Top

Published in:

01-09-2016 | Original Article

Distribution of oxytocin and co-localization with arginine vasopressin in the brain of mice

Authors: Marcos Otero-García, Carmen Agustín-Pavón, Enrique Lanuza, Fernando Martínez-García

Published in: Brain Structure and Function | Issue 7/2016

Abstract

Oxytocin (OT) and vasopressin (AVP) play a major role in social behaviours. Mice have become the species of choice for neurobiology of social behaviour due to identification of mouse pheromones and the advantage of genetically modified mice. However, neuroanatomical data on nonapeptidergic systems in mice are fragmentary, especially concerning the central distribution of OT. Therefore, we analyse the immunoreactivity for OT and its neurophysin in the brain of male and female mice (strain CD1). Further, we combine immunofluorescent detection of OT and AVP to locate cells co-expressing both peptides and their putative axonal processes. The results indicate that OT is present in cells of the neurosecretory paraventricular (Pa) and supraoptic hypothalamic nuclei (SON). From the anterior SON, OTergic cells extend into the medial amygdala, where a sparse cell population occupies its ventral anterior and posterior divisions. Co-expression of OT and AVP in these nuclei is rare. Moreover, a remarkable OTergic cell group is found near the ventral bed nucleus of the stria terminalis (BST), distributed between the anterodorsal preoptic nucleus and the nucleus of anterior commissure (ADP/AC). This cell group, the rostral edge of the Pa and the periventricular hypothalamus display frequent OT + AVP double labelling, with a general dominance of OT over AVP immunoreactivity. Fibres with similar immunoreactivity profile innervate the accumbens shell and core, central amygdala and portions of the intervening BST. These data, together with data in the literature on rats, suggest that the projections of ADP/AC nonapeptidergic cells onto these brain centres could promote pup-motivated behaviours and inhibit pup avoidance during motherhood.

Banczerowski P et al (2003) Lesion of the amygdala on the right and left side suppresses testosterone secretion but only left-sided intervention decreases serum luteinizing hormone level. J Endocrinol Invest 26(5):429–434PubMedCrossRef

Beery AK, Lacey EA, Francis DD (2008) Oxytocin and vasopressin receptor distributions in a solitary and a social species of tuco-tuco (Ctenomys haigi and Ctenomys sociabilis). J Comp Neurol 507(6):1847–1859PubMedCrossRef

Belenky M et al (1992) Ultrastructural immunolocalization of rat oxytocin-neurophysin in transgenic mice expressing the rat oxytocin gene. Brain Res 583(1–2):279–286PubMedCrossRef

Ben-Barak Y et al (1985) Neurophysin in the hypothalamo-neurohypophysial system. I. Production and characterization of monoclonal antibodies. J Neurosci 5(1):81–97PubMed

Bielsky IF et al (2005) The V1a vasopressin receptor is necessary and sufficient for normal social recognition: a gene replacement study. Neuron 47(4):503–513PubMedCrossRef

Bosch OJ (2011) Maternal nurturing is dependent on her innate anxiety: the behavioral roles of brain oxytocin and vasopressin. Horm Behav 59(2):202–212PubMedCrossRef

Breiter HC et al (1996) Response and habituation of the human amygdala during visual processing of facial expression. Neuron 17(5):875–887PubMedCrossRef

Buijs RM (1978) Intra- and extrahypothalamic vasopressin and oxytocin pathways in the rat. Pathways to the limbic system, medulla oblongata and spinal cord. Cell Tissue Res 192(3):423–435PubMedCrossRef

Buijs RM et al (1978) Intra- and extrahypothalamic vasopressin and oxytocin pathways in the rat. Cell Tissue Res 186:423–433PubMedCrossRef

Butovsky E et al (2006) Chronic exposure to ∆9-tetrahydrocannabinol downregulates oxytocin and oxytocin-associated neurophysin in specific brain areas. Mol Cell Neurosci 31(4):795–804PubMedCrossRef

Bychowski ME, Mena JD, Auger CJ (2013) Vasopressin infusion into the lateral septum of adult male rats rescues progesterone-induced impairment in social recognition. Neuroscience 246:52–58PubMedCrossRef

