Skip to main content

Advertisement

SpringerLink
Log in

Endogenous opioid signalling in the brain during pregnancy and lactation

  • Review
  • Published:
Cell and Tissue Research Aims and scope Submit manuscript

Abstract

During pregnancy, the regulation of several neuroendocrine systems is altered to support the pregnancy and facilitate the transition to motherhood. These adaptations are organised by the mother’s brain and include those that serve to optimise foetal growth, protect the foetus(es) from adverse prenatal programming by maternal stress, facilitate timely parturition and ensure the offspring are nourished and cared for after birth. Although pregnancy hormones are important in inducing and maintaining many of these adaptations, their effects are often mediated via interactions with neuropeptide systems in the brain. In particular, endogenous opioids in the maternal brain play key roles in altered regulation of the stress axis, the oxytocin system, the prolactin system and the neural circuits controlling maternal behaviour. Together, these adaptations maximise the likelihood of a successful pregnancy outcome.

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

Similar content being viewed by others

References

  • Abe J, Okamura H, Makino S, Yanaihara N, Ibata Y (1987) Immunocytochemical distribution of [Met]enkephalin-Arg-Gly-Leu immunoreactivity in the rat diencephalon. Brain Res Bull 19:735–741

    Article  CAS  PubMed  Google Scholar 

  • Anderson GM, Beijer P, Bang AS, Fenwick MA, Bunn SJ, Grattan DR (2006a) Suppression of prolactin-induced signal transducer and activator of transcription 5b signaling and induction of suppressors of cytokine signaling messenger ribonucleic acid in the hypothalamic arcuate nucleus of the rat during late pregnancy and lactation. Endocrinology 147:4996–5005

    Article  CAS  PubMed  Google Scholar 

  • Anderson ST, Barclay JL, Fanning KJ, Kusters DH, Waters MJ, Curlewis JD (2006b) Mechanisms underlying the diminished sensitivity to prolactin negative feedback during lactation: reduced STAT5 signaling and up-regulation of cytokine-inducible SH2 domain-containing protein (CIS) expression in tuberoinfundibular dopaminergic neurons. Endocrinology 147:1195–1202

    Article  CAS  PubMed  Google Scholar 

  • Andrews ZB, Grattan DR (2002) Opioid control of prolactin secretion in late pregnant rats is mediated by tuberoinfundibular dopamine neurons. Neurosci Lett 328:60–64

    Article  CAS  PubMed  Google Scholar 

  • Andrews ZB, Grattan DR (2003) Opioid receptor subtypes involved in the regulation of prolactin secretion during pregnancy and lactation. J Neuroendocrinol 15:227–236

    Article  CAS  PubMed  Google Scholar 

  • Arbogast LA, Voogt JL (1991) Hyperprolactinemia increases and hypoprolactinemia decreases tyrosine hydroxylase messenger ribonucleic acid levels in the arcuate nuclei, but not the substantia nigra or zona incerta. Endocrinology 128:997–1005

    Article  CAS  PubMed  Google Scholar 

  • Augustine RA, Kokay IC, Andrews ZB, Ladyman SR, Grattan DR (2003) Quantitation of prolactin receptor mRNA in the maternal rat brain during pregnancy and lactation. J Mol Endocrinol 31:221–232

    Article  CAS  PubMed  Google Scholar 

  • Bali A, Randhawa PK, Jaggi AS (2015) Stress and opioids: role of opioids in modulating stress-related behavior and effect of stress on morphine conditioned place preference. Neurosci Biobehav Rev 51:138–150

    Article  CAS  PubMed  Google Scholar 

  • Barfield ET, Barry SM, Hodgin HB, Thompson BM, Allen SS, Grisel JE (2010) Beta-endorphin mediates behavioral despair and the effect of ethanol on the tail suspension test in mice. Alcohol Clin Exp Res 34:1066–1072

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Beaulieu J, Champagne D, Drolet G (1996) Enkephalin innervation of the paraventricular nucleus of the hypothalamus: distribution of fibers and origins of input. J Chem Neuroanat 10:79–92

    Article  CAS  PubMed  Google Scholar 

  • Benarroch EE (2012) Endogenous opioid systems: current concepts and clinical correlations. Neurology 79:807–814

    Article  PubMed  Google Scholar 

  • Ben-Jonathan N, Neill MA, Arbogast LA, Peters LL, Hoefer MT (1980) Dopamine in hypophysial portal blood: relationship to circulating prolactin in pregnant and lactating rats. Endocrinology 106:690–696

    Article  CAS  PubMed  Google Scholar 

  • Berube P, Laforest S, Bhatnagar S, Drolet G (2013) Enkephalin and dynorphin mRNA expression are associated with resilience or vulnerability to chronic social defeat stress. Physiol Behav 122:237–245

    Article  CAS  PubMed  Google Scholar 

  • Berube P, Poulin JF, Laforest S, Drolet G (2014) Enkephalin knockdown in the basolateral amygdala reproduces vulnerable anxiety-like responses to chronic unpredictable stress. Neuropsychopharmacology 39:1159–1168

    Article  CAS  PubMed  Google Scholar 

  • Bicknell RJ, Leng G, Russell JA, Dyer RG, Mansfield S, Zhao BG (1988) Hypothalamic opioid mechanisms controlling oxytocin neurones during parturition. Brain Res Bull 20:743–749

    Article  CAS  PubMed  Google Scholar 

  • Bodnar RJ (2011) Endogenous opiates and behavior: 2010. Peptides 32:2522–2552

    Article  CAS  PubMed  Google Scholar 

  • Bridges RS (1984) A quantitative analysis of the roles of dosage, sequence, and duration of estradiol and progesterone exposure in the regulation of maternal behavior in the rat. Endocrinology 114:930–940

    Article  CAS  PubMed  Google Scholar 

  • Bridges RS (2015) Neuroendocrine regulation of maternal behavior. Front Neuroendocrinol 36:178–196

    Article  CAS  PubMed  Google Scholar 

  • Bridges RS, Ronsheim PM (1990) Prolactin (PRL) regulation of maternal behavior in rats: bromocriptine treatment delays and PRL promotes the rapid onset of behavior. Endocrinology 126:837–848

    Article  CAS  PubMed  Google Scholar 

  • Bridges RS, Rosenblatt JS, Feder HH (1978) Serum progesterone concentrations and maternal behavior in rats after pregnancy termination: behavioral stimulation after progesterone withdrawal and inhibition by progesterone maintenance. Endocrinology 102:258–267

    Article  CAS  PubMed  Google Scholar 

  • Bridges RS, DiBiase R, Loundes DD, Doherty PC (1985) Prolactin stimulation of maternal behavior in female rats. Science 227:782–784

