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Prolactin function and putative expression in the brain

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Abstract

Introduction

Prolactin is a peptide hormone mainly synthetized and secreted by the anterior pituitary gland, but also by extrapituitary tissues, such as mammary gland, decidua, prostate, skin, and possibly the brain. Similarly, prolactin receptor is expressed in the pituitary gland, many peripheral tissues, and in contrast to prolactin, its receptor has been consistently detected in several brain regions, such as cerebral cortex, olfactory bulb, hypothalamus, hippocampus, amygdala, among others. Classically, prolactin function has been related to the stimulation of lactogenesis and galactopoiesis, however, it is well known that prolactin induces a wide range of functions in different brain areas.

Purpose

The aim of this review is to summarize recent reports on prolactin and prolactin receptor synthesis and localization, as well as recapitulate both the classic functions attributed to this hormone in the brain and the recently described functions such as neurogenesis, neurodevelopment, sleep, learning and memory, and neuroprotection.

Conclusion

The distribution and putative expression of prolactin and its receptors in several neuronal tissues suggests that this hormone has pleiotropic functions in the brain.

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References

  1. A. Ignacak, M. Kasztelnik, T. Sliwa, R.A. Korbut, K. Rajda, T.J. Guzik, Prolactin—Not only lactotrophin a “new” view of the “old” hormone. J. Physiol. Pharmacol. 63(5), 435–443 (2012)

    CAS  PubMed  Google Scholar 

  2. R.J. Marano, N. Ben-Jonathan, Minireview: extrapituitary prolactin: an update on the distribution, regulation, and functions. Mol. Endocrinol. 28(5), 622–633 (2014)

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  3. D.R. Grattan, I.C. Kokay, Prolactin: a pleiotropic neuroendocrine hormone. J. Neuroendocrinol. 20(6), 752–763 (2008)

    Article  CAS  PubMed  Google Scholar 

  4. R., Bates, E., Lahr, O., Riddle, The gross action of prolactin and follicle-stimulating hormone on the mature ovary and sex accessories of fowl. Am. J. Physiol. I(II), 361–368 (1935)

  5. N. Ben-jonathan, J.L. Mershonf, D.L. Allen, R.W. Steinmetz, Extrapituitary prolactin: distribution, regulation, functions, and clinical aspects. Endocr. Rev. 17(6), 639–669 (1996)

    CAS  PubMed  Google Scholar 

  6. S. Harvey, Extrapituitary growth hormone. Endocrine 38(3), 335–359 (2010)

    Article  CAS  PubMed  Google Scholar 

  7. S. Harvey, C. Arámburo, E.J. Sanders, Extrapituitary production of anterior pituitary hormones: an overview. Endocrine 41(1), 19–30 (2012)

    Article  CAS  PubMed  Google Scholar 

  8. R.J., Walsh, F.J., Slaby, B.I.Posner, A receptor-mediated mechanism for the transport of prolactin from blood to cerebrospinal fluid. Endocrinology 120(5), 1846–1850 (1987)

  9. R.S.E. Brown, A.K. Wyatt, R.E. Herbison, P.J. Knowles, S.R. Ladyman, N. Binart, W.A. Banks, D.R. Grattan, Prolactin transport into mouse brain is independent of prolactin receptor. FASEB J. 30(2), 1002–1010 (2016)

    Article  CAS  PubMed  Google Scholar 

  10. N. Emanuele, J. Jurgens, M. Halloran, J. Tentler, A. Lawrence, M. Kelley, The rat prolactin gene is expressed in brain tissue: detection of normal and alternatively spliced prolactin messenger RNA. Mol. Endocrinol. 6(1), 35–42 (1992)

    CAS  PubMed  Google Scholar 

  11. K. Fields, E. Kulig, R. Lloyd, Detection of prolactin messenger RNA in mammary and other normal and neoplastic tissues by polymerase chain reaction. Lab. Invest. 68(3), 354–360 (1993)

    CAS  PubMed  Google Scholar 

  12. H. Ehmann, C. Salzig, P. Lang, E. Friauf, H. Nothwang, Minimal sex differences in gene expression in the rat superior olivary complex. Hear. Res. 245(1–2), 65–72 (2008)

    Article  PubMed  Google Scholar 

  13. W. DeVito, C. Avakian, S. Stone, C. Ace, Estradiol increases prolactin synthesis and prolactin messenger ribonucleic acid in selected brain regions in the hypophysectomized female rat. Endocrinology 131(5), 2154–2160 (1992)

    Article  CAS  PubMed  Google Scholar 

  14. C.E. Roselli, S. Bocklandt, H.L. Stadelman, T. Wadsworth, E. Vilain, F. Stormshak, Prolactin expression in the sheep brain. Neuroendocrinology 87(4), 206–215 (2008)

    Article  CAS  PubMed  Google Scholar 

  15. W. DeVito, Distribution of immunoreactive prolactin in the male and female rat brain: effects of hypophysectomy and intraventricular administration of colchicine. Neuroendocrinology 47(4), 284–289 (1988)

    Article  CAS  PubMed  Google Scholar 

  16. V. Goffin, P. Kelly, The prolactin/growth hormone receptor family: structure/function relationships. J. Mammary Gland Biol. Neoplasia 2(1), 7–17 (1997)

    Article  CAS  PubMed  Google Scholar 

  17. C. Bole-Feysot, V. Goffin, M. Edery, N. Binart, P. Kelly, Prolactin (PRL) and its receptor: action signal transduction pathways and phenotypes observed in PRL receptor knockout mice. Endocr. Rev. 19(3), 225–268 (1998)

    Article  CAS  PubMed  Google Scholar 

  18. M. Freeman, B. Kanyicska, A. Lenart, G. Nagy, Prolactin: structure, function and regulation of secretion. Physiol. Rev. 80, 1523–1631 (2000)

    CAS  PubMed  Google Scholar 

  19. C. Clevenger, J. Kline, Prolactin receptor signal transduction. Lupus 10(10), 706–718 (2001)

    Article  CAS  PubMed  Google Scholar 

  20. X. Pi, J.L. Voogt, Sex difference and estrous cycle: Expression of prolactin receptor mRNA in rat brain. Mol. Brain Res. 103(1–2), 130–139 (2002)