Cádiz-Moretti B, Martínez-García F, Lanuza E (2013) Neural substrate to associate odorants and pheromones: convergence of projections from the main and accessory olfactory bulbs in mice. In: East ML, Dehnhard M (eds) Chemical signals in vertebrates 12. Springer, New York, pp 269–275. doi:10.1007/978-1-4614-5927-9

Caffé AR et al (1989) Vasopressin and oxytocin systems in the brain and upper spinal cord of Macaca fascicularis. J Comp Neurol 287(3):302–325PubMedCrossRef

Caldwell H, Young 3rd WS (2006) Oxytocin and vasopressin: genetics and behavioral implications. Handbook of neurochemistry and molecular neurobiology, pp 573–607. doi:10.1007/978-0-387-30381-9_25

Caldwell HK, Wersinger SR, Young WS 3rd (2008) The role of the vasopressin 1b receptor in aggression and other social behaviours. Prog Brain Res 170:65–72PubMedCrossRef

Campbell P, Ophir AG, Phelps SM (2009) Central vasopressin and oxytocin receptor distributions in two species of singing mice. J Comp Neurol 516(4):321–333PubMedCrossRef

Carter CS et al (2008) Oxytocin, vasopressin and sociality. Prog Brain Res 170:331–336PubMedCrossRef

Castel M, Morris JF (1988) The neurophysin-containing innervation of the forebrain of the mouse. Neuroscience 24(3):937–966PubMedCrossRef

Caughey SD et al (2011) Changes in the intensity of maternal aggression and central oxytocin and vasopressin V1a receptors across the peripartum period in the rat. J Neuroendocrinol 23(11):1113–1124PubMedCrossRef

Chamero P et al (2007) Identification of protein pheromones that promote aggressive behaviour. Nature 450(7171):899–902PubMedCrossRef

Choleris E, Pfaff DW, Kavaliers M (2013) Oxytocin, vasopressin and related peptides in the regulation of behavior. In: Oxytocin, vasopressin and related peptides in the regulation of behavior. pp 379–381. http://ebooks.cambridge.org/ref/id/CBO9781139017855

Condés-Lara M et al (2007) Branched oxytocinergic innervations from the paraventricular hypothalamic nuclei to superficial layers in the spinal cord. Brain Res 1160(1):20–29PubMedCrossRef

DeVries GJ et al (1985) The vasopressinergic innervation of the brain in normal and castrated rats. J Comp Neurol 233(2):236–254PubMedCrossRef

Dölen G et al (2013) Social reward requires coordinated activity of nucleus accumbens oxytocin and serotonin. Nature 501(7466):179–84. http://www.ncbi.nlm.nih.gov/pubmed/24025838

Donaldson ZR, Young LJ (2008) Oxytocin, vasopressin, and the neurogenetics of sociality. Science 322(5903):900–904PubMedCrossRef

Dong HW, Swanson LW (2006) Projections from bed nuclei of the stria terminalis, dorsomedial nucleus: implications for cerebral hemisphere integration of neuroendocrine, autonomic, and drinking responses. J Comp Neurol 494(1):75–107PubMedPubMedCentralCrossRef

Dubois-Dauphin M, Barberis C, De Bilbao F (1996) Vasopressin receptors in the mouse (Mus musculus) brain: sex-related expression in the medial preoptic area and hypothalamus. Brain Res 743(1–2):32–39PubMedCrossRef

Eaton JL et al (2012) Organizational effects of oxytocin on serotonin innervation. Dev Psychobiol 54(1):92–97PubMedCrossRef

Egashira N et al (2007) Impaired social interaction and reduced anxiety-related behavior in vasopressin V1a receptor knockout mice. Behav Brain Res 178(1):123–127PubMedCrossRef

Evans DW et al. (2014) Social cognition and brain morphology: implications for developmental brain dysfunction. Brain Imaging Behav

Feldman R et al (2010) Natural variations in maternal and paternal care are associated with systematic changes in oxytocin following parent-infant contact. Psychoneuroendocrinology 35(8):1133–1141. doi:10.1016/j.psyneuen.2010.01.013 PubMedCrossRef