    Article  CAS  PubMed  Google Scholar 

  • Bridges RS, Numan M, Ronsheim PM, Mann PE, Lupini CE (1990) Central prolactin infusions stimulate maternal behavior in steroid-treated, nulliparous female rats. Proc Natl Acad Sci U S A 87:8003–8007

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bridges RS, Mann PE, Coppeta JS (1999) Hypothalamic involvement in the regulation of maternal behaviour in the rat: inhibitory roles for the ventromedial hypothalamus and the dorsal/anterior hypothalamic areas. J Neuroendocrinol 11:259–266

    Article  CAS  PubMed  Google Scholar 

  • Brown RS, Wyatt AK, Herbison RE, Knowles PJ, Ladyman SR, Binart N, Banks WA, Grattan DR (2016) Prolactin transport into mouse brain is independent of prolactin receptor. FASEB J 30:1002–1010

    Article  CAS  PubMed  Google Scholar 

  • Brown RSE, Aoki M, Ladyman SR, Phillipps HR, Wyatt A, Boehm U, Grattan DR (2017) Prolactin action in the medial preoptic area is necessary for postpartum maternal nursing behavior. Proc Natl Acad Sci U S A 114:10779–10784

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brunton PJ (2010) Resetting the dynamic range of hypothalamo-pituitary-adrenal axis stress responses through pregnancy. J Neuroendocrinol 22:1198–1213

    Article  CAS  PubMed  Google Scholar 

  • Brunton PJ, Russell JA (2003) Hypothalamic-pituitary-adrenal responses to centrally administered orexin-A are suppressed in pregnant rats. J Neuroendocrinol 15:633–637

    Article  CAS  PubMed  Google Scholar 

  • Brunton PJ, Russell JA (2010) Prenatal social stress in the rat programmes neuroendocrine and behavioural responses to stress in the adult offspring: sex specific effects. J Neuroendocrinol 22:258–271

    Article  CAS  PubMed  Google Scholar 

  • Brunton PJ, Meddle SL, Ma S, Ochedalski T, Douglas AJ, Russell JA (2005) Endogenous opioids and attenuated hypothalamic-pituitary-adrenal axis responses to immune challenge in pregnant rats. J Neurosci 25:5117–5126

    Article  CAS  PubMed  Google Scholar 

  • Brunton PJ, Bales J, Russell JA (2006a) Neuroendocrine stress but not feeding responses to centrally administered neuropeptide Y are suppressed in pregnant rats. Endocrinology 147:3737–3745

    Article  CAS  PubMed  Google Scholar 

  • Brunton PJ, Sabatier N, Leng G, Russell JA (2006b) Suppressed oxytocin neuron responses to immune challenge in late pregnant rats: a role for endogenous opioids. Eur J Neurosci 23:1241–1247

    Article  PubMed  Google Scholar 

  • Brunton PJ, McKay AJ, Ochedalski T, Piastowska A, Rebas E, Lachowicz A, Russell JA (2009) Central opioid inhibition of neuroendocrine stress responses in pregnancy in the rat is induced by the neurosteroid allopregnanolone. J Neurosci 29:6449–6460

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brunton PJ, Bales J, Russell JA (2012) Allopregnanolone and induction of endogenous opioid inhibition of oxytocin responses to immune stress in pregnant rats. J Neuroendocrinol 24:690–700

    Article  CAS  PubMed  Google Scholar 

  • Brunton PJ, Russell JA, Hirst JJ (2014) Allopregnanolone in the brain: protecting pregnancy and birth outcomes. Prog Neurobiol 113:106–136

    Article  CAS  PubMed  Google Scholar 

  • Brussaard AB, Herbison AE (2000) Long-term plasticity of postsynaptic GABA(A)-receptor function in the adult brain: insights from the oxytocin neurone. Trends Neurosci 23:190–195

    Article  CAS  PubMed  Google Scholar 

  • Buckingham JC, Cooper TA (1984) Differences in hypothalamo-pituitary-adrenocortical activity in the rat after acute and prolonged treatment with morphine. Neuroendocrinology 38:411–417

    Article  CAS  PubMed  Google Scholar 

  • Buckingham JC, Cooper TA (1986) Effects of naloxone on hypothalamo-pituitary-adrenocortical activity in the rat. Neuroendocrinology 42:421–426

    Article  CAS  PubMed  Google Scholar 

  • Buller KM, Hamlin AS, Osborne PB (2005) Dissection of peripheral and central endogenous opioid modulation of systemic interleukin-1beta responses using c-fos expression in the rat brain. Neuropharmacology 49:230–242

    Article  CAS  PubMed  Google Scholar 

  • Burbach JPH, Young LJ, Russell JA (2006) Oxytocin: synthesis, secretion, and reproductive functions. In: Neill JD (ed) Knobil and Neill’s physiology of reproduction. Elsevier, Amsterdam, pp 3055–3128

  • Byrnes EM, Bridges RS (2000) Endogenous opioid facilitation of maternal memory in rats. Behav Neurosci 114:797–804

    Article  CAS  PubMed  Google Scholar 

  • Byrnes EM, Rigero BA, Bridges RS (2000) Opioid receptor antagonism during early lactation results in the increased duration of nursing bouts. Physiol Behav 70:211–216

    Article  CAS  PubMed  Google Scholar 

  • Callahan P, Klosterman S, Prunty D, Tompkins J, Janik J (2000) Immunoneutralization of endogenous opioid peptides prevents the suckling-induced prolactin increase and the inhibition of tuberoinfundibular dopaminergic neurons. Neuroendocrinology 71:268–276

    Article  CAS  PubMed  Google Scholar 

  • Caron MG, Beaulieu M, Raymond V, Gagne B, Drouin J, Lefkowitz RJ, Labrie F (1978) Dopaminergic receptors in the anterior pituitary gland. Correlation of [3H]dihydroergocryptine binding with the dopaminergic control of prolactin release. J Biol Chem 253:2244–2253

    CAS  PubMed  Google Scholar 

  • Ceccatelli S, Orazzo C (1993) Effect of different types of stressors on peptide messenger ribonucleic acids in the hypothalamic paraventricular nucleus. Acta Endocrinol 128:485–492

    Article  CAS  PubMed  Google Scholar 

  • Champagne FA, Chretien P, Stevenson CW, Zhang TY, Gratton A, Meaney MJ (2004) Variations in nucleus accumbens dopamine associated with individual differences in maternal behavior in the rat. J Neurosci 24:4113–4123

    Article  CAS  PubMed  Google Scholar 

  • Cohn J, Gerall AA (1989) Pre- and postpuberal medial preoptic area lesions and maternal behavior in the rat. Physiol Behav 46:333–336

    Article  CAS  PubMed  Google Scholar 

  • Concas A, Mostallino MC, Porcu P, Follesa P, Barbaccia ML, Trabucchi M, Purdy RH, Grisenti P, Biggio G (1998) Role of brain allopregnanolone in the plasticity of gamma-aminobutyric acid type A receptor in rat brain during pregnancy and after delivery. Proc Natl Acad Sci U S A 95:13284–13289

