Skip to main content
SpringerLink
Log in

Laboratory domestication changed the expression patterns of oxytocin and vasopressin in brains of rats and mice

  • Original Article
  • Published:
Anatomical Science International Aims and scope Submit manuscript

Abstract

The process of domestication is recognized to exert significant effects on the social behaviors of various animal species, including defensive and cognitive behaviors that are closely linked to the expression of oxytocin (OT) and vasopressin (AVP) in selected areas of the brain. However, it is still unclear whether the behavioral changes observed under domestication have resulted in differences in the neurochemical systems that regulate them. In this study, we compared the differences in distribution patterns and regional quantities of OT and/or AVP staining in the forebrains of wild and laboratory strains of rats and mice. Our results indicated that, in the anterior hypothalamus (AH), laboratory strains showed significantly higher densities of OT-ir (immunoreactive) and AVP-ir cells than wild strains, while no significant difference in the densities of those cells in the lateral hypothalamus (LH) was detected between wild and laboratory strains. Laboratory strains showed higher densities of OT-ir and AVP-ir cells than wild strains in the medial preoptic area (MPOA), and differed in almost every MPOA subnucleus. Our results suggest that domestication significantly alters the expression of OT and AVP in related brain areas of laboratory rats and mice, an observation that could explain the identified changes in behavioral patterns.

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.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10

Similar content being viewed by others

References

  • Barnett SA (1963) The rat: a study in behaviour. Aldine, Chicago

    Google Scholar 

  • Bester-Meredith JK, Marler CA (2001) Vasopressin and aggression in cross-fostered California mice (Peromyscus californicus) and white-footed mice (Peromyscus leucopus). Horm Behav 40:51–64

    Article  CAS  PubMed  Google Scholar 

  • Bester-Meredith JK, Marler CA (2003) Vasopressin and the transmission of paternal behavior across generations in mated, cross-fostered Peromyscus mice. Behav Neurosci 117:455–463

  • Bester-Meredith JK, Young LJ, Marler CA (1999) Species differences in paternal behavior and aggression in Peromyscus and their associations with vasopressin immunoreactivity and receptors. Horm Behav 36:25–38

  • Boice R (1972) Some behavioral tests of domestication. Behaviour 42:3–4

    Article  Google Scholar 

  • Boice R (1981) Behavioral comparability of wild and domesticated rats. Behav Genet 11:545–553

    Article  CAS  PubMed  Google Scholar 

  • Brownstein MJ, Russell JT, Gainer H (1980) Synthesis, transport, and release of posterior pituitary hormones. Science 207:373–378

    Article  CAS  PubMed  Google Scholar 

  • Burbach JP, Young LJ, Russell J (2005) Oxytocin: synthesis, secretion, and reproductive functions. In: Neill JD (ed) Knobil and Neill’s physiology of reproduction. Academic, New York, pp 3055–3127

  • Caldwell HK, Albers HE (2004) Effect of photoperiod on vasopressin-induced aggression in Syrian hamsters. Horm Behav 46:444–449

    Article  CAS  PubMed  Google Scholar 

  • Caldwell JD, Moe BD (1999) Conjugated estradiol increases female sexual receptivity in response to oxytocin infused into the medial preoptic area and medial basal hypothalamus. Horm Behav 35:38–46

    Article  CAS  PubMed  Google Scholar 

  • Caldwell JD, Greer ER, Johnson MF, Prange AJ Jr, Pedersen CA (1987) Oxytocin and vasopressin immunoreactivity in hypothalamic and extrahypothalamic sites in late pregnant and postpartum rats. Neuroendocrinology 46:39–47

    Article  CAS  PubMed  Google Scholar 

  • Caldwell JD, Jirikowski GF, Greer ER, Pedersen CA (1989) Medial preoptic area oxytocin and female sexual receptivity. Behav Neurosci 103:655–662

    Article  CAS  PubMed  Google Scholar 

  • Carter CS (2007) Sex differences in oxytocin and vasopressin: implications for autism spectrum disorders? Behav Brain Res 176:170–186

    Article  CAS  PubMed  Google Scholar 

  • Castle WE (1947) The domestication of the rat. Proc Natl Acad Sci USA 33:109–117

  • Chalfin L, Dayan M, Levy DR, Austad SN, Miller RA, Iraqi FA, Dulac C, Kimchi T (2014) Mapping ecologically relevant social behaviours by gene knockout in wild mice. Nat Commun 5:4569

    Article  CAS  PubMed  Google Scholar 

  • Chernigovskaia EV, Glazova MV, Iamova LA, Evteeva SE, Krasnovskaia IA (2001) Catecholamines in the regulation of the functional state of vasopressinergic cells in the rat hypothalamus. Zh Evol Biokhim Fiziol 37:144–149