    Article  CAS  PubMed  Google Scholar 

  21. J. Bakowska, J. Morrell, The distribution of mRNA for the short form of the prolactin receptor in the forebrain of the female rat. Brain Res. 116(1–2), 50–58 (2003)

    Article  CAS  Google Scholar 

  22. J.C. Bakowska, J.I. Morrell, Atlas of the neurons that express mRNA for the long form of the prolactin receptor in the forebrain of the female rat. J. Comp. Neurol. 386(2), 161–177 (1997)

    Article  CAS  PubMed  Google Scholar 

  23. X.J. Pi, D.R. Grattan, Increased expression of both short and long forms of prolactin receptor mRNA in hypothalamic nuclei of lactating rats. J. Mol. Endocrinol. 23(1), 13–22 (1999)

    Article  CAS  PubMed  Google Scholar 

  24. T. Fujikawa, H. Soya, H. Yoshizato, K. Sakaguchi, K. Doh-Ura, M. Tanaka, K. Nakashima, Restraint stress enhances the gene expression of prolactin receptor long form at the choroid plexus. Endocrinology 136, 5608–5613 (1995)

    Article  CAS  PubMed  Google Scholar 

  25. J. Hirai, M. Nishita, N. Nakao, T.R. Saito, M. Tanaka, Regulation of prolactin receptor gene expression in the rat choroid plexus via transcriptional activation of multiple first exons during postnatal development and lactation. Exp. Anim. 62(1), 49–56 (2013)

    Article  CAS  PubMed  Google Scholar 

  26. S. Chiu, P.M. Wise, Prolactin receptor mRNA localization in the hypothalamus by in situ hybridization. J. Neuroendocrinol. 6(2), 191–199 (1994)

    Article  CAS  PubMed  Google Scholar 

  27. R.S. Brown, I.C. Kokay, A.E. Herbison, D.R. Grattan, Distribution of prolactin-responsive neurons in the mouse forebrain. J. Comp. Neurol. 518(1), 92–102 (2010)

    Article  CAS  PubMed  Google Scholar 

  28. T.A. Möderscheim, T. Gorba, P. Pathipati, I.C. Kokay, D.R. Grattan, C.E. Williams, A. Scheepens, Prolactin is involved in glial responses following a focal injury to the juvenile rat brain. Neuroscience 145(3), 963–973 (2007)

    Article  PubMed  CAS  Google Scholar 

  29. L. Torner, S. Karg, A. Blume, M. Kandasamy, H.G. Kuhn, J. Winkler, L. Aigner, I.D. Neumann, Prolactin prevents chronic stress-induced decrease of adult hippocampal neurogenesis and promotes neuronal fate. J. Neurosci. 29(6), 1826–1833 (2009)

    Article  CAS  PubMed  Google Scholar 

  30. E.A. Cabrera-Reyes, E. Vergara-Castañeda, N. Rivero-Segura, M. Cerbón, Sex differences in prolactin and its receptor expression in pituitary, hypothalamus, and hippocampus of the rat. Rev. Mex. Endocrinol. Metab. Nutr. 2(2), 60–67 (2015)

    Google Scholar 

  31. X.J. Pi, D.R. Grattan, Distribution of prolactin receptor immunoreactivity in the brain of estrogen-treated, ovariectomized rats. J. Comp. 394, 462–474 (1998)

    CAS  Google Scholar 

  32. Allen Institute for Brain Science, Allen Mouse Brain Atlas. http://mouse.brain-map.org/experiment/show/72340223 (2004).

  33. M. Shamgochian, C. Avakian, N. Truong, S. Stone, K. Tang, W. DeVito, Regulation of prolactin receptor expression by estradiol in the female rat brain. Neuroreport. 6(18), 2537–2541 (1995)

    Article  CAS  PubMed  Google Scholar 

  34. P. Mann, R. Bridges, Prolactin receptor gene expression in the forebrain of pregnant and lactating rats. Brain Res. Mol. Brain Res. 105(1–2), 136–145 (2002)

    Article  CAS  PubMed  Google Scholar 

  35. S. Chiu, R.D. Koos, P.M. Wise, Detection of prolactin receptor (PRL-R) mRNA in the rat hypothalamus and pituitary gland. Endocrinology 130(3), 1747–1749 (1992)

    CAS  PubMed  Google Scholar 

  36. S.H. Yip, R. Eguchi, D.R. Grattan, S.J. Bunn, Prolactin signalling in the mouse hypothalamus is primarily mediated by signal transducer and activator of transcription factor 5b but not 5a. J. Neuroendocrinol. 24(12), 1484–1491 (2012)

    Article  CAS  PubMed  Google Scholar 

  37. R. Das, B. Vonderhaar, Transduction of prolactin’s (PRL) growth signal through both long and short forms of the PRL receptor. Mol. Endocrinol. 9, 1750–1759 (1995)

    CAS  PubMed  Google Scholar 

  38. J. Harris, P.M. Stanford, S.R. Oakes, C.J. Ormandy, Prolactin and the prolactin receptor: new targets of an old hormone. Ann. Med. 36(6), 414–425 (2004)

    Article  CAS  PubMed  Google Scholar 

  39. L. Torner, E. Tinajero, N. Lajud, A. Quintanar-Stéphano, E. Olvera-Cortés, Hyperprolactinemia impairs object recognition without altering spatial learning in male rats. Behav. Brain Res. 252, 32–39 (2013)

    Article  CAS  PubMed  Google Scholar 

  40. M.J. Patil, M.A. Henry, A.N. Akopian, Prolactin receptor in regulation of neuronal excitability and channels. Channels 8(3), 193–202 (2014)

    Article  PubMed  PubMed Central  Google Scholar 

  41. F. Drago, Prolactin and sexual behavior: a review. Neurosci. Biobehav. Rev. 8, 433–439 (1984)

    Article  CAS  PubMed  Google Scholar 

  42. D. Tejadilla, M. Cerbón, T. Morales, Prolactin reduces the damaging effects of excitotoxicity in the dorsal hippocampus of the female rat independently of ovarian hormones. Neuroscience 169(3), 1178–1185 (2010)

