Skip to main content
SpringerLink
Log in

Anxiogenic role of vasopressin during the early postnatal period: maternal separation-induced ultrasound vocalization in vasopressin-deficient Brattleboro rats

  • Original Article
  • Published:
Amino Acids Aims and scope Submit manuscript

Abstract

Both animal and human studies suggest that in adulthood, plasma vasopressin level correlates well with anxiety. Little is known about the mood regulation during the perinatal period. Here, we aim to investigate the influence of vasopressin on anxiety during the early postnatal age. As a sign of distress, rat pups emit ultrasonic vocalizations (USVs) when they are separated from their mother. This USV was detected in 7- to 8-day-old vasopressin-deficient Brattleboro pups, and they were compared to their heterozygote littermates and wild-type pups. The results were confirmed by V1b antagonist treatment (SSR149415 10 mg/kg ip 30 min before test) in wild-types. Chlordiazepoxide (3 mg/kg ip 30 min before test)—an anxiolytic—was used to test the interaction with the GABAergic system. At the end of the test, stress-hormone levels were measured by radioimmunoassay. Vasopressin-deficient pups vocalized substantially less than non-deficient counterparts. Treatment with V1b antagonist resulted in similar effect. Chlordiazepoxide reduced the frequency and duration of the vocalization only in wild-types. Reduced vocalization was accompanied by smaller adrenocorticotropin levels but the level of corticosterone was variable. Our results indicate that the anxiolytic effect of vasopressin deficiency (both genetic and pharmacological) exists already during the early postnatal age. Vasopressin interacts with the GABAergic system. As mood regulation does not go parallel with glucocorticoid levels, we suggest that vasopressin might have a direct effect on special brain areas.

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

References

  • Abelson JL, Khan S, Liberzon I, Young EA (2007) HPA axis activity in patients with panic disorder: review and synthesis of four studies. Depress Anxiety 24:66–76

    Article  PubMed  Google Scholar 

  • Aguilera G (1994) Regulation of pituitary ACTH secretion during chronic stress. Front Neuroendocrinol 15:321–350

    Article  CAS  PubMed  Google Scholar 

  • Aguilera G, Subburaju S, Young S, Chen J (2008) The parvocellular vasopressinergic system and responsiveness of the hypothalamic pituitary adrenal axis during chronic stress. Prog Brain Res 170:29–39

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Allin JT, Banks EM (1971) Effects of temperature on ultrasound production by infant albino rats. Dev Psychobiol 4:149–156

    Article  CAS  PubMed  Google Scholar 

  • Amikishieva AV, Ilnitskaya SI, Nikolin VP, Popova NA (2011) Effect of vasopressin V1b receptor antagonist, SSR149415, on anxiety-like behavior and Lewis lung carcinoma metastasis in mice. Exp Oncol 33:126–129

    CAS  PubMed  Google Scholar 

  • Arvat E, Giordano R, Grottoli S, Ghigo E (2002) Benzodiazepines and anterior pituitary function. J Endocrinol Invest 25:735–747

    Article  CAS  PubMed  Google Scholar 

  • Bayart F, Hayashi KT, Faull KF, Barchas JD, Levine S (1990) Influence of maternal proximity on behavioral and physiological responses to separation in infant rhesus monkeys (Macaca mulatta). Behav Neurosci 104:98–107

    Article  CAS  PubMed  Google Scholar 

  • Benton D, Nastiti K (1988) The influence of psychotropic drugs on the ultrasonic calling of mouse pups. Psychopharmacology 95:99–102

    Article  CAS  PubMed  Google Scholar 

  • Bleickardt CJ, Mullins DE, Macsweeney CP, Werner BJ, Pond AJ, Guzzi MF, Martin FD, Varty GB, Hodgson RA (2009) Characterization of the V1a antagonist, JNJ-17308616, in rodent models of anxiety-like behavior. Psychopharmacology 202:711–718

    Article  CAS  PubMed  Google Scholar 

  • Blumberg MS, Sokoloff G, Kent KJ (2000) A developmental analysis of clonidine’s effects on cardiac rate and ultrasound production in infant rats. Dev Psychobiol 36:186–193

