Effects of prolactin deficiency during the early postnatal period on the development of maternal behavior in female rats: Mother's milk makes the difference

Hormones and Behavior

Volumn 56, Issue 3, 2009, Pages 281-291

  Melo, Angel I ^a   Pérez Ledezma, Mirsha ^a   Clapp, Carmen ^b   Arnold, Edith ^b   Rivera, José Carlos ^b   Fleming, Alison, S ^c  

^a CENTRO TLAXCALA DE BIOLOGÍA DE LA CONDUCTA   (Mexico)

^b UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

^c UNIVERSITY OF TORONTO   (Canada)

Author keywords

Bromocriptine; Development; Early life; Emotionality; Maternal behavior; Milk; Prolactin; Rat; Sensitization

Indexed keywords

BROMOCRIPTINE; PROLACTIN;

ADULT ANIMAL; ANIMAL EXPERIMENT; ARTICLE; BREAST MILK; CONTROLLED STUDY; FEMALE; HORMONE DEFICIENCY; HORMONE DETERMINATION; JUVENILE; LACTATION; LATENT PERIOD; LICKING; MATERNAL BEHAVIOR; NONHUMAN; OPEN FIELD TEST; PERINATAL PERIOD; PRIORITY JOURNAL; PROGENY; RAT; SENSITIZATION; WEIGHT GAIN;

AGING; ANIMALS; ANIMALS, NEWBORN; BROMOCRIPTINE; FEMALE; HORMONE ANTAGONISTS; LACTATION; MATERNAL BEHAVIOR; MILK; MOTHERS; MOTOR ACTIVITY; POSTPARTUM PERIOD; PROLACTIN; RATS; RATS, WISTAR; TIME FACTORS;

EID: 69349095943     PISSN: 0018506X     EISSN: 10956867     Source Type: Journal    
DOI: 10.1016/j.yhbeh.2009.06.005     Document Type: Article

References (73)