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • da Costa APC, Wood S, Ingram CD, Lightman SL (1996) Region-specific reduction in stress-induced c-fos mRNA expression during pregnancy and lactation. Brain Res 742:177–184

    Article  PubMed  Google Scholar 

  • da Costa APC, Kampa RJ, Windle RJ, Ingram CD, Lightman SL (1997) Region-specific immediate-early gene expression following the administration of corticotropin-releasing hormone in virgin and lactating rats. Brain Res 770:151–162

    Article  PubMed  Google Scholar 

  • da Costa AP, Ma X, Ingram CD, Lightman SL, Aguilera G (2001) Hypothalamic and amygdaloid corticotropin-releasing hormone (CRH) and CRH receptor-1 mRNA expression in the stress-hyporesponsive late pregnant and early lactating rat. Brain Res Mol Brain Res 91:119–130

    Article  PubMed  Google Scholar 

  • Demarest KT, Duda NJ, Riegle GD, Moore KE (1983a) Placental lactogen mimics prolactin in activating tuberoinfundibular dopaminergic neurons. Brain Res 272:175–178

    Article  CAS  PubMed  Google Scholar 

  • Demarest KT, McKay DW, Riegle GD, Moore KE (1983b) Biochemical indices of tuberoinfundibular dopaminergic neuronal activity during lactation: a lack of response to prolactin. Neuroendocrinology 36:130–137

    Article  CAS  PubMed  Google Scholar 

  • Desjardins GC, Brawer JR, Beaudet A (1990) Distribution of mu, delta, and kappa opioid receptors in the hypothalamus of the rat. Brain Res 536:114–123

    Article  CAS  PubMed  Google Scholar 

  • Douglas AJ, Clarke G, MacMillan SJ, Bull PM, Neumann I, Way SA, Wright DM, McGrory BG, Russell JA (1993a) Effects of the kappa-opioid agonist U50,488 on parturition in rats. Br J Pharmacol 109:251–258

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Douglas AJ, Dye S, Leng G, Russell JA, Bicknell RJ (1993b) Endogenous opioid regulation of oxytocin secretion through pregnancy in the rat. J Neuroendocrinol 5:307–314

    Article  CAS  PubMed  Google Scholar 

  • Douglas AJ, Neumann I, Meeren HKM, Leng G, Johnstone LE, Munro G, Russell JA (1995) Central endogenous opioid inhibition of supraoptic oxytocin neurons in pregnant rats. J Neurosci 15:5049–5057

    Article  CAS  PubMed  Google Scholar 

  • Douglas AJ, Johnstone HA, Wigger A, Landgraf R, Neumann ID (1998a) The role of endogenous opioids in neurohypophysial and hypothalamo-pituitary-adrenal axis hormone secretory responses to stress in pregnant rats. J Endocrinol 158:285–293

    Article  CAS  PubMed  Google Scholar 

  • Douglas AJ, Meeren HK, Johnstone LE, Pfaff DW, Russell JA, Brooks PJ (1998b) Stimulation of expression of the oxytocin gene in rat supraoptic neurons at parturition. Brain Res 782:167–174

    Article  CAS  PubMed  Google Scholar 

  • Douglas AJ, Johnstone H, Brunton P, Russell JA (2000) Sex-steroid induction of endogenous opioid inhibition on oxytocin secretory responses to stress. J Neuroendocrinol 12:343–350

    Article  CAS  PubMed  Google Scholar 

  • Douglas AJ, Scullion S, Antonijevic IA, Brown D, Russell JA, Leng G (2001) Uterine contractile activity stimulates supraoptic neurons in term pregnant rats via a noradrenergic pathway. Endocrinology 142:633–644

    Article  CAS  PubMed  Google Scholar 

  • Douglas AJ, Bicknell RJ, Leng G, Russell JA, Meddle SL (2002) Beta-endorphin cells in the arcuate nucleus: projections to the supraoptic nucleus and changes in expression during pregnancy and parturition. J Neuroendocrinol 14:768–777

    Article  CAS  PubMed  Google Scholar 

  • Douglas AJ, Brunton PJ, Bosch OJ, Russell JA, Neumann ID (2003) Neuroendocrine responses to stress in mice: hyporesponsiveness in pregnancy and parturition. Endocrinology 144:5268–5276

    Article  CAS  PubMed  Google Scholar 

  • Douglas A, Meddle S, Toschi N, Bosch O, Neumann I (2005) Reduced activity of the noradrenergic system in the paraventricular nucleus at the end of pregnancy: implications for stress hyporesponsiveness. J Neuroendocrinol 17:40–48

    Article  CAS  PubMed  Google Scholar 

  • Driessen TM, Eisinger BE, Zhao C, Stevenson SA, Saul MC, Gammie SC (2014) Genes showing altered expression in the medial preoptic area in the highly social maternal phenotype are related to autism and other disorders with social deficits. BMC Neurosci 15:11

    Article  PubMed  PubMed Central  Google Scholar 

  • Drolet G, Dumont EC, Gosselin I, Kinkead R, Laforest S, Trottier JF (2001) Role of endogenous opioid system in the regulation of the stress response. Prog Neuro-Psychopharmacol Biol Psychiatry 25:729–741

    Article  CAS  Google Scholar 

  • Dyball RE, Leng G (1986) Regulation of the milk ejection reflex in the rat. J Physiol 380:239–256

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Eisinger BE, Zhao C, Driessen TM, Saul MC, Gammie SC (2013) Large scale expression changes of genes related to neuronal signaling and developmental processes found in lateral septum of postpartum outbred mice. PLoS One 8:e63824

    Article  PubMed  PubMed Central  Google Scholar 

  • Eisinger BE, Driessen TM, Zhao C, Gammie SC (2014) Medial prefrontal cortex: genes linked to bipolar disorder and schizophrenia have altered expression in the highly social maternal phenotype. Front Behav Neurosci 8:110

    Article  PubMed  PubMed Central  Google Scholar 

  • Elovitz MA, Mrinalini C (2004) Animal models of preterm birth. Trends Endocrinol Metab 15:479–487

    Article  CAS  PubMed  Google Scholar 

  • Ericsson A, Kovacs KJ, Sawchenko PE (1994) A functional anatomical analysis of central pathways subserving the effects of interleukin-1 on stress-related neuroendocrine neurons. J Neurosci 14:897–913

    Article  CAS  PubMed  Google Scholar 

  • Fallon JH, Leslie FM (1986) Distribution of dynorphin and enkephalin peptides in the rat brain. J Comp Neurol 249:293–336