Garcia-Moreno F et al (2010) A neuronal migratory pathway crossing from diencephalon to telencephalon populates amygdala nuclei. Nat Neurosci 13(6):680–689PubMedCrossRef

Glasgow E et al (1999) Single cell reverse transcription-polymerase chain reaction analysis of rat supraoptic magnocellular neurons: neuropeptide phenotypes and high voltage-gated calcium channel subtypes. Endocrinology 140(11):5391–5401PubMedCrossRef

Gregory R et al (2015) Oxytocin increases VTA activation to infant and sexual stimuli in nulliparous and postpartum women. Horm Behav 69:82–88PubMedPubMedCentralCrossRef

Hammock EAD, Levitt P (2013) Oxytocin receptor ligand binding in embryonic tissue and postnatal brain development of the C57BL/6J mouse. Front Behav Neurosci 7:195. doi:10.3389/fnbeh.2013.00195 PubMedPubMedCentralCrossRef

Hatton GI, Cobbett P, Salm AK (1985) Extranuclear axon collaterals of paraventricular neurons in the rat hypothalamus: intracellular staining, immunocytochemistry and electrophysiology. Brain Res Bull 14(2):123–132PubMedCrossRef

Hawthorn J, Ang VT, Jenkins JS (1985) Effects of lesions in the hypothalamic paraventricular, supraoptic and suprachiasmatic nuclei on vasopressin and oxytocin in rat brain and spinal cord. Brain Res 346(1):51–57PubMedCrossRef

Hermes MLHJ et al (1988) Oxytocinergic innervation of the brain of the garden dormouse (Eliomys quercinus L.). J Comp Neurol 273:252–262PubMedCrossRef

Honda K, Higuchi T (2010a) Effects of unilateral electrolytic lesion of the dorsomedial nucleus of the hypothalamus on milk-ejection reflex in the rat. J Reprod Dev 56(1):98–102PubMedCrossRef

Honda K, Higuchi T (2010b) Electrical activities of neurones in the dorsomedial hypothalamic nucleus projecting to the supraoptic nucleus during milk-ejection reflex in the rat. J Reprod Dev 56(3):336–340PubMedCrossRef

Hou-Yu A et al (1986) Comparative distribution of vasopressin and oxytocin neurons in the rat brain using a double-label procedure. Neuroendocrinology 44(2):235–246PubMedCrossRef

Huber D, Veinante P, Stoop R (2005) Vasopressin and oxytocin excite distinct neuronal populations in the central amygdala. Science 308(5719):245–248PubMedCrossRef

Insel TR, Harbaugh CR (1989) Lesions of the hypothalamic paraventricular nucleus disrupt the initiation of maternal behavior. Physiol Behav 45(5):1033–1041PubMedCrossRef

Insel TR et al (1993) Gonadal steroids have paradoxical effects on brain oxytocin receptors. J Neuroendocrinol 5(6):619–628PubMedCrossRef

Isogai Y et al (2011) Molecular organization of vomeronasal chemoreception. Nature 478(7368):241–245PubMedPubMedCentralCrossRef

Jin D et al (2007) CD38 is critical for social behaviour by regulating oxytocin secretion. Nature 446(7131):41–45PubMedCrossRef

Jirikowski GF, Ramalho-Ortigao FJ, Caldwell JD (1991) Transitory coexistence of oxytocin and vasopressin in the hypothalamo neurohypophysial system of parturient rats. Hormone and metabolic research = Hormon- und Stoffwechselforschung = Hormones et metabolisme 23(10):476–480

Kang N, Baum MJ, Cherry JA (2009) A direct main olfactory bulb projection to the “vomeronasal” amygdala in female mice selectively responds to volatile pheromones from males. Eur J Neurosci 29(3):624–634PubMedPubMedCentralCrossRef

Kiyama H, Emson PC (1990) Evidence for the co-expression of oxytocin and vasopressin messenger ribonucleic acids in magnocellular neurosecretory cells: simultaneous demonstration of two neurohypophysin messenger ribonucleic acids by hybridization histochemistry. J Neuroendocrinol 2(3):257–259PubMedCrossRef

Knobloch HS et al (2012) Evoked axonal oxytocin release in the central amygdala attenuates fear response. Neuron 73(3):553–566. doi:10.1016/j.neuron.2011.11.030 PubMedCrossRef