1. Afonso V.M., Grella S.L., Chatterjee D., and Fleming A.S. Previous maternal experience affects accumbal dopaminergic responses to pup-stimuli. Brain Res. 1198 (2008) 115-123
2. Afonso V.M., King S., Chatterjee D., and Fleming A.S. Hormones that increase maternal responsiveness affect accumbal dopaminergic responses to pup- and food-stimuli in the female rat. Horm. Behav. 56 (2009) 11-23
3. Beach F.A., and Jaynes J. Effects of early experience upon the behavior of animals. Psychol. Bull. 51 (1954) 239-263
4. Bridges R.S., Numan M., Ronsheim P.M., Mann P.E., and Lupini C.E. Central prolactin infusions stimulate maternal behavior in steroid-treated, nulliparous female rats. Proc. Natl. Acad. Sci. U. S. A. 87 (1990) 8003-8007
5. Bridges R.S., and Ronsheim P.M. Prolactin (PRL) regulation of maternal behavior in rats: bromocriptine treatment delays and PRL promotes the rapid onset of behavior. Endocrinology (Baltimore) 126 (1990) 837-848
6. Cajero-Juárez M., Avila B., Ochoa A., Garrido-Guerrero E., Varela-Echavarría A., Martínez de la Escalera G., and Clapp C. Immortalization of bovine umbilical vein endotelial cells: a model for the study of vascular endothelium. Eur. J. Cell. Biol. 81 (2002) 1-8
7. Crowley W.R., Shah G.V., Watanobe H., and Grosvenor C.E. Effects of neonatal exposure to estradiol on prolactin secretion and activity of the tuberoinfundibular dopamine system in young adulthood: comparison with neonatal prolactin deficiency. J. Endocrinol. 2 (1990) 19-24
8. Dueñas Z., Torner L., Carbacho A.M., Ochoa A., Gutierrez-Ospina G., López-Barrera F., Barrios F.A., Berger P., Martinez de la Escalera G., and Clapp C. Inhibition of rat corneal angiogenesis by 16-kDa prolactin and by endogenous prolactin-like molecules. Invest. Ophtalmol. Vis. Sci. 40 (1999) 2498-2505
9. Ellis L.A., and Picciano M.F. Bioactive and immunoreactive prolactin variants in human milk. Endocrinology 136 (1995) 2711-2720
10. Ellis L.A., Mastro A.M., and Picciano M.F. Milk-borne prolactin and neonatal development. J. Mam. Gland Biol. Neoplasia 1 (1996) 259-267
11. Fleming A.S., Kraemer G.W., Gonzalez A., Lovic V., Ress S., and Melo A. Mothering begets mothering: the transmission of behavior and its neurobiology across generations. Pharm. Biochem. Behav. 73 (2002) 61-75
12. Fleming A.S., O Day D.H., and Kraemer G.W. Neurobiology of mother-infant interactions: experience and central nervous system plasticity across development and generations. Neurosc. Biobehav. 23 (1999) 673-685
13. Fleming A.S., and Rosenblatt J.S. Maternal behavior in the virgin and lactating rat. J. Comp. Physiol. Psychol. 86 (1974) 957-972
14. Freeman M.E., Kanyicska B., Lerant A., and Nagy G. Prolactin: structure, function, and regulation of secretion. Physiol. Rev. 80 (2000) 1523-1631
15. Freemark M., Driscoll P., Andrews J., Kelly P.A., and Royster M. Ontogenesis of prolactin receptor gene expression in the rat olfactory system: potential roles for lactogenic hormones in olfactory development. Endocrinology 137 (1996) 934-942
16. Gala R.R., Forsyth I.A., and Turvey A. Milk prolactin is biologically active. Life Sci. 26 (1980) 987-993
17. Gala R.R., and Shevach E.M. Influence of bromocriptine administration to the mothers on the development of pup thymocyte and splenocyte subsets and on mitogen-induced proliferation in the mouse. Life Sci. 53 (1993) 1981-1994
18. Galler J.R., and Propert K.J. Maternal behavior following rehabilitation of rats with intergenerational malnutrition. 1. Persistent changes in lactation-related behaviors. J. Nutr. 111 (1981) 1330-1336
19. Gonella P., Harnatz P., and Walker Q.A. Prolactin is transported across the epithelium of the jejunum and ileum of suckling rat. J. Cell Physiol. 140 (1989) 138-149
20. Gonzalez A., and Fleming A.S. Artificial rearing causes changes in maternal behavior and c-fos expression in juvenile female rats. Behav. Neurosci. 116 (2002) 999-1013
21. Gonzalez A., Lovic V., Ward G.R., Wainwright P.E., and Fleming A.S. Intergenerational effects of complete maternal deprivation and replacement stimulation on maternal behavior and emotionality in female rats. Dev. Psychobiol. 38 (2001) 11-32
22. González-Mariscal G., and Poindron P. Parental care in mammals: immediate internal and sensory factors of control. In: Pfaff D., Arnold A.P., Etgen A.M., Fahrbach S.E., and Rubin R.T. (Eds). Horm. Brain Behav. 1st ed. Vol 1 (2002), Academic Press, San Diego 215-298 Chap. 3
23. Grosvenor C.E., Picciano M.F., and Baumrucker C.R. Hormones and growth factors in milk. Endocr. Rev. 14 (1992) 710-728