    Article  CAS  PubMed  Google Scholar 

  • Feher P, Olah M, Bodnar I, Hechtl D, Bacskay I, Juhasz B, Nagy GM, Vecsernyes M (2010) Dephosphorylation/inactivation of tyrosine hydroxylase at the median eminence of the hypothalamus is required for suckling-induced prolactin and adrenocorticotrop hormone responses. Brain Res Bull 82:141–145

    Article  CAS  PubMed  Google Scholar 

  • Ferguson JKW (1941) A study of the motility of the intact uterus at term. Surg Gynecol Obstet 73:359–366

    Google Scholar 

  • Ferris CF, Kulkarni P, Sullivan JM Jr, Harder JA, Messenger TL, Febo M (2005) Pup suckling is more rewarding than cocaine: evidence from functional magnetic resonance imaging and three-dimensional computational analysis. J Neurosci 25:149–156

    Article  CAS  PubMed  Google Scholar 

  • Fitzsimmons MD, Olschowka JA, Wiegand SJ, Hoffman GE (1992) Interaction of opioid peptide-containing terminals with dopaminergic perikarya in the rat hypothalamus. Brain Res 581:10–18

    Article  CAS  PubMed  Google Scholar 

  • Fuchs AR, Saito S (1971) Pituitary oxytocin and vasopressin content of pregnant rats before, during and after parturition. Endocrinology 88:574–578

    Article  CAS  PubMed  Google Scholar 

  • Gammie SC, Driessen TM, Zhao C, Saul MC, Eisinger BE (2016) Genetic and neuroendocrine regulation of the postpartum brain. Front Neuroendocrinol 42:1–17

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gibori G, Richards JS (1978) Dissociation of two distinct luteotropic effects of prolactin: regulation of luteinizing hormone-receptor content and progesterone secretion during pregnancy. Endocrinology 102:767–774

    Article  CAS  PubMed  Google Scholar 

  • Gonzalez-Iglesias AE, Fletcher PA, Arias-Cristancho JA, Cristancho-Gordo R, Helena CV, Bertram R, Tabak J (2015) Direct stimulatory effects of oxytocin in female rat gonadotrophs and somatotrophs in vitro: comparison with lactotrophs. Endocrinology 156:600–612

    Article  CAS  PubMed  Google Scholar 

  • Goodwin TM, Paul R, Silver H, Spellacy W, Parsons M, Chez R, Hayashi R, Valenzuela G, Creasy GW, Merriman R (1994) The effect of the oxytocin antagonist atosiban on preterm uterine activity in the human. Am J Obstet Gynecol 170:474–478

    Article  CAS  PubMed  Google Scholar 

  • Grattan DR, Averill RL (1990) Effect of ovarian steroids on a nocturnal surge of prolactin secretion that precedes parturition in the rat. Endocrinology 126:1199–1205

    Article  CAS  PubMed  Google Scholar 

  • Grattan DR, Steyn FJ, Kokay IC, Anderson GM, Bunn SJ (2008) Pregnancy-induced adaptation in the neuroendocrine control of prolactin secretion. J Neuroendocrinol 20:497–507

    Article  CAS  PubMed  Google Scholar 

  • Grisel JE, Bartels JL, Allen SA, Turgeon VL (2008) Influence of beta-endorphin on anxious behavior in mice: interaction with EtOH. Psychopharmacology 200:105–115

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guillou A, Romano N, Steyn F, Abitbol K, Le Tissier P, Bonnefont X, Chen C, Mollard P, Martin AO (2015) Assessment of lactotroph axis functionality in mice: longitudinal monitoring of PRL secretion by ultrasensitive-ELISA. Endocrinology 156:1924–1930

    Article  CAS  PubMed  Google Scholar 

  • Gunnet JW, Freeman ME (1983) The mating-induced release of prolactin: a unique neuroendocrine response. Endocr Rev 4:44–61

    Article  CAS  PubMed  Google Scholar 

  • Gustafson P, Bunn SJ, Grattan DR (2017) The role of prolactin in the suppression of Crh mRNA expression during pregnancy and lactation in the mouse. J Neuroendocrinol 29

  • Hammer RP Jr, Bridges RS (1987) Preoptic area opioids and opiate receptors increase during pregnancy and decrease during lactation. Brain Res 420:48–56

    Article  CAS  PubMed  Google Scholar 

  • Hansen S, Harthon C, Wallin E, Lofberg L, Svensson K (1991) Mesotelencephalic dopamine system and reproductive behavior in the female rat: effects of ventral tegmental 6-hydroxydopamine lesions on maternal and sexual responsiveness. Behav Neurosci 105:588–598

    Article  CAS  PubMed  Google Scholar 

  • Harbuz MS, Lightman SL (1989) Responses of hypothalamic and pituitary mRNA to physical and psychological stress in the rat. J Endocrinol 122:705–711

    Article  CAS  PubMed  Google Scholar 

  • Harbuz MS, Jessop DS, Lightman SL, Chowdrey SL (1994) The effects of restraint or hypertonic saline stress on corticotropin-releasing factor, arginine-vasopressin, and proenkephalin-a messenger-RNAs in the CFY, Sprague-Dawley and Wistar strains of rat. Brain Res 667:6–12

    Article  CAS  PubMed  Google Scholar 

  • Harlan RE, Shivers BD, Romano GJ et al (1987) Localization of preproenkephalin mRNA in the rat brain and spinal cord by in situ hybridization. J Comp Neurol 258:159–184

    Article  CAS  PubMed  Google Scholar 

  • Henry MS, Bisht K, Vernoux N, Gendron L, Torres-Berrio A, Drolet G, Tremblay ME (2018) Delta opioid receptor signaling promotes resilience to stress under the repeated social defeat paradigm in mice. Front Mol Neurosci 11:100

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Herbison AE, Voisin DL, Douglas AJ, Chapman C (1997) Profile of monoamine and excitatory amino acid release in rat supraoptic nucleus over parturition. Endocrinology 138:33–40

    Article  CAS  PubMed  Google Scholar 

  • Higuchi T, Uchide K, Honda K, Negoro H (1986) Oxytocin release during parturition in the pelvic-neurectomized rat. J Endocrinol 109:149–154

    Article  CAS  PubMed  Google Scholar 

  • Horvath TL, Naftolin F, Leranth C (1992) Beta-endorphin innervation of dopamine neurons in the rat hypothalamus: a light and electron microscopic double immunostaining study. Endocrinology 131:1547–1555

    Article  CAS  PubMed  Google Scholar 

  • Kammerer M, Adams D, Castelberg Bv B, Glover V (2002) Pregnant women become insensitive to cold stress. BMC Pregnancy Childbirth 2:8

    Article  PubMed  PubMed Central  Google Scholar 

  • Kang W, Wilson SP, Wilson MA (2000) Overexpression of proenkephalin in the amygdala potentiates the anxiolytic effects of benzodiazepines. Neuropsychopharmacology 22:77–88

