B (2003) Chemical coding of GABA(B) receptor-immunoreactive neurones in hypothalamic regions regulating body weight. J Neuroendocrinol 15:1–14

    Article  PubMed  CAS  Google Scholar 

  • Backberg M, Ultenius C, Fritschy JM, Meister B (2004) Cellular localization of GABA receptor alpha subunit immunoreactivity in the rat hypothalamus: relationship with neurones containing orexigenic or anorexigenic peptides. J Neuroendocrinol 16:589–604

    Article  PubMed  CAS  Google Scholar 

  • Beck B, Stricker-Krongrad A, Nicolas JP, Burlet C (1992) Chronic and continuous intracerebroventricular infusion of neuropeptide Y in Long-Evans rats mimics the feeding behaviour of obese Zucker rats. Int J Obes Relat Metab Disord 16:295–302

    PubMed  CAS  Google Scholar 

  • Bertile F, Oudart H, Criscuolo F, Maho YL, Raclot T (2003) Hypothalamic gene expression in long-term fasted rats: relationship with body fat. Biochem Biophys Res Commun 303:1106–1113

    Article  PubMed  CAS  Google Scholar 

  • Bromee T, Sjodin P, Fredriksson R, Boswell T, Larsson TA, Salaneck E, Zoorob R, Mohell N, Larhammar D (2006) Neuropeptide Y-family receptors Y6 and Y7 in chicken. Cloning, pharmacological characterization, tissue distribution and conserved synteny with human chromosome region. FEBS J 273:2048–2063

    Article  PubMed  CAS  Google Scholar 

  • Bungo T, Izumi T, Kawamura K, Takagi T, Ueda H, Furuse M (2003) Intracerebroventricular injection of muscimol, baclofen or nipecotic acid stimulates food intake in layer-type, but not meat-type, chicks. Brain Res 993:235–238

    Article  PubMed  CAS  Google Scholar 

  • Cone RD (2005) Anatomy and regulation of the central melanocortin system. Nat Neurosci 8:571–578

    Article  PubMed  CAS  Google Scholar 

  • Cowley MA, Smart JL, Rubinstein M, Cerdan MG, Diano S, Horvath TL, Cone RD, Low MJ (2001) Leptin activates anorexigenic POMC neurons through a neural network in the arcuate nucleus. Nature 411:480–484

    Article  PubMed  CAS  Google Scholar 

  • Csillag A, Stewart MG, Curtis EM (1987) GABAergic structures in the chick telencephalon: GABA immunocytochemistry combined with light and electron microscope autoradiography, and Golgi impregnation. Brain Res 437:283–297

    Article  PubMed  CAS  Google Scholar 

  • Davis JL, Masuoka DT, Gerbrandt LK, Cherkin A (1979) Autoradiographic distribution of l-proline in chicks after intracerebral injection. Physiol Behav 22:693–695

    Article  PubMed  CAS  Google Scholar 

  • Decavel C, Van den Pol AN (1990) GABA: a dominant neurotransmitter in the hypothalamus. J Comp Neurol 302:1019–1037

    Article  PubMed  CAS  Google Scholar 

  • Denbow DM (1991) Induction of food intake by a GABAergic mechanism in the turkey. Physiol Behav 49:485–488

    Article  PubMed  CAS  Google Scholar 

  • Denbow DM, Snapir N, Furuse M (1999) Inhibition of food intake by CRF in chickens. Physiol Behav 66:645–649

    Article  PubMed  CAS  Google Scholar 

  • Dodo K, Izumi T, Ueda H, Bungo T (2005) Response of neuropeptide Y-induced feeding to mu-, delta- and kappa-opioid receptor antagonists in the neonatal chick. Neurosci Lett 373:85–88

    Article  PubMed  CAS  Google Scholar 

  • Dridi S, Swennen Q, Decuypere E, Buyse J (2005) Mode of leptin action in chicken hypothalamus. Brain Res 1047:214–223

    Article  PubMed  CAS  Google Scholar 

  • Ebenezer IS (1990) The effect of intracerebroventricular administration of baclofen on food intake in rats. NeuroReport 1:73–76

    Article  PubMed  CAS  Google Scholar 

  • Furuse M, Matsumoto M, Okumura J, Sugahara K, Hasegawa S (1997a) Intracerebroventricular injection of mammalian and chicken glucagon-like peptide-1 inhibits food intake of the neonatal chick. Brain Res 755:167–169

    Article  PubMed  CAS  Google Scholar 

  • Furuse M, Matsumoto M, Saito N, Sugahara K, Hasegawa S (1997b) The central corticotropin-releasing factor and glucagon-like peptide-1 in food intake of the neonatal chick. Eur J Pharmacol 339:211–214

    Article  PubMed  CAS  Google Scholar 

  • Gerald C, Walker MW, Criscione L, Gustafson EL, Batzl-Hartmann C, Smith KE, Vaysse P, Durkin MM, Laz TM, Linemeyer DL, Schaffhauser AO, Whitebread S, Hofbauer KG, Taber RI, Branchek TA, Weinshank RL (1996) A receptor subtype involved in neuropeptide-Y-induced food intake. Nature 382:168–171