    Article  CAS  PubMed  Google Scholar 

  • Bohus B, de Wied D (1998) The vasopressin deficient Brattleboro rats: a natural knockout model used in the search for CNS effects of vasopressin. Prog Brain Res 119:555–573

    Article  CAS  PubMed  Google Scholar 

  • Bornstein SR, Engeland WC, Ehrhart-Bornstein M, Herman JP (2008) Dissociation of ACTH and glucocorticoids. Trends Endocrinol Metab 19:175–180

    Article  CAS  PubMed  Google Scholar 

  • Branchi I, Santucci D, Alleva E (2001) Ultrasonic vocalisation emitted by infant rodents: a tool for assessment of neurobehavioural development. Behav Brain Res 125:49–56

    Article  CAS  PubMed  Google Scholar 

  • Buckingham JC, Leach JH (1980) Hypothalamo-pituitary-adrenocortical function in rats with inherited diabetes insipidus. J Physiol 305:397–404

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Caldwell HK, Lee HJ, Macbeth AH, Young WS 3rd (2008) Vasopressin: behavioral roles of an “original” neuropeptide. Prog Neurobiol 84:1–24

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Campo JV, Jansen-McWilliams L, Comer DM, Kelleher KJ (1999) Somatization in pediatric primary care: association with psychopathology, functional impairment, and use of services. J Am Acad Child Adolesc Psychiatry 38:1093–1101

    Article  CAS  PubMed  Google Scholar 

  • Claustre Y, Rouquier L, Desvignes C, Leonetti M, Montegut J, Aubin N, Allouard N, Bougault I, Oury-Donat F, Steinberg R (2006) Effects of the vasopressin (V1b) receptor antagonist, SSR149415, and the corticotropin-releasing factor 1 receptor antagonist, SSR125543, on FG 7142-induced increase in acetylcholine and norepinephrine release in the rat. Neuroscience 141:1481–1488

    Article  CAS  PubMed  Google Scholar 

  • Costello EJ, Egger HL, Angold A (2005) The developmental epidemiology of anxiety disorders: phenomenology, prevalence, and comorbidity. Child Adolesc Psychiatr Clin N Am 14:631–648 (vii)

    Article  PubMed  Google Scholar 

  • Decaux G, Soupart A, Vassart G (2008) Non-peptide arginine-vasopressin antagonists: the vaptans. Lancet 371:1624–1632

    Article  CAS  PubMed  Google Scholar 

  • Engelmann M, Ludwig M, Singewald N, Ebner K, Sabatier N, Lubec G, Landgraf R, Wotjak CT (2001) Taurine selectively modulates the secretory activity of vasopressin neurons in conscious rats. Eur J Neurosci 14:1047–1055

    Article  CAS  PubMed  Google Scholar 

  • Fenelon VS, Herbison AE (1995) Characterisation of GABAA receptor gamma subunit expression by magnocellular neurones in rat hypothalamus. Brain Res Mol Brain Res 34:45–56

    Article  CAS  PubMed  Google Scholar 

  • Frank E, Landgraf R (2008) The vasopressin system–from antidiuresis to psychopathology. Eur J Pharmacol 583:226–242

    Article  CAS  PubMed  Google Scholar 

  • Gallo-Payet N, Guillon G (1998) Regulation of adrenocortical function by vasopressin. Horm Metab Res 30:360–367

    Article  CAS  PubMed  Google Scholar 

  • Gardner CR (1985) Distress vocalization in rat pups. A simple screening method for anxiolytic drugs. J Pharmacol Methods 14:181–187

    Article  CAS  PubMed  Google Scholar 

  • Guldenaar SE, Pickering BT (1988) Mutant vasopressin precursor in the endoplasmic reticulum of the Brattleboro rat. Ultrastructural evidence from individual “vasopressin” cells localized with the light microscope by use of a new gold/silver method for immunostain enhancement. Cell Tissue Res 253:671–676

    Article  CAS  PubMed  Google Scholar 

  • Hard E, Engel J (1988) Effects of 8-OH-DPAT on ultrasonic vocalization and audiogenic immobility reaction in pre-weanling rats. Neuropharmacology 27:981–986

    Article  CAS  PubMed  Google Scholar 

  • Hodgson RA, Higgins GA, Guthrie DH, Lu SX, Pond AJ, Mullins DE, Guzzi MF, Parker EM, Varty GB (2007) Comparison of the V1b antagonist, SSR149415, and the CRF1 antagonist, CP-154,526, in rodent models of anxiety and depression. Pharmacol Biochem Behav 86:431–440