    Article  CAS  PubMed  Google Scholar 

  • Katoh A, Nabeshima T, Kameyama T (1990) Behavioral changes induced by stressful situations: effects of enkephalins, dynorphin, and their interactions. J Pharmacol Exp Ther 253:600–607

    CAS  PubMed  Google Scholar 

  • Keer SE, Stern JM (1999) Dopamine receptor blockade in the nucleus accumbens inhibits maternal retrieval and licking, but enhances nursing behavior in lactating rats. Physiol Behav 67:659–669

    Article  CAS  PubMed  Google Scholar 

  • Khachaturian H, Watson SJ, Lewis ME, Coy D, Goldstein A, Akil H (1982) Dynorphin immunocytochemistry in the rat central nervous system. Peptides 3:941–954

    Article  CAS  PubMed  Google Scholar 

  • Khachaturian H, Lewis ME, Watson SJ (1983) Enkephalin systems in diencephalon and brainstem of the rat. J Comp Neurol 220:310–320

    Article  CAS  PubMed  Google Scholar 

  • Knobloch HS, Charlet A, Hoffmann LC, Eliava M, Khrulev S, Cetin AH, Osten P, Schwarz MK, Seeburg PH, Stoop R, Grinevich V (2012) Evoked axonal oxytocin release in the central amygdala attenuates fear response. Neuron 73:553–566

    Article  CAS  PubMed  Google Scholar 

  • Koksma JJ, van Kesteren RE, Rosahl TW, Zwart R, Smit AB, Luddens H, Brussaard AB (2003) Oxytocin regulates neurosteroid modulation of GABA(A) receptors in supraoptic nucleus around parturition. J Neurosci 23:788–797

    Article  CAS  PubMed  Google Scholar 

  • Konig M, Zimmer AM, Steiner H, Holmes PV, Crawley JN, Brownstein MJ, Zimmer A (1996) Pain responses, anxiety and aggression in mice deficient in pre-proenkephalin. Nature 383:535–538

    Article  CAS  PubMed  Google Scholar 

  • Lang RE, Heil JWE, Ganten D, Hermann K, Unger T, Rascher W (1983) Oxytocin unlike vasopressin is a stress hormone in the rat. Neuroendocrinology 37:314–316

    Article  CAS  PubMed  Google Scholar 

  • Le Merrer J, Becker JA, Befort K, Kieffer BL (2009) Reward processing by the opioid system in the brain. Physiol Rev 89:1379–1412

    Article  PubMed  PubMed Central  Google Scholar 

  • Lee Y, Voogt JL (1999) Feedback effects of placental lactogens on prolactin levels and Fos-related antigen immunoreactivity of tuberoinfundibular dopaminergic neurons in the arcuate nucleus during pregnancy in the rat. Endocrinology 140:2159–2166

    Article  CAS  PubMed  Google Scholar 

  • Lee A, Clancy S, Fleming AS (2000) Mother rats bar-press for pups: effects of lesions of the MPOA and limbic sites on maternal behavior and operant responding for pup-reinforcement. Behav Brain Res 108:215–231

    Article  CAS  PubMed  Google Scholar 

  • Lee HJ, Macbeth AH, Pagani JH, WSr Y (2009) Oxytocin: the great facilitator of life. Prog Neurobiol 88:127–151

    CAS  PubMed  PubMed Central  Google Scholar 

  • Leng G, Mansfield S, Bicknell RJ, Blackburn RE, Brown D, Chapman C, Dyer RG, Hollingsworth S, Shibuki K, Yates JO, Way SA (1988) Endogenous opioid actions and effects of environmental disturbance on parturition and oxytocin secretion in rats. J Reprod Fertil 84:345–356

    Article  CAS  PubMed  Google Scholar 

  • Leng G, Bicknell R, Brown D, Bowden C, Chapman C, Russell J (1994) Stimulus-induced depletion of pro-enkephalins, oxytocin and vasopressin and pro-enkephalin interaction with posterior pituitary hormone release in vitro. Neuroendocrinology 60:559–566

    Article  CAS  PubMed  Google Scholar 

  • Leng G, Brown CH, Murphy NP, Onaka T, Russell JA (1995) Opioid-noradrenergic interactions in the control of oxytocin cells. Adv Exp Med Biol 395:95–104

    CAS  PubMed  Google Scholar 

  • Lerant A, Freeman ME (1998) Ovarian steroids differentially regulate the expression of PRL-R in neuroendocrine dopaminergic neuron populations: a double label confocal microscopic study. Brain Res 802:141–154

    Article  CAS  PubMed  Google Scholar 

  • Lightman SL, Young WSI (1989) Lactation inhibits stress-mediated secretion of corticosterone and oxytocin and hypothalamic accumulation of corticotropin-releasing factor and enkephalin messenger ribonucleic acids. Endocrinology 124:2358–2364

    Article  CAS  PubMed  Google Scholar 

  • Lucas BK, Ormandy CJ, Binart N, Bridges RS, Kelly PA (1998) Null mutation of the prolactin receptor gene produces a defect in maternal behavior. Endocrinology 139:4102–4107

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Ma S, Shipston MJ, Morilak D, Russell JA (2005) Reduced hypothalamic vasopressin secretion underlies attenuated adrenocorticotropin stress responses in pregnant rats. Endocrinology 146:1626–1637

    Article  CAS  PubMed  Google Scholar 

  • Maccari S, Krugers HJ, Morley-Fletcher S, Szyf M, Brunton PJ (2014) The consequences of early-life adversity: neurobiological, behavioural and epigenetic adaptations. J Neuroendocrinol 26:707–723

    Article  CAS  PubMed  Google Scholar 

  • Mann PE, Bridges RS (1992) Neural and endocrine sensitivities to opioids decline as a function of multiparity in the rat. Brain Res 580:241–248

    Article  CAS  PubMed  Google Scholar 

  • Mann PE, Kinsley CH, Bridges RS (1991) Opioid receptor subtype involvement in maternal behavior in lactating rats. Neuroendocrinology 53:487–492

    Article  CAS  PubMed  Google Scholar 

  • Mansi JA, Laforest S, Drolet G (2000) Effect of stress exposure on the activation pattern of enkephalin-containing perikarya in the rat ventral medulla. J Neurochem 74:2568–2575

    Article  CAS  PubMed  Google Scholar 

  • Mansour A, Khachaturian H, Lewis ME, Akil H, Watson SJ (1987) Autoradiographic differentiation of mu, delta, and kappa opioid receptors in the rat forebrain and midbrain. J Neurosci 7:2445–2464

    CAS  PubMed  Google Scholar 

  • Mansour A, Meador-Woodruff JH, Bunzow JR, Civelli O, Akil H, Watson SJ (1990) Localization of dopamine D2 receptor mRNA and D1 and D2 receptor binding in the rat brain and pituitary: an in situ hybridization-receptor autoradiographic analysis. J Neurosci 10:2587–2600