    CAS  PubMed  Google Scholar 

  • Consiglio AR, Lucion AB (1996) Lesion of hypothalamic paraventricular nucleus and maternal aggressive behavior in female rats. Physiol Behav 59:591–596

    Article  CAS  PubMed  Google Scholar 

  • Da Silva RK, Saad WA, Renzi A, Menani JV, Camargo LA (1995) Effect of lateral hypothalamus lesions on the water and salt intake, and sodium and urine excretion induced by activation of the median preoptic nucleus in conscious rats. J Auton Nerv Syst 53:195–204

    Article  PubMed  Google Scholar 

  • Dantzer R, Koob GF, Bluthe RM, Le Moal M (1988) Septal vasopressin modulates social memory in male rats. Brain Res 457:143–147

    Article  CAS  PubMed  Google Scholar 

  • De Vries GJ, Miller MA (1998) Anatomy and function of extrahypothalamic vasopressin systems in the brain. Prog Brain Res 119:3–20

    Article  PubMed  Google Scholar 

  • De Vries GJ, Panzica GC (2006) Sexual differentiation of central vasopressin and vasotocin systems in vertebrates: different mechanisms, similar endpoints. Neuroscience 138:947–955

    Article  PubMed  Google Scholar 

  • Delgado JM, Anand BK (1953) Increase of food intake induced by electrical stimulation of the lateral hypothalamus. Am J Physiol 172:162–168

    CAS  PubMed  Google Scholar 

  • Edmunds R, West JP (1962) A study of the effect of vasopressin on portal and systemic blood pressure. Surg Gynecol Obstet 114:458–462

    CAS  PubMed  Google Scholar 

  • Edward OP (1984) Behavioral aspects of animal domestication. Quarterly Rev Biol 59:1–32

    Google Scholar 

  • Ferris CF, Delville Y (1994) Vasopressin and serotonin interactions in the control of agonistic behavior. Psychoneuroendocrinology 19:593–601

    Article  CAS  PubMed  Google Scholar 

  • Ferris CF, Potegal M (1988) Vasopressin receptor blockade in the anterior hypothalamus suppresses aggression in hamsters. Physiol Behav 44:235–239

    Article  CAS  PubMed  Google Scholar 

  • Ferris CF, Melloni RH Jr, Koppel G, Perry KW, Fuller RW, Delville Y (1997) Vasopressin/serotonin interactions in the anterior hypothalamus control aggressive behavior in golden hamsters. J Neurosci 17:4331–4340

    CAS  PubMed  Google Scholar 

  • Ferris CF, Stolberg T, Delville Y (1999) Serotonin regulation of aggressive behavior in male golden hamsters (Mesocricetus auratus). Behav Neurosci 113:804–815

    Article  CAS  PubMed  Google Scholar 

  • Frazer KA, Eskin E, Kang HM, Bogue MA, Hinds DA, Beilharz EJ, Gupta RV, Montgomery J, Morenzoni MM, Nilsen GB, Pethiyagoda CL, Stuve LL, Johnson FM, Daly MJ, Wade CM, Cox DR (2007) A sequence-based variation map of 8.27 million SNPs in inbred mouse strains. Nature 448:1050–1053

    Article  CAS  PubMed  Google Scholar 

  • Freeman LC, Currie WB (1985) Variation in the oxytocin content of caprine corpora lutea across the breeding season. Theriogenology 23:481–486

    Article  CAS  PubMed  Google Scholar 

  • Gerlai R (2002) Phenomics: fiction or the future? Trends Neurosci 25:506–509

    Article  PubMed  Google Scholar 

  • Giuliano F, Rampin O, Brown K, Courtois F, Benoit G, Jardin A (1996) Stimulation of the medial preoptic area of the hypothalamus in the rat elicits increases in intracavernous pressure. Neurosci Lett 209:1–4

    Article  CAS  PubMed  Google Scholar 

  • Gobrogge KL, Liu Y, Young LJ, Wang Z (2009) Anterior hypothalamic vasopressin regulates pair-bonding and drug-induced aggression in a monogamous rodent. Proc Natl Acad Sci USA 106:19144–19149

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gray P, Brooks PJ (1984) Effect of lesion location within the medial preoptic-anterior hypothalamic continuum on maternal and male sexual behaviors in female rats. Behav Neurosci 98:703–711

    Article  CAS  PubMed  Google Scholar 

  • Harker KTWI (2002) Place and matching-to-place spatial learning affected by rat inbreeding (Dark–Agouti, Fischer 344) and albinism (Wistar, Sprague–Dawley) but not domestication (wild rat vs. Long–Evans, Fischer–Norway). Behav Brain Res 134:467–477

  • Hennessey AC, Huhman KL, Albers HE (1994) Vasopressin and sex differences in hamster flank marking. Physiol Behav 55:905–911