    Article  CAS  PubMed  Google Scholar 

  • Hodgson RA, Guthrie DH, Varty GB (2008) Duration of ultrasonic vocalizations in the isolated rat pup as a behavioral measure: sensitivity to anxiolytic and antidepressant drugs. Pharmacol Biochem Behav 88:341–348

    Article  CAS  PubMed  Google Scholar 

  • Hodgson RA, Mullins D, Lu SX, Guzzi M, Zhang X, Bleickardt CJ, Scott JD, Miller MW, Stamford AW, Parker EM, Varty GB (2014) Characterization of a novel vasopressin V1b receptor antagonist, V1B-30N, in animal models of anxiety-like and depression-like behavior. Eur J Pharmacol 730:157–163

    Article  CAS  PubMed  Google Scholar 

  • Hofer MA (1996) Multiple regulators of ultrasonic vocalization in the infant rat. Psychoneuroendocrinology 21:203–217

    Article  CAS  PubMed  Google Scholar 

  • Hofer MA, Shair H (1978) Ultrasonic vocalization during social interaction and isolation in 2-weeek-old rats. Dev Psychobiol 11:495–504

    Article  CAS  PubMed  Google Scholar 

  • Hussy N, Deleuze C, Pantaloni A, Desarmenien MG, Moos F (1997) Agonist action of taurine on glycine receptors in rat supraoptic magnocellular neurones: possible role in osmoregulation. J Physiol 502(Pt 3):609–621

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Iijima M, Chaki S (2005) Separation-induced ultrasonic vocalization in rat pups: further pharmacological characterization. Pharmacol Biochem Behav 82:652–657

    Article  CAS  PubMed  Google Scholar 

  • Iijima M, Yoshimizu T, Shimazaki T, Tokugawa K, Fukumoto K, Kurosu S, Kuwada T, Sekiguchi Y, Chaki S (2014) Antidepressant and anxiolytic profiles of newly synthesized arginine vasopressin V1B receptor antagonists: TASP0233278 and TASP0390325. Br J Pharmacol 171:3511–3525

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Insel TR, Hill JL, Mayor RB (1986) Rat pup ultrasonic isolation calls: possible mediation by the benzodiazepine receptor complex. Pharmacol Biochem Behav 24:1263–1267

    Article  CAS  PubMed  Google Scholar 

  • Kalman BA, Kim PJ, Cole MA, Chi MS, Spencer RL (1997) Diazepam attenuation of restraint stress-induced corticosterone levels is enhanced by prior exposure to repeated restraint. Psychoneuroendocrinology 22:349–360

    Article  CAS  PubMed  Google Scholar 

  • Keck ME (2006) Corticotropin-releasing factor, vasopressin and receptor systems in depression and anxiety. Amino Acids 31:241–250

    Article  CAS  PubMed  Google Scholar 

  • Keck ME, Holsboer F (2001) Hyperactivity of CRH neuronal circuits as a target for therapeutic interventions in affective disorders. Peptides 22:835–844

    Article  CAS  PubMed  Google Scholar 

  • Kehne JH, Boulis NM, Davis M (1991) Effects of the phosphodiesterase inhibitor rolipram on the acoustic startle response in rats. Psychopharmacology 105:27–36

    Article  CAS  PubMed  Google Scholar 

  • Krisch B, Nahke P, Richter D (1986) Immunocytochemical staining of supraoptic neurons from homozygous Brattleboro rats by use of antibodies against two domains of the mutated vasopressin precursor. Cell Tissue Res 244:351–358

    Article  CAS  PubMed  Google Scholar 

  • Landgraf R, Wigger A, Holsboer F, Neumann ID (1999) Hyper-reactive hypothalamo-pituitary-adrenocortical axis in rats bred for high anxiety-related behaviour. J Neuroendocrinol 11:405–407

    Article  CAS  PubMed  Google Scholar 

  • Levine S, Wiener SG (1988) Psychoendocrine aspects of mother-infant relationships in nonhuman primates. Psychoneuroendocrinology 13:143–154