    Article  CAS  PubMed  Google Scholar 

  43. A. Vanoye-Carlo, T. Morales, E. Ramos, A. Mendoza-Rodríguez, M. Cerbón, Neuroprotective effects of lactation against kainic acid treatment in the dorsal hippocampus of the rat. Horm. Behav. 53(1), 112–123 (2008)

    Article  CAS  PubMed  Google Scholar 

  44. V. Cabrera, D. Cantú, E. Ramos, A. Vanoye-Carlo, M. Cerbón, T. Morales, Lactation is a natural model of hippocampus neuroprotection against excitotoxicity. Neurosci. Lett. 461(2), 136–139 (2009)

    Article  CAS  PubMed  Google Scholar 

  45. V. Cabrera, E. Ramos, A. González-Arenas, M. Cerbón, I. Camacho-Arroyo, T. Morales, Lactation reduces glial activation induced by excitotoxicity in the rat hippocampus. J. Neuroendocrinol. 25(6), 519–527 (2013)

    Article  CAS  PubMed  Google Scholar 

  46. R. Brown, A. Herbison, D. Grattan, Effects of prolactin and lactation on A15 dopamine neurones in the rostral preoptic area of female mice. J. Neuroendocrinol. 27(9), 708–717 (2015)

    Article  CAS  PubMed  Google Scholar 

  47. J.A. Seggie, G.M. Brown, Stress response patterns of plasma corticosterone, prolactin, and growth hormone in the rat, following handling or exposure to novel environment. Can. J. Physiol. Pharmacol. 53(4), 629–637 (1975)

    Article  CAS  PubMed  Google Scholar 

  48. A.C. de Moura, V.M. Lazzari, R.O. Becker, M.S. Gil, C.A. Ruthschilling, G. Agnes, S. Almeida, A.B. da Veiga, A.B. Luicion, M. Giovenardo, Gene expression in the CNS of lactating rats with different patterns of maternal behavior. Neurosci. Res. 99, 8–15 (2015)

    Article  PubMed  CAS  Google Scholar 

  49. C.M. Larsen, I.C. Kokay, D.R. Grattan, Male pheromones initiate prolactin-induced neurogenesis and advance maternal behavior in female mice. Horm. Behav. 53(4), 509–517 (2008)

    Article  CAS  PubMed  Google Scholar 

  50. F. Lévy, M. Keller, P. Poindron, Olfactory regulation of maternal behavior in mammals. Horm. Behav. 46(3), 284–302 (2004)

    Article  PubMed  Google Scholar 

  51. H. Salais-López, E. Lanuza, C. Agustín-Pavón, F. Martínez-García, Tuning the brain for motherhood: prolactin-like central signalling in virgin, pregnant, and lactating female mice. Brain Struct. Funct. 222(2), 895–921 (2017)

    Article  PubMed  CAS  Google Scholar 

  52. M. Freemark, P. Driscoll, J. Andrews, P.A. Kelly, M. Royster, Ontogenesis of prolactin receptor gene expression in the rat olfactory system: potential roles for lactogenic hormones in olfactory development. Endocrinology 137(3), 934–942 (1996)

    Article  CAS  PubMed  Google Scholar 

  53. T. Shingo, C. Gregg, E. Enwere, H. Fujikawa, R. Hassam, C. Geary, J.C. Cross, S. Weiss, Pregnancy-stimulated neurogenesis in the adult female forebrain mediated by prolactin. Science 299(5603), 117–120 (2003)

    Article  CAS  PubMed  Google Scholar 

  54. R. Bridges, D. Grattan, Prolactin-induced neurogenesis in the maternal brain. Trends Endocrinol. Metab. 14(5), 199–201 (2003)

    Article  CAS  PubMed  Google Scholar 

  55. N., Lajud, R., Gonzalez-Zapien, A., Roque, E., Tinajero, J.J., Valdez, C., Clapp, L., Torner, Prolactin administration during early postnatal life decreases hippocampal and olfactory bulb neurogenesis and results in depressive-like behavior in adulthood. Horm. Behav. 64(5), 781–789 (2013)

  56. A. Fleming, M. Korsmit, Plasticity in the maternal circuit: effects of maternal experience on Fos-Lir in hypothalamic, limbic, and cortical structures in the postpartum rat. Behav. Neurosci. 110(3), 567–582 (1996)

    Article  CAS  PubMed  Google Scholar 

  57. Y. Elyada, A. Mizrahi, Becoming a mother-circuit plasticity underlying maternal behavior. Curr. Opin. Neurobiol. 35, 49–56 (2015)

    Article  CAS  PubMed  Google Scholar 

  58. J.N. Lundström, A. Mathe, B. Schaal, J. Frasnelli, K. Nitzsche, J. Gerber, T. Hummel, Maternal status regulates cortical responses to the body odor of newborns. Front. Psychol. 4, 1–6 (2013)

    Article  Google Scholar 

  59. L. Cohen, A. Mizrahi, Plasticity during motherhood: changes in excitatory and inhibitory layer 2/3 neurons in auditory cortex. J. Neurosci. 35(4), 1806–1815 (2015)

    Article  CAS  PubMed  Google Scholar 

  60. C. Gregg, V. Shikar, P. Larsen, G. Mak, A. Chojnacki, V.W. Yong, S. Weiss, White matter plasticity and enhanced remyelination in the maternal CNS. J. Neurosci. 27(8), 1812–1823 (2007)

    Article  CAS  PubMed  Google Scholar 

  61. M. Maheu, E. Akbari, A. Fleming, Callosal oligodendrocyte number in postpartum Sprague-Dawley rats. Brain Res. 24(1267), 18–24 (2009)