    Article  CAS  PubMed  Google Scholar 

  • Mansour A, Fox CA, Burke S, Meng F, Thompson RC, Akil H, Watson SJ (1994a) Mu, delta, and kappa opioid receptor mRNA expression in the rat CNS: an in situ hybridization study. J Comp Neurol 350:412–438

    Article  CAS  PubMed  Google Scholar 

  • Mansour A, Fox CA, Meng F, Akil H, Watson SJ (1994b) Kappa 1 receptor mRNA distribution in the rat CNS: comparison to kappa receptor binding and prodynorphin mRNA. Mol Cell Neurosci 5:124–144

    Article  CAS  PubMed  Google Scholar 

  • Mansour A, Fox CA, Thompson RC, Akil H, Watson SJ (1994c) Mu-opioid receptor mRNA expression in the rat CNS: comparison to mu-receptor binding. Brain Res 643:245–265

    Article  CAS  PubMed  Google Scholar 

  • Meddle SL, Leng G, Selvarajah JR, Bicknell RJ, Russell JA (2000) Direct pathways to the supraoptic nucleus from the brainstem and the main olfactory bulb are activated at parturition in the rat. Neuroscience 101:1013–1021

    Article  CAS  PubMed  Google Scholar 

  • Meddle SL, Bishop VR, Gkoumassi E, van Leeuwen FW, Douglas AJ (2007) Dynamic changes in oxytocin receptor expression and activation at parturition in the rat brain. Endocrinology 148:5095–5104

    Article  CAS  PubMed  Google Scholar 

  • Merchenthaler I (1994) Induction of enkephalin in tuberoinfundibular dopaminergic neurons of pregnant, pseudopregnant, lactating and aged female rats. Neuroendocrinology 60:185–193

    Article  CAS  PubMed  Google Scholar 

  • Merchenthaler I, Maderdrut JL, Altschuler RA, Petrusz P (1986) Immunocytochemical localization of proenkephalin-derived peptides in the central nervous system of the rat. Neuroscience 17:325–348

    Article  CAS  PubMed  Google Scholar 

  • Merchenthaler I, Lennard DE, Cianchetta P, Merchenthaler A, Bronstein D (1995) Induction of proenkephalin in tuberoinfundibular dopaminergic neurons by hyperprolactinemia: the role of sex steroids. Endocrinology 136:2442–2450

    Article  CAS  PubMed  Google Scholar 

  • Mesiano S, Chan EC, Fitter JT, Kwek K, Yeo G, Smith R (2002) Progesterone withdrawal and estrogen activation in human parturition are coordinated by progesterone receptor A expression in the myometrium. J Clin Endocrinol Metab 87:2924–2930

    Article  CAS  PubMed  Google Scholar 

  • Minami M, Onogi T, Toya T, Katao Y, Hosoi Y, Maekawa K, Katsumata S, Yabuuchi K, Satoh M (1994) Molecular cloning and in situ hybridization histochemistry for rat mu-opioid receptor. Neurosci Res 18:315–322

    Article  CAS  PubMed  Google Scholar 

  • Moos F, Gouzenes L, Brown D, Dayanithi G, Sabatier N, Boissin L, Rabie A, Richard P (1998) New aspects of firing pattern autocontrol in oxytocin and vasopressin neurones. Adv Exp Med Biol 449:153–162

    Article  CAS  PubMed  Google Scholar 

  • Murata T, Murata E, Liu CX, Narita K, Honda K, Higuchi T (2000) Oxytocin receptor gene expression in rat uterus: regulation by ovarian steroids. J Endocrinol 166:45–52

    Article  CAS  PubMed  Google Scholar 

  • Murata T, Narita K, Honda K, Matsukawa S, Higuchi T (2003) Differential regulation of estrogen receptor alpha and beta mRNAs in the rat uterus during pregnancy and labor: possible involvement of estrogen receptors in oxytocin receptor regulation. Endocr J 50:579–587

    Article  CAS  PubMed  Google Scholar 

  • Nahi F, Arbogast LA (2003) Prolactin modulates hypothalamic preproenkephalin, but not proopiomelanocortin, gene expression during lactation. Endocrine 20:115–122

    Article  CAS  PubMed  Google Scholar 

  • Nelson EE, Panksepp J (1998) Brain substrates of infant-mother attachment: contributions of opioids, oxytocin, and norepinephrine. Neurosci Biobehav Rev 22:437–452

    Article  CAS  PubMed  Google Scholar 

  • Neumann I, Russell JA, Wolff B, Landgraf R (1991) Naloxone increases the release of oxytocin, but not vasopressin, within limbic brain areas of conscious parturient rats: a push-pull perfusion study. Neuroendocrinology 54:545–551

    Article  CAS  PubMed  Google Scholar 

  • Neumann I, Russell JA, Landgraf R (1993) Oxytocin and vasopressin release within the supraoptic and paraventricular nuclei of pregnant, parturient and lactating rats: a microdialysis study. Neuroscience 53:65–75

    Article  CAS  PubMed  Google Scholar 

  • Neumann I, Douglas AJ, Pittman QJ, Russell JA, Landgraf R (1996) Oxytocin released within the supraoptic nucleus of the rat brain by positive feedback action is involved in parturition-related events. J Neuroendocrinol 8:227–233

    Article  CAS  PubMed  Google Scholar 

  • Neumann ID, Johnstone HA, Hatzinger M, Liebsch G, Shipston M, Russell JA, Landgraf R, Douglas AJ (1998) Attenuated neuroendocrine responses to emotional and physical stressors in pregnant rats involve adenohypophysial changes. J Physiol 508:289–300

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Neumann ID, Bosch OJ, Toschi N, Torner L, Douglas AJ (2003) No stress response of the hypothalamo-pituitary-adrenal axis in parturient rats: lack of involvement of brain oxytocin. Endocrinology 144:2473–2479

    Article  CAS  PubMed  Google Scholar 

  • Numan M (2007) Motivational systems and the neural circuitry of maternal behavior in the rat. Dev Psychobiol 49:12–21

    Article  CAS  PubMed  Google Scholar 

  • 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 29:23–51

    Article  CAS  PubMed  Google Scholar 

  • Numan M, Smith HG (1984) Maternal behavior in rats: evidence for the involvement of preoptic projections to the ventral tegmental area. Behav Neurosci 98:712–727

    Article  CAS  PubMed  Google Scholar 

  • Numan M, Rosenblatt JS, Komisaruk BR (1977) Medial preoptic area and onset of maternal behavior in the rat. J Comp Physiol Psychol 91:146–164

    Article  CAS  PubMed  Google Scholar 

  • Ormandy CJ, Binart N, Kelly PA (1997) Mammary gland development in prolactin receptor knockout mice. J Mammary Gland Biol Neoplasia 2:355–364