24. Grosvenor C.E., and Whitworth N.S. Incorporation of rat prolactin into rat milk in vivo and in vitro. Endocrinology 70 (1976) 71-79
25. Grove D.S., Bour B., Kacsoh B., and Mastro A.M. Effect of neonatal milk-prolactin deprivation on the ontogeny of the immune system. Endocr. Regul. 25 (1991) 111-119
26. Gudelsky G.A., and Porter J.C. Release of dopamine from tuberoinfundibular neurons into pituitary stalk blood after prolactin or haloperidol administration. Endocrinology 106 (1995) 526-529
27. Hall F.S. Social deprivation of neonatal, adolescent, and adult rats has distinct neurochemical and behavioral consequences. Crit. Rev. Neurobiol. 12 (1998) 129-162
28. Hoeffler J.P., Boockfor F.R., and Frawley L.S. Ontogeny of prolactin cells in neonatal rats: initial prolactin secretors also release growth hormone. Endocrinology 117 (1985) 187-195
29. Hofer M.A. Hidden regulatory processes in early social relationships. In: Bateson P.P.G., and Klopfer P.H. (Eds). Perspectives in Ethology (1978), Plenum Press, New York City
30. Hofer M.A. Early relationships as regulators of infant physiology and behavior. Acta Pediatr. Suppl. 397 (1994) 9-18
31. Jakubowski M., and Terkel J. Transition from pup killing to parental behavior in male and virgin female albino rats. Physiol. Behav. 34 (1985) 683-686
32. Jouan P.-N., Pouliot Y., Gauthier S.F., and Laforest J.-P. Hormones in bovine milk and milk products: a survey. Int. Dairy J. 16 (2006) 1408-1414
33. Kacsoh B., Toth B.E., Avery L.M., Yamamuro Y., and Grosvenor C.E. Molecular heterogeneity of prolactin in lactating rats and their pups: biological and immunological activities in pituitary gland, serum and milk. Endocr. Regul. 25 (1991) 98-110
34. Kacsoh B., Veress Z., Toth B.E., Avery L.M., and Grosvenor C.E. Bioactive and immunoreactive variants of prolactin in milk and serum of lactating rats and their pups. J. Endocrinol. 138 (1993) 243-257
35. Karabulut A., and Pratten M.K. Species-specific of growth-promoting effects of prolactin during rat embryogenesis. J. Anat. 192 (1998) 1-12
36. Kinsley C.H., and Bridges R.S. Prolactin modulation of the maternal-like behavior displayed by juvenile rats. Horm. Behav. 22 (1988) 49-65
37. Koldovsky O. The potential physiological significance of milk-borne hormonally active substances for the neonate. J. Mam. Gland Biol. Neoplasia 1 (1996) 317-323
38. Lamb M.E. Physiological mechanisms in the control of maternal behavior in rats: a review. Psychol. Bull. 82 (1975) 104-119
39. Lerant A., and Freeman M.E. Ovarian steroids differentially regulate the expression of PRL-R in neuroendocrine dopaminergic neuron populations: a double label confocal microscopic study. Brain Res. 802 (1998) 141-154
40. Levine S., Haltmeyer G.C., Karas G.G., and Denenberg V.H. Physiological and behavioral effects of infantile stimulation. Physiol. Behav. 2 (1967) 55-59
41. Levy F., Melo A.I., Galef B.G., Madden M., and Fleming A.S. Complete maternal deprivation affects social but not spatial learning in adult rats. Dev. Psychobiol. 43 (2003) 177-191
42. Lkhider M., Delpal S., and Bousquet M.O. Rat prolactin in serum, milk, and mammary tissue: characterization and intracellular localization. Endocrinology 137 (1996) 4969-4979
43. Lovic V., Gonzalez A., and Fleming A.S. Maternally separated rats show deficits in maternal care in adulthood. Dev. Psychobiol. 39 (2001) 19-33
44. Lovic V., and Fleming A.S. Artificially-reared female rats show reduced prepulse inhibition and deficits in the attentional set shifting task-reversal of effects with maternal-like licking stimulation. Behav. Brain Res. 148 (2004) 209-219
45. Marinari K.T., and Moltz H. Serum prolactin levels and vaginal cyclicity in concaveated and lactating female rats. Physiol. Behav. 21 (1978) 525-528
46. McMurtry J.P., and Malven P.V. Radioimmunoassay for endogenous and exogenous prolactin in milk of rats. J. Endocrinol. 61 (1974) 211-217
47. McMurtry J.P., and Malven P.V. Experimental alterations in prolactin levels in goat milk and blood plasma. Endocrinology 95 (1974) 559-564
48. Melo A.I., Hernández-Curiel M., and Hoffman K.L. Maternal and peer contact during the postnatal period participate in the normal development of maternal aggression, maternal behavior, and the behavioral response to novelty. Behav. Brain Res. 201 (2009) 14-21
49. Melo A.I., Lovic V., Gonzalez A., Madden M., Sinopoli K., and Fleming A.S. Maternal and littermate deprivation disrupts maternal behavior and social-learning of food preference in adulthood: tactile stimulation, nest odor, and social rearing prevent these effects. Dev. Psychobiol. 48 (2006) 209-219