    Article  CAS  Google Scholar 

  62. P. Mann, R. Bridges, Lactogenic hormone regulation of maternal behavior. Prog. Brain Res. 133, 251–262 (2001)

    Article  CAS  PubMed  Google Scholar 

  63. M. Numan, M. Numan, 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. Psycobiol. 29(1), 23–51 (1996)

    Article  CAS  Google Scholar 

  64. M. Numan, A neural circuitry analysis of maternal behavior in the rat. Acta Paediatr. Suppl. 397, 19–28 (1994)

    Article  CAS  PubMed  Google Scholar 

  65. A. Consiglio, A. Borsoi, G. Pereira, A. Lucion, Effects of oxytocin microinjected into the central amygdaloid nucleus and bed nucleus of stria terminalis on maternal aggressive behavior in rats. Physiol. Behav. 85(3), 354–362 (2005)

    Article  CAS  PubMed  Google Scholar 

  66. S. Kenny, L. Wright, A. Green, R. Mashoodh, T. Perrot, Expression of maternal behavior and activation of the bed nucleus of the stria terminalis during predatory threat exposure: modulatory effects of transport stress. Physiol. Behav. 17(123), 148–155 (2014)

    Article  CAS  Google Scholar 

  67. L.P. Mangurian, R.J. Walsh, B.I. Posner, Prolactin enhancement of its own uptake at the choroid plexus. Endocrinology 131, 698–702 (1992)

    CAS  PubMed  Google Scholar 

  68. R.A. Augustine, I.C. Kokay, Z.B. Andrews, S.R. Ladyman, D.R. Grattan, Quantitation of prolactin receptor mRNA in the maternal rat brain during pregnancy and lactation. J. Mol. Endocrinol. 31(1), 221–232 (2003)

    Article  CAS  PubMed  Google Scholar 

  69. H. Tabata, M. Kobayashi, J.H. Ikeda, N. Nakao, T.R. Saito, M. Tanaka, Characterization of multiple first exons in murine prolactin receptor gene and the effect of prolactin on their expression in the choroid plexus. J. Mol. Endocrinol. 48(2), 169–176 (2012)

    Article  CAS  PubMed  Google Scholar 

  70. X.J. Pi, D.R. Grattan, Differential expression of the two forms of prolactin receptor mRNA within microdissected hypothalamic nuclei of the rat. Brain Res. Mol. Brain Res. 59(1), 1–12 (1998)

    Article  CAS  PubMed  Google Scholar 

  71. R. Abs, E. Van Vleymen, P. Parizel, K. Van Acker, M. Martin, J. Martin, Congenital cerebellar hypoplasia and hypogonadotropic hypogonadism. J. Neurol. Sci. 98(2–3), 259–265 (1990)

    Article  CAS  PubMed  Google Scholar 

  72. G. Leng, R. Dyball, S. Luckman, Mechanisms of vasopressin secretion. Horm. Res. 37(1–2), 33–38 (1992)

    Article  CAS  PubMed  Google Scholar 

  73. G. Kennedy, The hypothalamic control of food intake in rats. Proc. R. Soc. Lond. B. Biol. Sci. 137(889), 535–549 (1950)

    Article  CAS  PubMed  Google Scholar 

  74. C.M., Brooks, E., Lambert, P., Bard, Experimental production of obesity in the monkey (Macaca mulatta). Fed. Proc. 1, 11 (1942)

  75. D. Sauvé, B. Woodside, The effect of central administration of prolactin on food intake in virgin female rats is dose-dependent, occurs in the absence of ovarian hormones and the latency to onset varies with feeding regimen. Brain Res. 729(1), 75–81 (1996)

    Article  PubMed  Google Scholar 

  76. D. Sauve, B. Woodside, Neuroanatomical specificity of prolactin-induced hyperphagia in virgin female rats. Brain Res. 868(2), 306–314 (2000)

    Article  CAS  PubMed  Google Scholar 

  77. S. Mejía, L.M. Torner, M.C. Jeziorski, C. Gonzalez, M.A. Morales, G.M. Martínez de la Escalera, C.: Clapp, Prolactin and 16K prolactin stimulate release of vasopressin by a direct effect on hypothalamo-neurohypophyseal system. Endocrine 20(1–2), 155–162 (2003)

    Article  PubMed  Google Scholar 

  78. S. Mejía, M. Morales, M. Zetina, G. Martínez de la Escalera, C.: Clapp, Immunoreactive prolactin forms colocalize with vasopressin in neurons of the hypothalamic paraventricular and supraoptic nuclei. Neuroendocrinology 66(3), 151–159 (1997)

    Article  PubMed  Google Scholar 

  79. C. Pedersen, J. Ascher, Y. Monroe, A.J. Prange, Oxytocin induces maternal behavior in virgin female rats. Science 216(4546), 648–650 (1982)

    Article  CAS  PubMed  Google Scholar 

  80. J.M. Zimmermann-Peruzatto, V.M. Lazzari, A.C. de Moura, S. Almeida, M. Giovenardi, Examining the role of vasopressin in the modulation of parental and sexual behaviors. Front. Psychiatry 6, 1–8 (2015)

    Article  Google Scholar 

  81. H.H. Van Tol, E.L. Bolwerk, B. Liu, J.P. Burbach, Oxytocin and vasopressin gene expression in the hypothalamo-neurohypophyseal system of the rat during the estrous cycle, pregnancy, and lactation. Endocrinology 122(3), 945–951 (1988)

    Article  PubMed  Google Scholar 

  82. N. Donner, I. Neumann, Effects of chronic intracerebral prolactin on the oxytocinergic and vasopressinergic system of virgin ovariectomized rats. Neuroendocrinology 90(3), 315–322 (2009)

    Article  CAS  PubMed  Google Scholar 

  83. R., Augustine, G., Bouwer, A., Seymour, D., Grattan, C., Brown, Reproductive regulation of gene expression in the hypothalamic supraoptic and paraventricular nuclei. J. Neuroendocrinol. (4), (2016). doi:10.1111/jne.12350

  84. K. Suzuki, N. Koizumi, H. Hirose, R. Hokao, N. Takemura, S. Motoyoshi, Changes in plasma arginine vasopressin concentration during lactation in rats. Comp. Med. 50(3), 277–280 (2000)

    CAS  PubMed  Google Scholar 

  85. N. Donner, R. Bredewold, R. Maloumby, I.D. Neumann, Chronic intracerebral prolactin attenuates neuronal stress circuitries in virgin rats. Eur. J. Neurosci. 25(6), 1804–1814 (2007)