    Article  CAS  PubMed  Google Scholar 

  • Parada M, King S, Li M, Fleming AS (2008) The roles of accumbal dopamine D1 and D2 receptors in maternal memory in rats. Behav Neurosci 122:368–376

    Article  PubMed  Google Scholar 

  • Paris JJ, Brunton PJ, Russell JA, Walf AA, Frye CA (2011) Inhibition of 5alpha-reductase activity in late pregnancy decreases gestational length and fecundity and impairs object memory and central progestogen milieu of juvenile rat offspring. J Neuroendocrinol 23:1079–1090

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pedersen CA, Ascher JA, Monroe YL, Prange AJ Jr (1982) Oxytocin induces maternal behavior in virgin female rats. Science 216:648–650

    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 

  • Peters LC, Kristal MB, Komisaruk BR (1987) Sensory innervation of the external and internal genitalia of the female rat. Brain Res 408:199–204

    Article  CAS  PubMed  Google Scholar 

  • Pumford KM, Leng G, Russell JA (1991) Morphine actions on supraoptic oxytocin neurones in anaesthetized rats: tolerance after i.c.v. morphine infusion. J Physiol 440:437–454

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pumford KM, Russell JA, Leng G (1993) Effects of the selective kappa-opioid agonist U50,488 upon the electrical activity of supraoptic neurones in morphine-tolerant and morphine-naive rats. Exp Brain Res 94:237–246

    CAS  PubMed  Google Scholar 

  • Randle JC, Mazurek M, Kneifel D, Dufresne J, Renaud LP (1986) Alpha 1-adrenergic receptor activation releases vasopressin and oxytocin from perfused rat hypothalamic explants. Neurosci Lett 65:219–223

    Article  CAS  PubMed  Google Scholar 

  • Reymond MJ, Porter JC (1985) Involvement of hypothalamic dopamine in the regulation of prolactin secretion. Horm Res 22:142–152

    Article  CAS  PubMed  Google Scholar 

  • Romano N, Yip SH, Hodson DJ, Guillou A, Parnaudeau S, Kirk S, Tronche F, Bonnefont X, Le Tissier P, Bunn SJ, Grattan DR, Mollard P, Martin AO (2013) Plasticity of hypothalamic dopamine neurons during lactation results in dissociation of electrical activity and release. J Neurosci 33:4424–4433

    Article  CAS  PubMed  Google Scholar 

  • Rossoni E, Feng J, Tirozzi B, Brown D, Leng G, Moos F (2008) Emergent synchronous bursting of oxytocin neuronal network. PLoS Comput Biol 4:e1000123

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rubin BS, Bridges RS (1984) Disruption of ongoing maternal responsiveness in rats by central administration of morphine sulfate. Brain Res 307:91–97

    Article  CAS  PubMed  Google Scholar 

  • Russell JA, Brunton PJ (2009) Oxytocin. In: Squire LR (ed) Encyclopedia of neuroscience, vol 7. Oxford Academic Press, pp 337–347

  • Russell JA, Douglas AJ (2000) Opioids. In: Fink G (ed) Encyclopedia of Stress, vol 3. Academic Press, San Diego, pp 86–98

  • Russell JA, Gosden RG, Humphreys EM, Cutting R, Fitzsimons N, Johnston V, Liddle S, Scott S, Stirland JA (1989) Interruption of parturition in rats by morphine: a result of inhibition of oxytocin secretion. J Endocrinol 121:521–536

    Article  CAS  PubMed  Google Scholar 

  • Sagrillo CA, Voogt JL (1991) Endogenous opioids mediate the nocturnal prolactin surge in the pregnant rat. Endocrinology 129:925–930

    Article  CAS  PubMed  Google Scholar 

  • Samson WK, Lumpkin MD, McCann SM (1986) Evidence for a physiological role for oxytocin in the control of prolactin secretion. Endocrinology 119:554–560

    Article  CAS  PubMed  Google Scholar 

  • Sanders MJ, Kieffer BL, Fanselow MS (2005) Deletion of the mu opioid receptor results in impaired acquisition of Pavlovian context fear. Neurobiol Learn Mem 84:33–41

    Article  CAS  PubMed  Google Scholar 

  • Schulte HM, Weisner D, Allolio B (1990) The corticotrophin releasing hormone test in late pregnancy: lack of adrenocorticotrophin and cortisol response. Clin Endocrinol 33:99–106

    Article  CAS  Google Scholar 

  • Selmanoff M, Gregerson KA (1985) Suckling decreases dopamine turnover in both medial and lateral aspects of the median eminence in the rat. Neurosci Lett 57:25–30

    Article  CAS  PubMed  Google Scholar 

  • Selmanoff M, Wise PM (1981) Decreased dopamine turnover in the median eminence in response to suckling in the lactating rat. Brain Res 212:101–115

    Article  CAS  PubMed  Google Scholar 

  • Shanks N, Windle RJ, Perks P, Wood S, Ingram CD, Lightman SL (1999) The hypothalamic-pituitary-adrenal axis response to endotoxin is attenuated during lactation. J Neuroendocrinol 11:857–865

    Article  CAS  PubMed  Google Scholar 

  • Sheehan T, Numan M (2002) Estrogen, progesterone, and pregnancy termination alter neural activity in brain regions that control maternal behavior in rats. Neuroendocrinology 75:12–23

    Article  CAS  PubMed  Google Scholar 

  • Smith MS, Neill JD (1976) Termination at midpregnancy of the two daily surges of plasma prolactin initiated by mating in the rat. Endocrinology 98:696–701

    Article  CAS  PubMed  Google Scholar 

  • Soaje M, Deis RP (1994) A modulatory role of endogenous opioids on prolactin secretion at the end of pregnancy in the rat. J Endocrinol 140:97–102

    Article  CAS  PubMed  Google Scholar 

  • Soaje M, Valdez S, Bregonzio C, Penissi A, Deis RP (2006) Dopaminergic mechanisms involved in prolactin release after mifepristone and naloxone treatment during late pregnancy in the rat. Neuroendocrinology 84:58–67

    Article  CAS  PubMed  Google Scholar 

  • Srisawat R, Ludwig M, Bull PM, Douglas AJ, Russell JA, Leng G (2000) Nitric oxide and the oxytocin system in pregnancy. J Neurosci 20:6721–6727

    Article  CAS  PubMed  Google Scholar 

  • Stack EC, Balakrishnan R, Numan MJ, Numan M (2002) A functional neuroanatomical investigation of the role of the medial preoptic area in neural circuits regulating maternal behavior. Behav Brain Res 131:17–36

    Article  PubMed  Google Scholar 

  • Steyn FJ, Anderson GM, Grattan DR (2008) Hormonal regulation of suppressors of cytokine signaling (SOCS) messenger ribonucleic acid in the arcuate nucleus during late pregnancy. Endocrinology 149:3206–3214