50. Möderscheim T.A., Gorba T., Pathipati P., Kokay C., Grattan D.R., Williams C.E., and Scheepens A. Prolactin is involved in glial responses following a focal injury to the juvenile rat brain. Neuroscience 145 (2007) 963-973
51. Mulloy A.L., and Malven P.V. Relationships between concentrations of porcine prolactin in blood serum and milk of lactating sows. J. Anim. Sci. 48 (1979) 876-881
52. Numan M., and Insel T.R. The Neurobiology of Parental Behavior. Hormones, Brain, and Behavior (2003), Springer-Verlag New York, Inc. 12-17
53. Numan M., and Stolzenberg D.S. Medial preoptic area interactions with dopamine neural systems in the control of the onset and maintenance of maternal behavior in rats. Front. Neuroendocrinol. 30 (2009) 46-64
54. Peters F., Geisthövel F., and Breckwoldt M. Serum prolactin levels in woman with excessive milk production. Normalization by transitory prolactin inhibition. Acta Endocrinol. (Copenh) 109 (1985) 463-466
55. Rees S.L., Akbari E., Steiner M., and Fleming A.S. Effects of early deprivation and maternal separation on pup-directed behavior and HPA axis measures in the juvenile female rat. Dev. Psychobiol. 50 (2008) 315-321
56. Rees S.L., and Fleming A.S. How early separation and juvenile experience with pups affect maternal behavior and emotionality in adult postpartum rats. Anim. Learn. Behav. 29 (2001) 221-233
57. Rosenblatt J.S. Nonhormonal basis of maternal behavior in the rat. Science 156 (1967) 1512-1514
58. Rosenblatt J.S., and Lehrman D.S. Maternal Behavior in the Laboratory Rat. In: Rheingold H.L. (Ed) (1963), Maternal Behavior in Mammals, New York Wiley
59. Royster M., Driscoll P., Kelly P.A., and Freemark M. 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 (1995) 3892-3900
60. Sakaguchi K., Tanaka M., Ohkuo T., Doh-ura K., Fujikawa T., Sudo S., and Nakashima K. Induction of brain prolactin receptor long-form RNAm expression and maternal behavior in pup-contacted male rats: promotion by prolactin administration and suppression by female contact. Neuroendocrinology 63 (1996) 559-568
61. Salas M., Torrero C., and Pulido S. Long-term alterations in the maternal behavior of neonatally undernourished rats. Physiol. Behav. 33 (1984) 273-278
62. Shah V., Shyr S.W., Grosvenor C.E., and Crowley W.R. Hyperprolactinemia after neonatal prolactin (PRL) deficiency in rats: evidence for altered anterior pituitary regulation of PRL secretion. Endocrinology 122 (1988) 1883-1889
63. Shieh K.R.P. Stimulatory role of prolactin on the development of tuberoinfundibular dopaminergic neurones in prepubertal female rats: studies with cysteamine and somatostatin. J. Neuroendocrinology 11 (1999) 907-917
64. Shingo T., Gregg C., Enwere E., Fujikawa H., Hassam R., Geary C., Cross J.C., and Weiss S. Pregnancy-stimulated neurogenesis in the adult female forebrain mediate by prolactin. Science 299 (2003) 117-120
65. Shyr S.W., Crowley W.R., and Grosvenor C.E. Effect of neonatal prolactin deficiency on prepubertal tuberoinfundibular and tuberohypophyseal dopaminergic neuronal activity. Endocrinology 119 (1986) 1217-1221
66. Sinha Y.N., and Vanderlaan W.P. Effect on growth of prolactin deficiency induced in infant mice. Endocrinology 110 (1982) 1871-1878
67. Stern J.M. Offspring-induced nurturance: animal-human parallels. Dev. Psychobiol. 31 (1997) 19-37
68. Tanaka T., Shiu R.P., Gout P.W., Beer C.T., Noble R.L., and Friesen H.G. A new sensitive and specific bioassay for lactogenic hormones: measurement of prolactin and growth hormone in human serum. J. Clin. Endocrinol. Metab. 51 (1980) 1058-1063
69. Torner L., Toschi N., Pohlinger A., Landgraf R., and Neumann D. Anxiolytic and anti-stress effects of brain prolactin: improved efficacy of antisense targeting of the prolactin receptor by molecular modeling. J. Neurosci. 21 (2001) 3207-3214
70. Vorbrodt A.W. Morphological evidence of the functional polarization of brain microvascular epithelium. In: Pardridge W.M. (Ed). The Blood-brain Barrier (1993), Raven Press, New York 137-164
71. Yrigollen C.M., Han S.S., Kochetkova A., Babitz T., Chang J.T., Volkmar F.R., Leckman J.F., and Grigorenko E.L. Genes controlling affiliative behavior as candidate genes for autism. Biol. Psychiatry 63 (2008) 911-916
72. Whitworth N.S., and Grosvenor C.E. Transfer of milk prolactin to the plasma of neonatal rats by intestinal absorption. J. Endocr. 79 (1978) 191-199
73. Wiesner B.P., and Sheard N.M. Maternal behavior in the rat (1933), Oliver and Boyd, Edinburgh, London