    Article  CAS  PubMed  Google Scholar 

  • Holmes A, Wrenn CC, Harris AP, Thayer KE, Crawley JN (2002) Behavioral profiles of inbred strains on novel olfactory, spatial and emotional tests for reference memory in mice. Genes Brain Behav 1:55–69

    Article  CAS  PubMed  Google Scholar 

  • Huck UW, Price EO (1975) Differential effects of environmental enrichment on the open-field behavior of wild and domestic Norway rats. J Comp Physiol Psychol 89:892–898

    Article  CAS  PubMed  Google Scholar 

  • Insel TR, Shapiro LE (1992) Oxytocin receptor distribution reflects social organization in monogamous and polygamous voles. Proc Natl Acad Sci USA 89:5981–5985

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Insel TR, Wang ZX, Ferris CF (1994) Patterns of brain vasopressin receptor distribution associated with social organization in microtine rodents. J Neurosci 14:5381–5392

    CAS  PubMed  Google Scholar 

  • Jing M, Yu HT, Bi X, Lai YC, Jiang W, Huang L (2014) Phylogeography of Chinese house mice (Mus musculus musculus/castaneus): distribution, routes of colonization and geographic regions of hybridization. Mol Ecol 23:4387–4405

    Article  PubMed  Google Scholar 

  • Kruska D (1975) Comparative quantitative study on brains of wild and laboratory rats. I. Comparison of volume of total brain and classical brain parts. J Hirnforsch 16:469–483

    CAS  PubMed  Google Scholar 

  • Le Roy I, Roubertoux PL, Jamot L, Maarouf F, Tordjman S, Mortaud S, Blanchard C, Martin B, Guillot PV, Duquenne V (1998) Neuronal and behavioral differences between Mus musculus domesticus (C57BL/6JBy) and Mus musculus castaneus (CAST/Ei). Behav Brain Res 95:135–142

    Article  PubMed  Google Scholar 

  • Leon VA, Fraschina J, Guidobono JS, Busch M (2013) Habitat use and demography of Mus musculus in a rural landscape of Argentina. Integrative Zoology 8:18–29

    Article  PubMed  Google Scholar 

  • Lindvall O, Bjorklund A, Skagerberg G (1984) Selective histochemical demonstration of dopamine terminal systems in rat di- and telencephalon: new evidence for dopaminergic innervation of hypothalamic neurosecretory nuclei. Brain Res 306:19–30

    Article  CAS  PubMed  Google Scholar 

  • Liu Y, Curtis JT, Wang Z (2001) Vasopressin in the lateral septum regulates pair bond formation in male prairie voles (Microtus ochrogaster). Behav Neurosci 115:910–919

    Article  CAS  PubMed  Google Scholar 

  • McGinnis MY, Montana RC, Lumia AR (2002) Effects of hydroxyflutamide in the medial preoptic area or lateral septum on reproductive behaviors in male rats. Brain Res Bull 59:227–234

    Article  CAS  PubMed  Google Scholar 

  • Michael VS (1983) Morphology of vasopressin and oxytocin neurones and their central and vascular projections. Prog Brain Res 60:101–114

    Article  Google Scholar 

  • Moos F, Richard P (1982) Excitatory effect of dopamine on oxytocin and vasopressin reflex releases in the rat. Brain Res 241:249–260

    Article  CAS  PubMed  Google Scholar 

  • Ness RW, Zhang YH, Cong L, Wang Y, Zhang JX, Keightley PD (2012) Nuclear gene variation in wild brown rats. G3 (Bethesda) 2:1661–1664

  • Nielsen S, Chou CL, Marples D, Christensen EI, Kishore BK, Knepper MA (1995) Vasopressin increases water permeability of kidney collecting duct by inducing translocation of aquaporin-CD water channels to plasma membrane. Proc Natl Acad Sci USA 92:1013–1017

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Parker KJ, Phillips KM, Kinney LF, Lee TM (2001) Day length and sociosexual cohabitation alter central oxytocin receptor binding in female meadow voles (Microtus pennsylvanicus). Behav Neurosci 115:1349–1356

    Article  CAS  PubMed  Google Scholar 

  • Pedersen CA, Caldwell JD, Walker C, Ayers G, Mason GA (1994) Oxytocin activates the postpartum onset of rat maternal behavior in the ventral tegmental and medial preoptic areas. Behav Neurosci 108:1163–1171

    Article  CAS  PubMed  Google Scholar 

  • Popik P, Van Ree JM (1991) Oxytocin but not vasopressin facilitates social recognition following injection into the medial preoptic area of the rat brain. Eur Neuropsychopharmacol 1:555–560

    Article  CAS  PubMed  Google Scholar 

  • Popik P, Vos PE, Van Ree JM (1992) Neurohypophyseal hormone receptors in the septum are implicated in social recognition in the rat. Behav Pharmacol 3:351–358