Krisch B (1976) Immunohistochemical and electron microscopic study of the rat hypothalamic nuclei and cell clusters under various experimental conditions. Possible sites of hormone release. Cell Tissue Res 174(1):109–127PubMedCrossRef

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(3–4):150–176PubMedCrossRef

Lim MM, Murphy AZ, Young LJ (2004) Ventral striatopallidal oxytocin and vasopressin v1a receptors in the monogamous prairie vole (Microtus ochrogaster). J Comp Neurol 468(4):555–570PubMedCrossRef

Liu H et al (1994) Synaptic relationship between substance P and the substance P receptor: light and electron microscopic characterization of the mismatch between neuropeptides and their receptors. Proc Natl Acad Sci USA 91(3):1009–1013PubMedPubMedCentralCrossRef

Ludwig M, Leng G (2006) Dendritic peptide release and peptide-dependent behaviours. Nat Rev Neurosci 7(2):126–136PubMedCrossRef

Lukas M et al (2013) Oxytocin mediates rodent social memory within the lateral septum and the medial amygdala depending on the relevance of the social stimulus: male juvenile versus female adult conspecifics. Psychoneuroendocrinology 38(6):916–926PubMedCrossRef

Manning M et al (2012) Oxytocin and vasopressin agonists and antagonists as research tools and potential therapeutics. J Neuroendocrinol 24(4):609–628PubMedPubMedCentralCrossRef

Markowitsch HJ (1998) Differential contribution of right and left amygdala to affective information processing. Behav Neurol 11(4):233–244. http://www.ncbi.nlm.nih.gov/pubmed/11568425

Martínez-García F et al (2012) Chapter 6—piriform cortex and amygdala. In: GP Charles Watson, George Paxinos, Luis Puelles, Charles Watson, L Puelles (eds) The mouse nervous system, pp 140–172. Academic Press, San Diego. http://www.sciencedirect.com/science/article/pii/B9780123694973100068

Mottolese R et al (2014) Switching brain serotonin with oxytocin. Proceedings of the National Academy of Sciences of the United States of America, vol 111, issue 23, pp 8637–42. http://www.ncbi.nlm.nih.gov/pubmed/24912179

Melis MR et al (2007) Oxytocin injected into the ventral tegmental area induces penile erection and increases extracellular dopamine in the nucleus accumbens and paraventricular nucleus of the hypothalamus of male rats. Eur J Neurosci 26(4):1026–1035PubMedCrossRef

Merighi A et al (1989) Ultrastructural localization of neuropeptides and GABA in rat dorsal horn: a comparison of different immunogold labeling techniques. J Histochem Cytochem 37(4):529–540PubMedCrossRef

Meyer-Lindenberg A et al (2011) Oxytocin and vasopressin in the human brain: social neuropeptides for translational medicine. Nat Rev Neurosci 12(9):524–538PubMedCrossRef

Mezey E, Kiss JZ (1991) Coexpression of vasopressin and oxytocin in hypothalamic supraoptic neurons of lactating rats. Endocrinology 129(4):1814–1820PubMedCrossRef

Mohr E et al (1988) Expression of the vasopressin and oxytocin genes in rats occurs in mutually exclusive sets of hypothalamic neurons. FEBS Lett 242(1):144–148PubMedCrossRef

Muchlinski AE, Johnson DJ, Anderson DG (1988) Electron microscope study of the association between hypothalamic blood vessels and oxytocin-like immunoreactive neurons. Brain Res Bull 20(2):267–271PubMedCrossRef

Mullis K, Kay K, Williams DL (2013) Oxytocin action in the ventral tegmental area affects sucrose intake. Brain Res 1513:85–91PubMedPubMedCentralCrossRef

Nephew BC, Bridges RS (2008) Central actions of arginine vasopressin and a V1a receptor antagonist on maternal aggression, maternal behavior, and grooming in lactating rats. Pharmacol Biochem Behav 91(1):77–83PubMedPubMedCentralCrossRef

Neumann ID, Landgraf R (2012) Balance of brain oxytocin and vasopressin: Implications for anxiety, depression, and social behaviors. Trends Neurosci 35(11):649–659. http://dx.doi.org/10.1016/j.tins.2012.08.004