    Article  CAS  PubMed  Google Scholar 

  • Liebsch G, Wotjak CT, Landgraf R, Engelmann M (1996) Septal vasopressin modulates anxiety-related behaviour in rats. Neurosci Lett 217:101–104

    Article  CAS  PubMed  Google Scholar 

  • Lin RE, Ambler L, Billingslea EN, Suh J, Batheja S, Tatard-Leitman V, Featherstone RE, Siegel SJ (2013) Electroencephalographic and early communicative abnormalities in Brattleboro rats. Physiol Rep 1:e00100

    Article  PubMed Central  PubMed  Google Scholar 

  • Macdonald R, Barker JL (1978) Benzodiazepines specifically modulate GABA-mediated postsynaptic inhibition in cultured mammalian neurones. Nature 271:563–564

    Article  CAS  PubMed  Google Scholar 

  • Makara GB, Varga J, Barna I, Pinter O, Klausz B, Zelena D (2012) The vasopressin-deficient Brattleboro rat: lessons for the hypothalamo-pituitary-adrenal axis regulation. Cell Mol Neurobiol 32:759–766

    Article  CAS  PubMed  Google Scholar 

  • McCann SM, Antunes-Rodrigues J, Nallar R, Valtin H (1966) Pituitary-adrenal function in the absence of vasopressin. Endocrinology 79:1058–1064

    Article  CAS  PubMed  Google Scholar 

  • McCormick CM, Kehoe P, Kovacs S (1998) Corticosterone release in response to repeated, short episodes of neonatal isolation: evidence of sensitization. Int J Dev Neurosci 16:175–185

    Article  CAS  PubMed  Google Scholar 

  • Miczek KA, Weerts EM, Vivian JA, Barros HM (1995) Aggression, anxiety and vocalizations in animals: GABAA and 5-HT anxiolytics. Psychopharmacology 121:38–56

    Article  CAS  PubMed  Google Scholar 

  • Mlynarik M, Zelena D, Bagdy G, Makara GB, Jezova D (2007) Signs of attenuated depression-like behavior in vasopressin deficient Brattleboro rats. Horm Behav 51:395–405

    Article  CAS  PubMed  Google Scholar 

  • Muret L, Priou A, Oliver C, Grino M (1992) Stimulation of adrenocorticotropin secretion by insulin-induced hypoglycemia in the developing rat involves arginine vasopressin but not corticotropin-releasing factor. Endocrinology 130:2725–2732

    CAS  PubMed  Google Scholar 

  • Olivier B, Molewijk E, van Oorschot R, van der Heyden J, Ronken E, Mos J (1998) Rat pup ultrasonic vocalization: effects of benzodiazepine receptor ligands. Eur J Pharmacol 358:117–128

    Article  CAS  PubMed  Google Scholar 

  • Petracca FM, Baskin DG, Diaz J, Dorsa DM (1986) Ontogenetic changes in vasopressin binding site distribution in rat brain: an autoradiographic study. Brain Res 393:63–68

    Article  CAS  PubMed  Google Scholar 

  • Pomara N, Willoughby LM, Sidtis JJ, Cooper TB, Greenblatt DJ (2005) Cortisol response to diazepam: its relationship to age, dose, duration of treatment, and presence of generalized anxiety disorder. Psychopharmacology 178:1–8

    Article  CAS  PubMed  Google Scholar 

  • Ramos Ade T, Homem KS, Suchecki D, Tufik S, Troncone LR (2014) Drug-induced suppression of ACTH secretion does not promote anti-depressive or anxiolytic effects. Behav Brain Res 265:69–75

    Article  PubMed  Google Scholar 

  • Sausville E, Carney D, Battey J (1985) The human vasopressin gene is linked to the oxytocin gene and is selectively expressed in a cultured lung cancer cell line. J Biol Chem 260:10236–10241

    CAS  PubMed  Google Scholar 

  • Scattoni ML, McFarlane HG, Zhodzishsky V, Caldwell HK, Young WS, Ricceri L, Crawley JN (2008) Reduced ultrasonic vocalizations in vasopressin 1b knockout mice. Behav Brain Res 187:371–378

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Schmale H, Ivell R, Breindl M, Darmer D, Richter D (1984) The mutant vasopressin gene from diabetes insipidus (Brattleboro) rats is transcribed but the message is not efficiently translated. EMBO J 3:3289–3293