    Article  PubMed  Google Scholar 

  86. L. Krulich, E. Hefco, P. Illner, C.B. Read, The effects of acute stress on the secretion of LH, FSH, prolactin and GH in the normal male rat, with comments on their statistical evaluation. Neuroendocrinology 16, 293–311 (1974)

    Article  CAS  PubMed  Google Scholar 

  87. B. Bodosi, F. Obál Jr., J. Gardi, J. Komlódi, J. Fang, J.M. Krueger, An ether stressor increases REM sleep in rats: possible role of prolactin. Am. J. Physiol. 279(5), 1590–1589 (2000)

    Google Scholar 

  88. R.R. Gala, The physiology and mechanisms of the stress-induced changes in prolactin secretion in the rat. Life Sci. 46, 1407–1420 (1990)

    Article  CAS  PubMed  Google Scholar 

  89. F. Obal Jr., M. Opp, A.B. Cady, L. Johannsen, J.M. Krueger, Prolactin, vasoactive intestinal peptide, and peptide histidine methionine elicit selective increases in REM sleep in rabbits. Brain Res. 490, 292–300 (1989)

    Article  CAS  PubMed  Google Scholar 

  90. P. Meerlo, A. Easton, B.M. Bergmann, F.W. Turek, Restraint increases prolactin and REM sleep in C57BL/6J mice but not in BALB/cJ mice. Am. J. Physiol. 281(3), 846–854 (2001)

    Google Scholar 

  91. R.B. Machado, M.R. Rocha, D. Suchecki, Brain prolactin is involved in stress-induced REM sleep rebound. Horm. Behav. 89, 38–47 (2016)

    Article  PubMed  CAS  Google Scholar 

  92. R.M. Frieboes, H. Murck, G.K. Stalla, I.A. Antonijevic, A. Steiger, Enhanced slow wave sleep in patients with prolactinoma. J. Clin. Endocrinol. Metab. 83, 2706–2710 (1998)

    Article  CAS  PubMed  Google Scholar 

  93. K. Koike, A. Miyake, T. Aono, T. Sakumoto, M. Ohmichi, M. Yamaguchi, O. Tanizawa, Effect of prolactin on the secretion of hypothalamic GnRH and pituitary gonadotropins. Horm. Res. 35(1), 5–12 (1991)

    Article  CAS  PubMed  Google Scholar 

  94. R. Araujo-Lopes, J. Crampton, N. Aquino, R. Miranda, I. Kokay, A. Reis, C.R. Franci, D.R. Grattan, R.E. Szawka, Prolactin regulates kisspeptin neurons in the arcuate nucleus to suppress LH secretion in female rats. Endocrinology 155(3), 1010–1020 (2014)

    Article  PubMed  CAS  Google Scholar 

  95. J. Clarkson, X. d’Anglemont de Tassigny, W. Colledge, A. Caraty, A. Herbison, Distribution of kisspeptin neurones in the adult female mouse brain. J. Neuroendocrinol. 21(8), 673–682 (2009)

    Article  CAS  PubMed  Google Scholar 

  96. I.C. Kokay, S.L. Petersen, D.R. Grattan, Identification of prolactin-sensitive GABA and kisspeptin neurons in regions of the rat hypothalamus involved in the control of fertility. Endocrinology 152(2), 526–535 (2011)

    Article  CAS  PubMed  Google Scholar 

  97. I. Cohen-Becker, M. Selmanoff, P. Wise, Hyperprolactinemia alters the frequency and amplitude of pulsatile luteinizing hormone secretion in the ovariectomized rat. Neuroendocrinology 42(4), 328–333 (1986)

    Article  CAS  PubMed  Google Scholar 

  98. A. Lerant, M.E. Freeman, Ovarian steroids differentially regulate the expression of PRL-R in neuroendocrine dopaminergic neuron populations: A double label confocal microscopic study. Brain Res. 802(1–2), 141–154 (1998)

    Article  CAS  PubMed  Google Scholar 

  99. G. Anderson, D. Grattan, W. van den Ancker, R. Bridges, Reproductive experience increases prolactin responsiveness in the medial preoptic area and arcuate nucleus of female rats. Endocrinology 147, 4688–4694 (2006)

    Article  CAS  PubMed  Google Scholar 

  100. L. Torner, R. Maloumby, G. Nava, J. Aranda, C. Clapp, I.D. Neumann, In vivo release and gene upregulation of brain prolactin in response to physiological stimuli. Eur. J. Neurosci. 19(6), 1601–1608 (2004)

    Article  PubMed  Google Scholar 

  101. J.A. McHenry, D.R. Rubinow, G.D. Stuber, Maternally responsive neurons in the bed nucleus of the stria terminalis and medial preoptic area: Putative circuits for regulating anxiety and reward. Front. Neuroendocrinol. 38, 65–72 (2015)

    Article  PubMed  PubMed Central  Google Scholar 

  102. R.S. Bridges, M. Numan, P.M. Ronsheim, P.E. Mann, C.E. Lupini, Central prolactin infusions stimulate maternal behavior in steroid-treated, nulliparous female rats. Proc. Natl. Acad. Sci. USA 87(20), 8003–8007 (1990)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  103. F.K. Stephan, I. Zucker, Circadian rhythms in drinking behavior and locomotor activity of rats are eliminated by hypothalamic lesions. Proc. Natl. Acad. Sci. USA 69(6), 1583–1586 (1972)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  104. C. Bethea, J. Neill, Lesions of the suprachiasmatic nuclei abolish the cervically stimulated prolactin surges in the rat. Endocrinology 107(1), 1–5 (1980)

    Article  CAS  PubMed  Google Scholar 

  105. K. Brown-Grant, G. Raisman, Abnormalities in reproductive function associated with the destruction of the suprachiasmatic nuclei in female rats. Proc. R. Soc. Lond. B Biol. Sci. 198(1132), 279–296 (1977)

    Article  CAS  PubMed  Google Scholar 

  106. J.T. Pan, R.R. Gala, Central nervous system regions involved in the estrogen-induced afternoon prolactin surge. II. Implantation studies. Endocrinology 117(1), 388–395 (1985)