Newman SW (1999) The medial extended amygdala in male reproductive behavior. A node in the mammalian social behavior network. Ann N Y Acad Sci 877:242–257PubMedCrossRef

Ni RJ et al (2014) Distribution of vasopressin, oxytocin and vasoactive intestinal polypeptide in the hypothalamus and extrahypothalamic regions of tree shrews. Neuroscience 265:124–136PubMedCrossRef

Nishimori K et al (2008) New aspects of oxytocin receptor function revealed by knockout mice: sociosexual behaviour and control of energy balance. Prog Brain Res 170:79–90PubMedCrossRef

Nodari F et al (2008) Sulfated steroids as natural ligands of mouse pheromone-sensing neurons. J Neurosci 28(25):6407–6418PubMedPubMedCentralCrossRef

Numan M, Numan M (1996) A lesion and neuroanatomical tract-tracing analysis of the role of the bed nucleus of the stria terminalis in retrieval behavior and other aspects of maternal responsiveness in rats. Dev Psychobiol 29(1):23–51PubMedCrossRef

Numan M, Woodside B (2010) Maternity: neural mechanisms, motivational processes, and physiological adaptations. Behav Neurosci 124(6):715–741PubMedCrossRef

Numan M et al (1988) Axon-sparing lesions of the preoptic region and substantia innominata disrupt maternal behavior in rats. Behav Neurosci 102(3):381–396PubMedCrossRef

Olazábal DE, Young LJ (2006) Oxytocin receptors in the nucleus accumbens facilitate “spontaneous” maternal behavior in adult female prairie voles. Neuroscience 141(2):559–568PubMedCrossRef

Olazabal DE et al (2002) MPOA cytotoxic lesions and maternal behavior in the rat: effects of midpubertal lesions on maternal behavior and the role of ovarian hormones in maturation of MPOA control of maternal behavior. Horm Behav 41(2):126–138PubMedCrossRef

Olucha-Bordonau FE et al (2014) Amygdala: structure and function. In: Paxinos G (ed) The rat nervous system. Academic Press, London, pp 441–490

Otero-Garcia M et al (2014) Extending the socio-sexual brain: arginine-vasopressin immunoreactive circuits in the telencephalon of mice. Brain Struct Funct 219(3):1055–1081PubMedCrossRef

Pagani JH et al (2015) Raphe serotonin neuron-specific oxytocin receptor knockout reduces aggression without affecting anxiety-like behavior in male mice only. Genes Brain Behav 14(2):167–176PubMedPubMedCentralCrossRef

Paxinos G, Franklin KBJ (2001) The mouse brain in stereotaxic coordinates. Academic Press, San Diego

Pedersen CA (1997) Oxytocin control of maternal behavior. Regulation by sex steroids and offspring stimuli. Ann N Y Acad Sci 807:126–145PubMedCrossRef

Pedersen CA et al (1994) Oxytocin activates the postpartum onset of rat maternal behavior in the ventral tegmental and medial preoptic areas. Behav Neurosci 108(6):1163–1171PubMedCrossRef

Pobbe RLH et al (2012) Oxytocin receptor knockout mice display deficits in the expression of autism-related behaviors. Horm Behav 61(3):436–444. doi:10.1016/j.yhbeh.2011.10.010 PubMedCrossRef

Rhodes CH, Morrell JI, Pfaff DW (1981) Immunohistochemical analysis of magnocellular elements in rat hypothalamus: distribution and numbers of cells containing neurophysin, oxytocin, and vasopressin. J Comp Neurol 198(1):45–64PubMedCrossRef

Roberts SA et al (2010) Darcin: a male pheromone that stimulates female memory and sexual attraction to an individual male’s odour. BMC Biol 8:75PubMedPubMedCentralCrossRef

Rood BD, De Vries GJ (2011) Vasopressin innervation of the mouse (Mus musculus) brain and spinal cord. J Comp Neurol 519(12):2434–2474PubMedPubMedCentralCrossRef

Rood BD et al (2013) Site of origin of and sex differences in the vasopressin innervation of the mouse (Mus musculus) brain. J Comp Neurol 521(10):2321–2358PubMedCrossRef