    Article  CAS  PubMed  Google Scholar 

  • Stolzenberg DS, McKenna JB, Keough S, Hancock R, Numan MJ, Numan M (2007) Dopamine D1 receptor stimulation of the nucleus accumbens or the medial preoptic area promotes the onset of maternal behavior in pregnancy-terminated rats. Behav Neurosci 121:907–919

    Article  CAS  PubMed  Google Scholar 

  • Sukikara MH, Mota-Ortiz SR, Baldo MV, Felicio LF, Canteras NS (2006) A role for the periaqueductal gray in switching adaptive behavioral responses. J Neurosci 26:2583–2589

    Article  CAS  PubMed  Google Scholar 

  • Sukikara MH, Platero MD, Canteras NS, Felicio LF (2007) Opiate regulation of behavioral selection during lactation. Pharmacol Biochem Behav 87:315–320

    Article  CAS  PubMed  Google Scholar 

  • Torner L, Neumann ID (2002) The brain prolactin system: involvement in stress response adaptations in lactation. Stress 5:249–257

    Article  CAS  PubMed  Google Scholar 

  • Torner L, Toschi N, Nava G, Clapp C, Neumann ID (2002) Increased hypothalamic expression of prolactin in lactation: involvement in behavioural and neuroendocrine stress responses. Eur J Neurosci 15:1381–1389

    Article  PubMed  Google Scholar 

  • Toufexis DJ, Walker C-D (1996) Noradrenergic facilitation of the adrenocorticotropin response to stress is absent during lactation in the rat. Brain Res 737:71–77

    Article  CAS  PubMed  Google Scholar 

  • Toufexis DJ, Thrivikraman KV, Plotsky PM, Morilak DA, Huang N, Walker C-D (1998) Reduced noradrenergic tone to the hypothalamic paraventricular nucleus contributes to the stress hyporesponsiveness of lactation. J Neuroendocrinol 10:417–427

    Article  CAS  PubMed  Google Scholar 

  • Toufexis DJ, Tesolin S, Huang N, Walker C (1999) Altered pituitary sensitivity to corticotropin-releasing factor and arginine vasopressin participates in the stress hyporesponsiveness of lactation in the rat. J Neuroendocrinol 11:757–764

    Article  CAS  PubMed  Google Scholar 

  • 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 521:1633–1663

    Article  CAS  PubMed  Google Scholar 

  • Valdez SR, Pennacchio GE, Gamboa DF, de Di Nasso EG, Bregonzio C, Soaje M (2014) Opioid modulation of prolactin secretion induced by stress during late pregnancy. Role of ovarian steroids. Pharmacol Rep 66:386–393

    Article  CAS  PubMed  Google Scholar 

  • Villegas-Gabutti CM, Pennacchio GE, Vivas L, Jahn GA, Soaje M (2018) Role of oxytocin in prolactin secretion during late pregnancy. Neuroendocrinology 106:324–334

    Article  CAS  PubMed  Google Scholar 

  • Voogt JL (1984) Evidence for an inhibitory influence of rat placental lactogen on prolactin release in vitro. Biol Reprod 31:141–147

    Article  CAS  PubMed  Google Scholar 

  • Voogt J, Robertson M, Friesen H (1982) Inverse relationship of prolactin and rat placental lactogen during pregnancy. Biol Reprod 26:800–805

    Article  CAS  PubMed  Google Scholar 

  • Walsh RJ, Slaby FJ, Posner BI (1987) A receptor-mediated mechanism for the transport of prolactin from blood to cerebrospinal fluid. Endocrinology 120:1846–1850

    Article  CAS  PubMed  Google Scholar 

  • Wamsley JK, Young WS 3rd, Kuhar MJ (1980) Immunohistochemical localization of enkephalin in rat forebrain. Brain Res 190:153–174

    Article  CAS  PubMed  Google Scholar 

  • Wang HJ, Hoffman GE, Smith MS (1993) Suppressed tyrosine hydroxylase gene expression in the tuberoinfundibular dopaminergic system during lactation. Endocrinology 133:1657–1663

    Article  CAS  PubMed  Google Scholar 

  • Welsh T, Johnson M, Yi L, Tan H, Rahman R, Merlino A, Zakar T, Mesiano S (2012) Estrogen receptor (ER) expression and function in the pregnant human myometrium: estradiol via ERalpha activates ERK1/2 signaling in term myometrium. J Endocrinol 212:227–238

    Article  CAS  PubMed  Google Scholar 

  • Wigger A, Lorscher P, Oehler I, Keck ME, Naruo T, Neumann ID (1999) Nonresponsiveness of the rat hypothalamo-pituitary-adrenocortical axis to parturition-related events: inhibitory action of endogenous opioids. Endocrinology 140:2843–2849

    Article  CAS  PubMed  Google Scholar 

  • Windle RJ, Wood S, Shanks N, Perks P, Conde GL, da Costa APC, Ingram CD, Lightman SL (1997) Endocrine and behavioural responses to noise stress: comparison of virgin and lactating female rats during non-disrupted maternal activity. J Neuroendocrinol 9:407–414

    Article  CAS  PubMed  Google Scholar 

  • Zhao BG, Chapman C, Bicknell RJ (1988a) Functional kappa-opioid receptors on oxytocin and vasopressin nerve terminals isolated from the rat neurohypophysis. Brain Res 462:62–66

    Article  CAS  PubMed  Google Scholar 

  • Zhao BG, Chapman C, Bicknell RJ (1988b) Opioid-noradrenergic interactions in the neurohypophysis. I. Differential opioid receptor regulation of oxytocin, vasopressin, and noradrenaline release. Neuroendocrinology 48:16–24

    Article  CAS  PubMed  Google Scholar 

  • Zhao C, Eisinger BE, Driessen TM, Gammie SC (2014) Addiction and reward-related genes show altered expression in the postpartum nucleus accumbens. Front Behav Neurosci 8:388

    PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

The research performed in the laboratory of PJB described here was funded by the Biotechnology and Biological Sciences Research Council.

Author information

Authors and Affiliations

  1. Centre for Discovery Brain Sciences, University of Edinburgh, Hugh Robson Building, George Square, Edinburgh, Scotland, EH8 9XD, UK

    Paula J. Brunton

  2. Zhejiang University–University of Edinburgh Institute, Haining, Zhejiang, People’s Republic of China

    Paula J. Brunton

Authors
  1. Paula J. Brunton
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Paula J. Brunton.

Ethics declarations

Conflict of interest

The author declares that she has no conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Brunton, P.J. Endogenous opioid signalling in the brain during pregnancy and lactation. Cell Tissue Res 375, 69–83 (2019). https://doi.org/10.1007/s00441-018-2948-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00441-018-2948-1

Keywords

Search

Navigation