    Article  PubMed  CAS  Google Scholar 

  • Granda RH, Crossland WJ (1989) GABA-like immunoreactivity of neurons in the chicken diencephalon and mesencephalon. J Comp Neurol 287:455–469

    Article  PubMed  CAS  Google Scholar 

  • Herzog H, Hort YJ, Shine J, Selbie LA (1993) Molecular cloning, characterization, and localization of the human homolog to the reported bovine NPY Y3 receptor: lack of NPY binding and activation. DNA Cell Biol 12:465–471

    Article  PubMed  CAS  Google Scholar 

  • Holmberg SK, Mikko S, Boswell T, Zoorob R, Larhammar D (2002) Pharmacological characterization of cloned chicken neuropeptide Y receptors Y1 and Y5. J Neurochem 81:462–471

    Article  PubMed  CAS  Google Scholar 

  • Horvath TL, Bechmann I, Naftolin F, Kalra SP, Leranth C (1997) Heterogeneity in the neuropeptide Y-containing neurons of the rat arcuate nucleus: GABAergic and non-GABAergic subpopulations. Brain Res 756:283–286

    Article  PubMed  CAS  Google Scholar 

  • Jazin EE, Yoo H, Blomqvist AG, Yee F, Weng G, Walker MW, Salon J, Larhammar D, Wahlestedt C (1993) A proposed bovine neuropeptide Y (NPY) receptor cDNA clone, or its human homologue, confers neither NPY binding sites nor NPY responsiveness on transfected cells. Regul Pept 47:247–258

    Article  PubMed  CAS  Google Scholar 

  • Jonaidi H, Babapour V, Denbow DM (2002) GABAergic control of food intake in the meat-type chickens. Physiol Behav 76:465–468

    Article  PubMed  CAS  Google Scholar 

  • Jonaidi H, Abbassi L, Yaghoobi MM, Kaiya H, Denbow DM, Kamali Y, Shojaei B (2012) The role of GABAergic system on the inhibitory effect of ghrelin on food intake in neonatal chicks. Neurosci Lett 520:82–86

    Article  PubMed  CAS  Google Scholar 

  • Kameda Y, Miura M, Nishimaki T (2001) Localization of neuropeptide Y mRNA and peptide in the chicken hypothalamus and their alterations after food deprivation, dehydration, and castration. J Comp Neurol 436:376–388

    Article  PubMed  CAS  Google Scholar 

  • Kanatani A, Mashiko S, Murai N, Sugimoto N, Ito J, Fukuroda T, Fukami T, Morin N, MacNeil DJ, Van der Ploeg LH, Saga Y, Nishimura S, Ihara M (2000) Role of the Y1 receptor in the regulation of neuropeptide Y-mediated feeding: comparison of wild-type, Y1 receptor-deficient, and Y5 receptor-deficient mice. Endocrinology 141:1011–1016

    Article  PubMed  CAS  Google Scholar 

  • Kuenzel WJ, Douglass LW, Davison BA (1987) Robust feeding following central administration of neuropeptide Y or peptide YY in chicks, Gallus domesticus. Peptides 8:823–828

    Article  PubMed  CAS  Google Scholar 

  • Larhammar D (1996) Structural diversity of receptors for neuropeptide Y, peptide YY and pancreatic polypeptide. Regul Pept 65:165–174

    Article  PubMed  CAS  Google Scholar 

  • Lecklin A, Lundell I, Paananen L, Wikberg JE, Mannisto PT, Larhammar D (2002) Receptor subtypes Y1 and Y5 mediate neuropeptide Y induced feeding in the guinea-pig. Br J Pharmacol 135:2029–2037

    Article  PubMed  CAS  Google Scholar 

  • Levine AS, Morley JE (1984) Neuropeptide Y: a potent inducer of consummatory behavior in rats. Peptides 5:1025–1029

    Article  PubMed  CAS  Google Scholar 

  • Lundell I, Boswell T, Larhammar D (2002) Chicken neuropeptide Y-family receptor Y4: a receptor with equal affinity for pancreatic polypeptide, neuropeptide Y and peptide YY. J Mol Endocrinol 28:225–235

    Article  PubMed  CAS  Google Scholar 

  • Morris BJ (1989) Neuronal localisation of neuropeptide Y gene expression in rat brain. J Comp Neurol 290:358–368

    Article  PubMed  CAS  Google Scholar 

  • Muroya S, Funahashi H, Uramura K, Shioda S, Yada T (2005) Gamma aminobutyric acid regulates glucosensitive neuropeptide Y neurons in arcuate nucleus via A/B receptors. NeuroReport 16:897–901

    Article  PubMed  CAS  Google Scholar 

  • Olgiati VR, Netti C, Guidobono F, Pecile A (1980) The central GABAergic system and control of food intake under different experimental conditions. Psychopharmacology 68:163–167