Rosen GJ et al (2008) Distribution of oxytocin in the brain of a eusocial rodent. Neuroscience 155(3):809–817PubMedPubMedCentralCrossRef

Ross HE et al (2009) Characterization of the oxytocin system regulating affiliative behavior in female prairie voles. Neuroscience 162(4):892–903. doi:10.1016/j.neuroscience.2009.05.055 PubMedPubMedCentralCrossRef

Sabatier N, Shibuya I, Dayanithi G (2004) Intracellular calcium increase and somatodendritic vasopressin release by vasopressin receptor agonists in the rat supraoptic nucleus: involvement of multiple intracellular transduction signals. J Neuroendocrinol 16(3):221–236PubMedCrossRef

Sanchez MA, Dominguez R (1995) Differential-effects of unilateral lesions in the medial amygdala on spontaneous and induced ovulation. Brain Res Bull 38(4):313–317. <Go to ISI>://A1995RV80800002

Sarnyai Z, Kovács GL (1994) Role of oxytocin in the neuroadaptation to drugs of abuse. Psychoneuroendocrinology 19(1):85–117PubMedCrossRef

Shahrokh DK et al (2010) Oxytocin-dopamine interactions mediate variations in maternal behavior in the rat. Endocrinology 151(5):2276–2286PubMedPubMedCentralCrossRef

Shipley MT, Adamek GD (1984) The connections of the mouse olfactory bulb: a study using orthograde and retrograde transport of wheat germ agglutinin conjugated to horseradish peroxidase. Brain Res Bull 12:669–688PubMedCrossRef

Staes N et al (2014) Oxytocin and vasopressin receptor gene variation as a proximate base for inter- and intraspecific behavioral differences in bonobos and chimpanzees. Plos One 9(11):e113364. doi:10.1371/journal.pone.0113364 PubMedPubMedCentralCrossRef

Stoop R (2012) Neuromodulation by oxytocin and vasopressin. Neuron 76(1):142–159. doi:10.1016/j.neuron.2012.09.025 PubMedCrossRef

Succu S et al (2008) Oxytocin induces penile erection when injected into the ventral tegmental area of male rats: role of nitric oxide and cyclic GMP. Eur J Neurosci 28(4):813–821. http://www.ncbi.nlm.nih.gov/pubmed/18671741

Swanson LW, Kuypers HG (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. J Comp Neurol 194(3):555–570PubMedCrossRef

Takahashi A, Miczek KA (2013) Neurogenetics of aggressive behavior: studies in rodents. Curr Top Behav Neurosci 17:3–44CrossRef

Takano S et al (1992) Lesion and electrophysiological studies on the hypothalamic afferent pathway of the milk ejection reflex in the rat. Neuroscience 50(4):877–883PubMedCrossRef

Tang Y et al (2014) Oxytocin activation of neurons in ventral tegmental area and interfascicular nucleus of mouse midbrain. Neuropharmacology 77:277–284CrossRefPubMed

Telleria-Diaz A, Grinevich VV, Jirikowski GF (2001) Colocalization of vasopressin and oxytocin in hypothalamic magnocellular neurons in water-deprived rats. Neuropeptides 35(3–4):162–167PubMedCrossRef

Tobin V, Leng G, Ludwig M (2012) The involvement of actin, calcium channels and exocytosis proteins in somato-dendritic oxytocin and vasopressin release. Front Physiol 3:261. doi:10.3389/fphys.2012.00261 PubMedPubMedCentralCrossRef

Toth I, Neumann ID (2013) Animal models of social avoidance and social fear. Cell Tissue Res 354(1):107–118PubMedCrossRef

Trueta C, De-Miguel FF (2012) Extrasynaptic exocytosis and its mechanisms: a source of molecules mediating volume transmission in the nervous system. Front Physiol 3:319. doi:10.3389/fphys.2012.00319 PubMedPubMedCentral

Tsuneoka Y, Maruyama T, Yoshida S, Nishimori K, Kato T, Numan M, Kuroda KO (2013) Functional, anatomical, and neurochemical differentiation of medial preoptic area subregions in relation to maternal behavior in the mouse. J Comp Neurol 521(7):1633–1663PubMedCrossRef