    PubMed Central  CAS  PubMed  Google Scholar 

  • Selye H (1975) Stress and distress. Compr Ther 1:9–13

    CAS  PubMed  Google Scholar 

  • Serradeil-Le Gal C, Wagnon J, Simiand J, Griebel G, Lacour C, Guillon G, Barberis C, Brossard G, Soubrie P, Nisato D, Pascal M, Pruss R, Scatton B, Maffrand JP, Le Fur G (2002) Characterization of (2S,4R)-1-[5-chloro-1-[(2,4-dimethoxyphenyl)sulfonyl]-3-(2-methoxy-phenyl)-2-oxo-2,3-dihydro-1H-indol-3-yl]-4-hydroxy-N, N-dimethyl-2-pyrrolidine carboxamide (SSR149415), a selective and orally active vasopressin V1b receptor antagonist. J Pharmacol Exp Ther 300:1122–1130

    Article  CAS  PubMed  Google Scholar 

  • Serradeil-Le Gal C, Derick S, Brossard G, Manning M, Simiand J, Gaillard R, Griebel G, Guillon G (2003) Functional and pharmacological characterization of the first specific agonist and antagonist for the V1b receptor in mammals. Stress 6:199–206

    Article  CAS  PubMed  Google Scholar 

  • Serradeil-Le Gal C, Wagnon J 3rd, Tonnerre B, Roux R, Garcia G, Griebel G, Aulombard A (2005) An overview of SSR149415, a selective nonpeptide vasopressin V(1b) receptor antagonist for the treatment of stress-related disorders. CNS Drug Rev 11:53–68

    CAS  PubMed  Google Scholar 

  • Shimazaki T, Iijima M, Chaki S (2006) The pituitary mediates the anxiolytic-like effects of the vasopressin V1B receptor antagonist, SSR149415, in a social interaction test in rats. Eur J Pharmacol 543:63–67

    Article  CAS  PubMed  Google Scholar 

  • Sjovall S, Kanto J, Gronroos M, Himberg JJ, Kangas L, Viinamaki O (1983) Antidiuretic hormone concentrations following midazolam premedication. Anaesthesia 38:1217–1220

    Article  CAS  PubMed  Google Scholar 

  • Tanabe K, Kozawa O, Niwa M, Yamomoto T, Matsuno H, Ito H, Kato K, Dohi S, Uematsu T (2001) Contrasting effects of midazolam on induction of heat shock protein 27 by vasopressin and heat in aortic smooth muscle cells. J Cell Biochem 84:39–46

    Article  CAS  PubMed  Google Scholar 

  • Torpy DJ, Grice JE, Hockings GI, Walters MM, Crosbie GV, Jackson RV (1994) Alprazolam attenuates vasopressin-stimulated adrenocorticotropin and cortisol release: evidence for synergy between vasopressin and corticotropin-releasing hormone in humans. J Clin Endocrinol Metab 79:140–144

    CAS  PubMed  Google Scholar 

  • Valtin H, Schroeder HA (1964) Familial hypothalamic diabetes insipidus in rats (Brattleboro Strain). Am J Physiol 206:425–430

    CAS  PubMed  Google Scholar 

  • Vicennati V, Ceroni L, Gagliardi L, Pagotto U, Gambineri A, Genghini S, Pasquali R (2004) Response of the hypothalamic-pituitary-adrenal axis to small dose arginine-vasopressin and daily urinary free cortisol before and after alprazolam pre-treatment differs in obesity. J Endocrinol Invest 27:541–547

    Article  CAS  PubMed  Google Scholar 

  • Welt T, Engelmann M, Renner U, Erhardt A, Muller MB, Landgraf R, Holsboer F, Keck ME (2006) Temazepam triggers the release of vasopressin into the rat hypothalamic paraventricular nucleus: novel insight into benzodiazepine action on hypothalamic-pituitary-adrenocortical system activity during stress. Neuropsychopharmacology 31:2573–2579

    Article  CAS  PubMed  Google Scholar 

  • Wible JH Jr, Zerbe RL, DiMicco JA (1985) Benzodiazepine receptors modulate circulating plasma vasopressin concentration. Brain Res 359:368–370