    Article  CAS  PubMed  Google Scholar 

  107. J. Pan, R. Gala, Central nervous system regions involved in the estrogen-induced afternoon prolactin surge. I. Lesion studies. Endocrinology 117(1), 382–387 (1985)

    Article  CAS  PubMed  Google Scholar 

  108. I. Clarke, J. Cummins, D. de Kretser, Pituitary gland function after disconnection from direct hypothalamic influences in the sheep. Neuroendocrinology 36(5), 376–384 (1983)

    Article  CAS  PubMed  Google Scholar 

  109. J.D. Johnston, D.J. Skene, Regulation of mammalian neuroendocrine physiology and rhythms by melatonin. J. Endocrinol. 226(2), T187–T198 (2015)

    Article  CAS  PubMed  Google Scholar 

  110. S. Shyr, W. Crowley, C. Grosvenor, Effect of neonatal prolactin deficiency on prepubertal tuberoinfundibuler and tuberohypophyseal dopaminergic neuronal activity. Endocrinology 119(3), 1217–1221 (1986)

    Article  CAS  PubMed  Google Scholar 

  111. C. Grosvenor, N. Whitworth, Accumulation of prolactin in maternal milk and its transfer to circulation of neonate rat: a review. Endocrinol. Exp. 17, 271–282 (1983)

    CAS  PubMed  Google Scholar 

  112. M. Royster, P. Driscoll, P. Kelly, M. Freemark, The prolactin receptor in the fetal rat: cellular localization of messenger ribonucleic acid, immunoreactive protein, and ligand-binding activity and induction of expression in late gestation. Endocrinology 136(9), 3892–3900 (1995)

    Article  CAS  PubMed  Google Scholar 

  113. A.I. Melo, M. Perez-Ledezma, C. Clapp, E. Arnold, J.C. Rivera, A.S. Fleming, Effects of prolactin deficiency during the early postnatal period on the development of maternal behavior in female rats: Mother’s milk makes the difference. Horm. Behav. 56(3), 281–291 (2009)

    Article  CAS  PubMed  Google Scholar 

  114. E. Vergara-Castañeda, D.R. Grattan, H. Pasantes-Morales, M. Pérez-Domínguez, E.A. Cabrera-Reyes, T. Morales, M. Cerbón, Prolactin mediates neuroprotection against excitotoxicity in primary cell cultures of hippocampal neurons via its receptor. Brain Res. 1636, 192–199 (2016)

    Article  CAS  Google Scholar 

  115. N.V. Emanuele, L. Metcalfe, L. Wallock, J. Tentler, T.C. Hagen, C.T. Beer, D. Martinson, P.W. Gout, L. Kirsteins, A.M. Lawrence, Extrahyponthalamic brain prolactin: characterization and evidence for independence from pituitary prolactin. Brain Res. 421(1–2), 255–262 (1987)

    Article  CAS  PubMed  Google Scholar 

  116. H. Eichenbaum, Hippocampus: cognitive processes and neural representations that underlie declarative memory. Neuron 44(1), 109–120 (2004)

    Article  CAS  PubMed  Google Scholar 

  117. G. Love, N. Torrey, I. McNamara, M. Morgan, M. Banks, N. Hester, E.R. Glasper, A.C. Devries, C.H. Kinsley, K.G. Lambert, Maternal experience produces long-lasting behavioral modifications in the rat. Behav. Neurosci. 119(4), 1084–1096 (2005)

    Article  PubMed  Google Scholar 

  118. C.H. Kinsley, L. Madonia, G.W. Gifford, K. Tureski, G.R. Griffin, C. Lowry, J. Williams, J. Collins, H. McLearie, K.G. Lambert, Motherhood improves learning and memory. Nature 402(6758), 137–138 (1999)

    Article  CAS  PubMed  Google Scholar 

  119. J.L. Pawluski, B.L. Vanderbyl, K. Ragan, L.A. Galea, First reproductive experience persistently affects spatial reference and working memory in the mother and these effects are not due to pregnancy or “mothering” alone. Behav. Brain Res. 175(1), 157–165 (2006)

    Article  PubMed  Google Scholar 

  120. J.L. Pawluski, S.K. Walker, L.A. Galea, Reproductive experience differentially affects spatial reference and working memory performance in the mother. Horm. Behav. 49(2), 143–149 (2006)

    Article  PubMed  Google Scholar 

  121. J. Henry, B. Sherwin, Hormones and cognitive functioning during late pregnancy and postpartum: a longitudinal study. Behav. Neurosci. 126(1), 73–85 (2012)

    Article  CAS  PubMed  Google Scholar 

  122. T. Castanho, P. Moreira, C. Portugal-Nunes, A. Novais, P. Costa, J. Palha, N. Sousa, N.C. Santos, The role of sex and sex-related hormones in cognition, mood and well-being in older men and women. Biol. Psychol. 103, 158–166 (2014)

    Article  PubMed  Google Scholar 

  123. T.L. Walker, J. Vukovic, M.M. Koudijs, D.G. Blackmore, E.W. Mackay, A.M. Sykes, R.W. Overall, A.S. Hamlin, P.F. Bartlett, Prolactin stimulates precursor cells in the adult mouse hippocampus. PLoS One 7(9), 1–11 (2012)

    Article  CAS  Google Scholar 

  124. J. Reyes-Mendoza, T. Morales, Post-treatment with prolactin protects hippocampal CA1 neurons of the ovariectomized female rat against kainic acid-induced neurodegeneration. Neuroscience 328, 58–68 (2016)

    Article  CAS  PubMed  Google Scholar 

  125. J.L. Pawluski, L.A. Galea, Reproductive experience alters hippocampal neurogenesis during the postpartum period in the dam. Neuroscience 149(1), 53–67 (2007)

    Article  CAS  PubMed  Google Scholar 

  126. G. Mak, S. Weiss, Paternal recognition of adult offspring mediated by newly generated CNS neurons. Nat. Neurosci. 13(6), 753–758 (2010)