    Article  CAS  PubMed  Google Scholar 

  • Reuss S, Hermes B, Fuchs E, Hiemke C (1999) Day- and night-time contents of monoamines and their metabolites in the medial preoptic area of the rat hypothalamus. Neurosci Lett 266:29–32

    Article  CAS  PubMed  Google Scholar 

  • Riters LV, Panksepp J (1997) Effects of vasotocin on aggressive behavior in male Japanese quail. Ann N Y Acad Sci 807:478–480

    Article  CAS  PubMed  Google Scholar 

  • Rosen GJ, de Vries GJ, Goldman SL, Goldman BD, Forger NG (2008) Distribution of oxytocin in the brain of a eusocial rodent. Neuroscience 155:809–817

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Waldherr M, Neumann ID (2007) Centrally released oxytocin mediates mating-induced anxiolysis in male rats. Proc Natl Acad Sci USA 104:16681–16684

  • Wang Z (1995) Species differences in the vasopressin-immunoreactive pathways in the bed nucleus of the stria terminalis and medial amygdaloid nucleus in prairie voles (Microtus ochrogaster) and meadow voles (Microtus pennsylvanicus). Behav Neurosci 109:305–311

    Article  CAS  PubMed  Google Scholar 

  • Wang Z, Zhou L, Hulihan TJ, Insel TR (1996) Immunoreactivity of central vasopressin and oxytocin pathways in microtine rodents: a quantitative comparative study. J Comp Neurol 366:726–737

    Article  CAS  PubMed  Google Scholar 

  • Wang Z, Liu Y, Young LJ, Insel TR (1997) Developmental changes in forebrain vasopressin receptor binding in prairie voles (Microtus ochrogaster) and montane voles (Microtus montanus). Ann N Y Acad Sci 807:510–513

    Article  CAS  PubMed  Google Scholar 

  • Wang Y, Xu L, Pan Y, Wang Z, Zhang Z (2013) Species differences in the immunoreactive expression of oxytocin, vasopressin, tyrosine hydroxylase and estrogen receptor alpha in the brain of Mongolian gerbils (Meriones unguiculatus) and Chinese striped hamsters (Cricetulus barabensis). PLoS One 8:e65807

  • Weitzman RE, Kleeman CR (1979) The clinical physiology of water metabolism. Part I: the physiologic regulation of arginine vasopressin secretion and thirst. West J Med 131:373–400

    CAS  PubMed  PubMed Central  Google Scholar 

  • Winslow JT, Hastings N, Carter CS, Harbaugh CR, Insel TR (1993) A role for central vasopressin in pair bonding in monogamous prairie voles. Nature 365:545–548

    Article  CAS  PubMed  Google Scholar 

  • Xu L, Pan Y, Young KA, Wang Z, Zhang Z (2010) Oxytocin and vasopressin immunoreactive staining in the brains of Brandt’s voles (Lasiopodomys brandtii) and greater long-tailed hamsters (Tscherskia triton). Neuroscience 169:1235–1247

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Young KA, Liu Y, Wang Z (2008) The neurobiology of social attachment: a comparative approach to behavioral, neuroanatomical, and neurochemical studies. Comp Biochem Physiol C 148:401–410

Download references

Acknowledgments

The authors would like to thank Drs. Linxi Xu and Yongliang Pan for their help with the experimental studies, and they express their gratitude to Dr. Dawei Wang for his help in the field trapping of animals, Prof. Zuoxin Wang for his help in improving the manuscript, and Dr. Sarita Maree (Department of Genetics, University of Pretoria, South Africa) for her help in improving the paper and polishing the English. This paper is partially supported by the Strategic Priority Research Program of the Chinese Academy of Sciences (grant no. XDB11050300), a grant from the State Key Laboratory of Integrated Management on Pest Insects and Rodents (grant no. Chinese IPM1204), and The Science and Technology Service (STS) project of the Chinese Academy of Sciences (KFJ-EW-STS-068-3).

Author information

Authors and Affiliations

  1. State Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Sciences, 1 Beichen West Road, Chaoyang District, Beijing, 100101, People’s Republic of China

    Chao Ruan & Zhibin Zhang

  2. University of Chinese Academy of Sciences, Beijing, People’s Republic of China

    Chao Ruan

Authors
  1. Chao Ruan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Zhibin Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Zhibin Zhang.

Ethics declarations

Conflict of interest

The authors declare no conflict of interest.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 92 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ruan, C., Zhang, Z. Laboratory domestication changed the expression patterns of oxytocin and vasopressin in brains of rats and mice. Anat Sci Int 91, 358–370 (2016). https://doi.org/10.1007/s12565-015-0311-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12565-015-0311-0

Keywords

Search

Navigation