    Article  CAS  PubMed  Google Scholar 

  • Winslow JT, Insel TR (1991) Endogenous opioids: do they modulate the rat pup’s response to social isolation? Behav Neurosci 105:253–263

    Article  CAS  PubMed  Google Scholar 

  • Winslow JT, Insel TR (1993) Effects of central vasopressin administration to infant rats. Eur J Pharmacol 233:101–107

    Article  CAS  PubMed  Google Scholar 

  • Yagi K, Onaka T (1996) A benzodiazepine, chlordiazepoxide, blocks vasopressin and oxytocin release after footshocks but not osmotic stimulus in the rat. Neurosci Lett 203:49–52

    Article  CAS  PubMed  Google Scholar 

  • Zelena D (2012) Vasopressin in health and disease with a focus on affective disorders. Cent Nerv Syst Agents Med Chem 12:286–303

    Article  CAS  PubMed  Google Scholar 

  • Zelena D, Kiem DT, Barna I, Makara GB (1999) Alpha 2-adrenoreceptor subtypes regulate ACTH and beta-endorphin secretions during stress in the rat. Psychoneuroendocrinology 24:333–343

    Article  CAS  PubMed  Google Scholar 

  • Zelena D, Mergl Z, Foldes A, Kovacs KJ, Toth Z, Makara GB (2003a) Role of hypothalamic inputs in maintaining pituitary-adrenal responsiveness in repeated restraint. Am J Physiol Endocrinol Metab 285:E1110–E1117

    Article  CAS  PubMed  Google Scholar 

  • Zelena D, Mergl Z, Makara GB (2003b) Maternal genotype influences stress reactivity of vasopressin-deficient brattleboro rats. J Neuroendocrinol 15:1105–1110

    Article  CAS  PubMed  Google Scholar 

  • Zelena D, Domokos A, Barna I, Mergl Z, Haller J, Makara GB (2008) Control of the hypothalamo-pituitary-adrenal axis in the neonatal period: adrenocorticotropin and corticosterone stress responses dissociate in vasopressin-deficient brattleboro rats. Endocrinology 149:2576–2583

    Article  CAS  PubMed  Google Scholar 

  • Zelena D, Langnaese K, Domokos A, Pinter O, Landgraf R, Makara GB, Engelmann M (2009a) Vasopressin administration into the paraventricular nucleus normalizes plasma oxytocin and corticosterone levels in Brattleboro rats. Endocrinology 150:2791–2798

    Article  CAS  PubMed  Google Scholar 

  • Zelena D, Mergl Z, Makara GB (2009b) Postnatal development in vasopressin deficient Brattleboro rats with special attention to the hypothalamo-pituitary-adrenal axis function: the role of maternal genotype. Int J Dev Neurosci 27:175–183

    Article  CAS  PubMed  Google Scholar 

  • Zelena D, Barna I, Pinter O, Klausz B, Varga J, Makara GB (2011) Congenital absence of vasopressin and age-dependent changes in ACTH and corticosterone stress responses in rats. Stress 14:420–430

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

Experiments were carried out in accordance with the European Communities Council Directive of 24 November 1986 (86/609/EEC) and were reviewed and approved by the Animal Welfare Committee of the Institute of Experimental Medicine, Budapest, Hungary. The manuscript does not contain clinical studies or patient data. All persons gave their informed consent prior to their inclusion in the study.

Author information

Authors and Affiliations

  1. Institute of Experimental Medicine, Hungarian Academy of Sciences, Budapest, Hungary

    János Varga, Anna Fodor, Barbara Klausz & Dóra Zelena

  2. János Szentágothai School of Neurosciences, Semmelweis University, Budapest, Hungary

    János Varga & Anna Fodor

Authors
  1. János Varga
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Anna Fodor
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Barbara Klausz
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Dóra Zelena
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Dóra Zelena.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Handling Editor: C. T. Wotjak.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Varga, J., Fodor, A., Klausz, B. et al. Anxiogenic role of vasopressin during the early postnatal period: maternal separation-induced ultrasound vocalization in vasopressin-deficient Brattleboro rats. Amino Acids 47, 2409–2418 (2015). https://doi.org/10.1007/s00726-015-2034-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00726-015-2034-x

Keywords

Search

Navigation