Valesky EM et al (2012) Distribution of oxytocin- and vasopressin-immunoreactive neurons in the brain of the eusocial mole rat (Fukomys anselli). Anat Rec 295(3):474–480CrossRef

Veenema AH, Neumann ID (2008) Central vasopressin and oxytocin release: regulation of complex social behaviours. Prog Brain Res 170:261–276PubMedCrossRef

Veinante P, Freund-Mercier MJ (1997) Distribution of oxytocin- and vasopressin-binding sites in the rat extended amygdala: a histoautoradiographic study. J Comp Neurol 383(3):305–325PubMedCrossRef

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(2):432–449PubMedCrossRef

Wang Z et al (1996) Immunoreactivity of central vasopressin and oxytocin pathways in microtine rodents: a quantitative comparative study. J Comp Neurol 366(4):726–737PubMedCrossRef

Whitnall MH et al (1985) Neurophysin in the hypothalamo-neurohypophysial system. II. Immunocytochemical studies of the ontogeny of oxytocinergic and vasopressinergic neurons. J Neurosci 5(1):98–109PubMed

Xi D, Kusano K, Gainer H (1999) Quantitative analysis of oxytocin and vasopressin messenger ribonucleic acids in single magnocellular neurons isolated from supraoptic nucleus of rat hypothalamus. Endocrinology 140(10):4677–4682PubMedCrossRef

Xiao M et al (2005) The distribution of neural nitric oxide synthase-positive cerebrospinal fluid-contacting neurons in the third ventricular wall of male rats and coexistence with vasopressin or oxytocin. Brain Res 1038(2):150–162CrossRefPubMed

Xu L et al (2010) Oxytocin and vasopressin immunoreactive staining in the brains of Brandt’s voles (Lasiopodomys brandtii) and greater long-tailed hamsters (Tscherskia triton). Neuroscience 169(3):1235–1247. doi:10.1016/j.neuroscience.2010.05.064 PubMedPubMedCentralCrossRef

Yang J et al (2011) Oxytocin in the periaqueductal gray participates in pain modulation in the rat by influencing endogenous opiate peptides. Peptides 32(6):1255–1261PubMedCrossRef

Yayou K-I, Ito S, Yamamoto N (2015) Relationships between postnatal plasma oxytocin concentrations and social behaviors in cattle. Anim Sci J 86(8):806–813PubMedCrossRef

Yoshida M et al (2009) Evidence that oxytocin exerts anxiolytic effects via oxytocin receptor expressed in serotonergic neurons in mice. J Neurosci 29(7):2259–2271PubMedCrossRef

Young LJ, Wang Z (2004) The neurobiology of pair bonding. Nat Neurosci 7(10):1048–1054PubMedCrossRef

Young LJ et al (1999) Increased affiliative response to vasopressin in mice expressing the V1a receptor from a monogamous vole. Nature 400(6746):766–768PubMedCrossRef

Zoli M, Agnati LF (1996) Wiring and volume transmission in the central nervous system: the concept of closed and open synapses. Prog Neurobiol 49(4):363–380PubMedCrossRef

Title: Distribution of oxytocin and co-localization with arginine vasopressin in the brain of mice
Authors: Marcos Otero-García
Carmen Agustín-Pavón
Enrique Lanuza
Fernando Martínez-García
Publication date: 01-09-2016
Publisher: Springer Berlin Heidelberg
Published in: Brain Structure and Function / Issue 7/2016
Print ISSN: 1863-2653
Electronic ISSN: 1863-2661
DOI: https://doi.org/10.1007/s00429-015-1111-y

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Distribution of oxytocin and co-localization with arginine vasopressin in the brain of mice

Abstract

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 7/2016

Exploring the role of neuropeptide S in the regulation of arousal: a functional anatomical study

Structure and function of the amygdaloid NPY system: NPY Y2 receptors regulate excitatory and inhibitory synaptic transmission in the centromedial amygdala

Common and distinct networks for self-referential and social stimulus processing in the human brain

Ascending serotonin neuron diversity under two umbrellas

The timing of language learning shapes brain structure associated with articulation

Linking morphological and functional variability in hand movement and silent reading