    Article  CAS  PubMed  Google Scholar 

  127. G.V. Pardo, J.F. Goularte, A.L. Hoefel, A.L. de Castro, L.C. Kucharski, A. da Rosa Araujo, A.B.: Lucion, Effects of sleep restriction during pregnancy on the mother and fetuses in rats. Physiol. Behav. 1(155), 66–76 (2016)

    Article  CAS  Google Scholar 

  128. G. Mak, E. Enwere, C. Gregg, T. Pakarainen, M. Poutanen, I. Huhtaniemi, S. Weiss, Male pheromone-stimulated neurogenesis in the adult female brain: possible role in mating behavior. Nat. Neurosci. 10(8), 1003–1011 (2007)

    Article  CAS  PubMed  Google Scholar 

  129. E. Gould, B.S. McEwen, P. Tanapat, L.A. Galea, E. Fuchs, Neurogenesis in the dentate gyrus of the adult tree shrew is regulated by psychosocial stress and NMDA receptor activation. J. Neurosci. 17(7), 2492–2498 (1997)

    CAS  PubMed  Google Scholar 

  130. R.S. Duman, J. Malberg, S. Nakagawa, Regulation of adult neurogenesis by psychotropic drugs and stress. J. Pharmacol. Exp. Ther. 299(2), 401–407 (2001)

    CAS  PubMed  Google Scholar 

  131. E.A. Nimchinsky, B.L. Sabatini, K. Svoboda, Structure and function of dendritic spines. Annu. Rev. Physiol. 64, 313–353 (2001)

    Article  Google Scholar 

  132. C.H. Kinsley, R. Trainer, G. Stafisso-Sandoz, P. Quadros, L.K. Marcus, C. Hearon, E.A. Meyer, N. Hester, M. Morgan, F.J. Kozub, K.G. Lambert, Motherhood and the hormones of pregnancy modify concentrations of hippocampal neuronal dendritic spines. Horm. Behav. 49(2), 131–142 (2006)

    Article  CAS  PubMed  Google Scholar 

  133. J.L. Pawluski, L.A. Galea, Hippocampal morphology is differentially affected by reproductive experience in the mother. J. Neurobiol. 66(1), 71–81 (2006)

    Article  PubMed  Google Scholar 

  134. J. Brusco, R. Wittmann, M. de Azevedo, A. Lucion, C. Franci, M. Giovenardi, A.A. Rasia-Filho, Plasma hormonal profiles and dendritic spine density and morphology in the hippocampal CA1 stratum radiatum, evidenced by light microscopy, of virgin and postpartum female rats. Neurosci. Lett. 438(3), 346–350 (2008)

    Article  CAS  PubMed  Google Scholar 

  135. R. Abbud, G. Hoffman, M. Smith, Cortical refractoriness to N-methyl-D,L-aspartic acid (NMDA) stimulation in the lactating rat: recovery after pup removal and blockade of progesterone receptors. Brain Res. 604(1–2), 16–23 (1993)

    Article  CAS  PubMed  Google Scholar 

  136. C.A. Standley, N-methyl-D-aspartate receptor binding is altered and seizure potential reduced in pregnant rats. Brain Res. 844(1–2), 10–19 (1999)

    Article  CAS  PubMed  Google Scholar 

  137. P. Anborgh, C. Godin, M. Pampillo, G. Dhami, L. Dale, S. Cregan, R. Truant, S.S. Ferguson, Inhibition of metabotropic glutamate receptor signaling by the huntingtin-binding protein optineurin. J. Biol. Chem. 280(41), 34840–34848 (2005)

    Article  CAS  PubMed  Google Scholar 

  138. M.R. Hynd, H.L. Scott, P.R. Dodd, Glutamate-mediated excitotoxicity and neurodegeneration in Alzheimer’s disease. Neurochem. Int. 45(5), 583–595 (2004)

    Article  CAS  PubMed  Google Scholar 

  139. M. Doretto, M. Oliveira-e-Silva, D. Ferreira-Alves, S. Pires, N. Garcia-Cairasco, A. Reis, Effect of lactation on the expression of audiogenic seizures: association with plasma prolactin profiles. Epilepsy Res. 54, 109–121 (2003)

    Article  CAS  PubMed  Google Scholar 

  140. P. Berzaghi Mda, D. Amado, E. Cavalheiro, Pregnancy decreases the frequency of spontaneous recurrent seizures in rats with kainic acid lesions of the hippocampus. Epilepsy Res. 1(2), 142–144 (1987)

    Article  PubMed  Google Scholar 

  141. T. Morales, M. Lorenson, A.M. Walker, E. Ramos, Both prolactin (PRL) and a molecular mimic of phosphorylated PRL, S179D-PRL, protect the hippocampus of female rats against excitotoxicity. Neuroscience 258, 211–217 (2014)

    Article  CAS  PubMed  Google Scholar 

  142. N.A. Rivero-Segura, E. Flores-Soto, S. García de la Cadena, I. Coronado-Mares, J.C. Gomez-Verjan, D.G. Ferreira, E.A. Cabrera-Reyes, L.V. Lopes, L. Massieu, M.: Cerbón, Prolactin-induced neuroprotection against glutamate excitotoxicity is mediated by the reduction of [Ca2+]i overload and NF-κB activation. PLoS One 12(5), e0176910 (2017)

    Article  PubMed  PubMed Central  Google Scholar 

  143. A.M. Thomson, Neocortical layer 6, a review. Front. Neuroanat. 4, 13 (2010)

    PubMed  PubMed Central  Google Scholar 

  144. I.Y. Zhou, R.W. Chan, L.C. Ho, E.X. Wu, Longitudinal metabolic changes in the hippocampus and thalamus of the maternal brain revealed by proton magnetic resonance spectroscopy. Neurosci. Lett. 553, 170–175 (2013)

    Article  CAS  PubMed  Google Scholar 

  145. J. Broida, S.D. Michael, B. Svare, Plasmin prolactin levels are not related to the initiation, maintenance, and decline of postpartum aggression in mice. Behav. Neural. Biol. 32(1), 121–125 (1981)