    Article  PubMed  CAS  Google Scholar 

  • Pu S, Jain MR, Horvath TL, Diano S, Kalra PS, Kalra SP (1999) Interactions between neuropeptide Y and gamma-aminobutyric acid in stimulation of feeding: a morphological and pharmacological analysis. Endocrinology 140:933–940

    Article  PubMed  CAS  Google Scholar 

  • Richards MP, Proszkowiec-Weglarz M (2007) Mechanisms regulating feed intake, energy expenditure, and body weight in poultry. Poult Sci 86:1478–1490

    PubMed  CAS  Google Scholar 

  • Saito ES, Kaiya H, Tachibana T, Tomonaga S, Denbow DM, Kangawa K, Furuse M (2005) Inhibitory effect of ghrelin on food intake is mediated by the corticotropin-releasing factor system in neonatal chicks. Regul Pept 125:201–208

    Article  PubMed  CAS  Google Scholar 

  • Salaneck E, Holmberg SK, Berglund MM, Boswell T, Larhammar D (2000) Chicken neuropeptide Y receptor Y2: structural and pharmacological differences to mammalian Y2(1). FEBS Lett 484:229–234

    Article  PubMed  CAS  Google Scholar 

  • Saneyasu T, Honda K, Kamisoyama H, Ikura A, Nakayama Y, Hasegawa S (2011) Neuropeptide Y effect on food intake in broiler and layer chicks. Comp Biochem Physiol A: Mol Integr Physiol 159:422–426

    Article  Google Scholar 

  • Schwartz MW, Sipols AJ, Marks JL, Sanacora G, White JD, Scheurink A, Kahn SE, Baskin DG, Woods SC, Figlewicz DP et al (1992) Inhibition of hypothalamic neuropeptide Y gene expression by insulin. Endocrinology 130:3608–3616

    Article  PubMed  CAS  Google Scholar 

  • Shiraishi J, Yanagita K, Fujita M, Bungo T (2008) Central insulin suppresses feeding behavior via melanocortins in chicks. Domest Anim Endocrinol 34:223–228

    Article  PubMed  CAS  Google Scholar 

  • Stephens TW, Basinski M, Bristow PK, Bue-Valleskey JM, Burgett SG, Craft L, Hale J, Hoffmann J, Hsiung HM, Kriauciunas A et al (1995) The role of neuropeptide Y in the antiobesity action of the obese gene product. Nature 377:530–532

    Article  PubMed  CAS  Google Scholar 

  • Tachibana T, Sugahara K, Ohgushi A, Ando R, Kawakami S, Yoshimatsu T, Furuse M (2001) Intracerebroventricular injection of agouti-related protein attenuates the anorexigenic effect of alpha-melanocyte stimulating hormone in neonatal chicks. Neurosci Lett 305:131–134

    Article  PubMed  CAS  Google Scholar 

  • Takagi T, Bungo T, Tachibana T, Saito ES, Saito S, Yamasaki I, Tomonaga S, Denbow DM, Furuse M (2003) Intracerebroventricular administration of GABA-A and GABA-B receptor antagonists attenuate feeding and sleeping-like behavior induced by L-pipecolic acid in neonatal chicks. J Neurosci Res 73:270–275

    Article  PubMed  CAS  Google Scholar 

  • van Tienhoven A, Juhász LP (1962) The chicken telencephalon, diencephalon and mesencephalon in stereotaxic coordinates. J Comp Neurol 118:185–197

    Article  Google Scholar 

  • Wang X, Day JR, Vasilatos-Younken R (2001) The distribution of neuropeptide Y gene expression in the chicken brain. Mol Cell Endocrinol 174:129–136

    Article  PubMed  CAS  Google Scholar 

  • Zhou W, Murakami M, Hasegawa S, Yoshizawa F, Sugahara K (2005) Neuropeptide Y content in the hypothalamic paraventricular nucleus responds to fasting and refeeding in broiler chickens. Comp Biochem Physiol A: Mol Integr Physiol 141:146–152

    Article  Google Scholar 

Download references

Acknowledgments

This study was supported by “Shahid Bahonar University of Kerman” Kerman, Iran. All experimental protocols were approved by the Research Ethic Committee of Neuroscience Research Center of Kerman, Iran. We are grateful to Mrs. Mary Ward for the English editing of the manuscript.

Author information

Authors and Affiliations

  1. Department of Basic Sciences, Faculty of Veterinary Medicine, Shahid Bahonar University of Kerman(SBUK), 76169-133, Kerman, Iran

    H. Jonaidi & Z. Noori

Authors
  1. H. Jonaidi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Z. Noori
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to H. Jonaidi.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Jonaidi, H., Noori, Z. Neuropeptide Y-induced feeding is dependent on GABAA receptors in neonatal chicks. J Comp Physiol A 198, 827–832 (2012). https://doi.org/10.1007/s00359-012-0753-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00359-012-0753-y

Keywords

Search

Navigation