    Article  CAS  PubMed  Google Scholar 

  146. M. Garland, B. Svare, Suckling stimulation modulates the maintenance of postpartum aggression in mice. Physiol. Behav. 44(3), 301–305 (1988)

    Article  CAS  PubMed  Google Scholar 

  147. O.J. Bosch, I.D. Neumann, Vasopressin released within the central amygdala promotes maternal aggression. Eur. J. Neurosci. 31(5), 883–891 (2010)

    Article  PubMed  Google Scholar 

  148. M. Davis, The role of the amygdala in fear and anxiety. Annu. Rev. Neurosci. 15, 353–375 (1992)

    Article  CAS  PubMed  Google Scholar 

  149. J. Allen, C. Allen, Role of the amygdaloid complexes in the stress-induced release of ACTH in the rat. Neuroendocrinology 15(3–4), 220–230 (1974)

    CAS  PubMed  Google Scholar 

  150. N. Donner, R. Bredewold, R. Maloumby, I. Neumann, Chronic intracerebral prolactin attenuates neuronal stress circuitries in virgin rats. Eur. J. Neurosci. 25(6), 1804–1814 (2007)

    Article  PubMed  Google Scholar 

  151. L. Torner, N. Toschi, A. Pohlinger, R. Landgraf, I.D. Neumann, Anxiolytic and anti-stress effects of brain prolactin: improved efficacy of antisense targeting of the prolactin receptor by molecular modeling. J. Neurosci. 21(9), 3207–3214 (2001)

    CAS  PubMed  Google Scholar 

  152. O. Picazo, A. Fernández-Guasti, Changes in experimental anxiety during pregnancy and lactation. Physiol. Behav. 54(2), 295–299 (1993)

    Article  CAS  PubMed  Google Scholar 

  153. D. Toufexis, S. Tesolin, N. Huang, C. Walker, Altered pituitary sensitivity to corticotropin-releasing factor and arginine vasopressin participates in the stress hyporesponsiveness of lactation in the rat. J. Neuroendocrinol. 11(10), 757–764 (1999)

    Article  CAS  PubMed  Google Scholar 

  154. L.D. Sanford, P. Nassar, R.J. Ross, J. Schulkin, A.R. Morrison, Prolactin microinjections into the amygdalar central nucleus lead to decreased NREM sleep. Sleep Res. Online 1, 109–113 (1998)

    CAS  PubMed  Google Scholar 

  155. X. Pi, J.L. Voogt, D.R. Grattan, Detection of prolactin receptor mRNA in the corpus striatum and substantia nigra of the rat. J. Neurosci. Res. 67(4), 551–558 (2002)

    Article  CAS  PubMed  Google Scholar 

  156. B.D. Palma, D.C. Hipolide, S. Tufik, Effects on prolactin secretion and binding to dopaminergic receptors in sleep-deprived lupus-prone mice. Braz. J. Med. Biol. Res. 42(3), 299–304 (2009)

    Article  CAS  PubMed  Google Scholar 

  157. P. Malven, Inhibition of prolactin release in conscious sheep following stimulation of nucleus accumbens and caudate nucleus. Neuroendocrinology 28(3), 160–168 (1979)

    Article  CAS  PubMed  Google Scholar 

  158. R.S.E. Brown, A.E. Herbison, D.R. Grattan, Differential changes in responses of hypothalamic and brainstem neuronal populations to prolactin during lactation in the mouse. Biol. Reprod. 84, 826–836 (2011)

    Article  CAS  PubMed  Google Scholar 

  159. L. Caligaris, S. Taleisnik, Involvement of neurones containing 5-hydroxytryptamine in the mechanism of prolactin release induced by oestrogen. J. Neuroendocrinol. 62(1), 25–33 (1974)

    CAS  Google Scholar 

  160. G.A. Jahn, R.P. Deis, Effect of serotonin antagonists on prolactin and progesterone secretion in rats: Evidence that the stimulatory and inhibitory actions of serotonin on prolactin release may be mediated through different receptors. J. Endocrinol. 117(3), 415–422 (1988)

    Article  CAS  PubMed  Google Scholar 

  161. A. Mistry, J.L. Voogt, Role of serotonin in nocturnal and diurnal surges of prolactin in the pregnant rat. Endocrinology 125(6), 2875–2880 (1989)

    Article  CAS  PubMed  Google Scholar 

  162. L. Paut-Pagano, R. Roky, J. Valatx, K. Kitahama, M. Jouvet, Anatomical distribution of prolactin-like immunoreactivity in the rat brain. Neuroendocrinology 58(6), 682–695 (1993)

    Article  CAS  PubMed  Google Scholar 

  163. M. Angoa-Pérez, D. Kuhn, Neuronal serotonin in the regulation of maternal behavior in rodents. Neurotransmitter 2, 615–625 (2015)

    Google Scholar 

  164. M.C. Popesco, A. Frostholm, K. Rejniak, A. Rotter, Digital transcriptome analysis in the aging cerebellum. Ann. N.Y. Acad. Sci. 1019, 58–63 (2004)

    Article  CAS  PubMed  Google Scholar 

  165. A.L. Barofsky, J. Taylor, V.J. Massari, Dorsal raphe-hypothalamic projections provide the stimulatory serotonergic input to suckling-induced prolactin release. Endocrinology 113(5), 1894–1903 (1983)

    Article  CAS  PubMed  Google Scholar 

  166. P. Eriksson, E. Perfilieva, T. Bjork-Eriksson, A. Alborn, C. Nordborg, D. Peterson, F.H. Gage, Neurogenesis in the adult human hippocampus. Nat. Med. 4(11), 1313–1317 (1998)

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

This work was supported by PAPIIT, UNAM grant (IN220315 and IN216817). PhD. Limon-Morales O. is recipient of a DGAPA, UNAM Post-doctoral Fellowship grant.

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Erika Alejandra Cabrera-Reyes and Ofelia Limón-Morales contributed equally to this work

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Cabrera-Reyes, E.A., Limón-Morales, O., Rivero-Segura, N.A. et al. Prolactin function and putative expression in the brain. Endocrine 57, 199–213 (2017). https://doi.org/10.1007/s12020-017-1346-x

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