Experience-facilitated improvements in pup retrieval; evidence for an epigenetic effect

Hormones and Behavior

Volumn 62, Issue 2, 2012, Pages 128-135

  Stolzenberg, Danielle S ^a   Stevens, Jacqueline S ^a   Rissman, Emilie F ^a  

^a UNIVERSITY OF VIRGINIA   (United States)

Author keywords

CBP; Epigenetics; HDAC inhibition; Maternal experience; Oxytocin; Sodium butyrate

Indexed keywords

BUTYRIC ACID; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN BINDING PROTEIN; ESTROGEN RECEPTOR BETA; OXYTOCIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CREBBP GENE; EPIGENETICS; ESR2 GENE; EXPERIENCE; FEMALE; GENE EXPRESSION; MATERNAL BEHAVIOR; MEDIAL PREOPTIC AREA; MOTHER CHILD RELATION; MOUSE; NONHUMAN; OXT GENE; PRIORITY JOURNAL;

ANIMALS; ANIMALS, NEWBORN; BEHAVIOR, ANIMAL; BUTYRATES; EPIGENESIS, GENETIC; EXPLORATORY BEHAVIOR; FEMALE; GENE EXPRESSION REGULATION; HISTONE DEACETYLASE INHIBITORS; LEARNING; MATERNAL BEHAVIOR; MICE; MICE, INBRED C57BL; PREGNANCY;

EID: 84864322436     PISSN: 0018506X     EISSN: 10956867     Source Type: Journal    
DOI: 10.1016/j.yhbeh.2012.05.012     Document Type: Article

References (102)

1. Afonso V.M., King S., Chatterjee D., Fleming A.S. Hormones that increase maternal responsiveness affect accumbal dopaminergic responses to pup- and food-stimuli in the female rat. Horm. Behav. 2009, 56:11-23.
2. Alarcon J.M., Malleret G., Touzani K., Vronskaya S., Ishii S., Kandel E.R., Barco A. Chromatin acetylation, memory, and LTP are impaired in CBP+/- mice: a model for the cognitive deficit in Rubinstein-Taybi syndrome and its amelioration. Neuron 2004, 42:947-959.
3. Arrati P.G., Carmona C., Dominguez G., Beyer C., Rosenblatt J.S. GABA receptor agonists in the medial preoptic area and maternal behavior in lactating rats. Physiol. Behav. 2006, 87:51-65.
4. Benoit D., Parker K.C. Stability and transmission of attachment across three generations. Child Dev. 1994, 65:1444-1456.
5. Bonthuis P.J., Patteson J.K., Rissman E.F. Acquisition of sexual receptivity: roles of chromatin acetylation, estrogen receptor-alpha, and ovarian hormones. Endocrinology 2011, 152:3172-3181.
6. Bosch O.J., Pfortsch J., Beiderbeck D.I., Landgraf R., Neumann I.D. Maternal behaviour is associated with vasopressin release in the medial preoptic area and bed nucleus of the stria terminalis in the rat. J. Neuroendocrinol. 2010, 22:420-429.
7. Bouchal J., Santer F.R., Hoschele P.P., Tomastikova E., Neuwirt H., Culig Z. Transcriptional coactivators p300 and CBP stimulate estrogen receptor-beta signaling and regulate cellular events in prostate cancer. Prostate 2011, 71:431-437.
8. Bridges R.S. Long-term effects of pregnancy and parturition upon maternal responsiveness in the rat. Physiol. Behav. 1975, 14:245-249.
9. Bridges R.S. Parturition: its role in the long term retention of maternal behavior in the rat. Physiol. Behav. 1977, 18:487-490.
10. Bridges R.S. Retention of rapid onset of maternal behavior during pregnancy in primiparous rats. Behav. Biol. 1978, 24:113-117.
11. Buranasin B. The effects of rooming-in on the success of breastfeeding and the decline in abandonment of children. Asia Pac. J. Public Health 1991, 5:217-220.
12. Burns M.J., Nixon G.J., Foy C.A., Harris N. Standardisation of data from real-time quantitative PCR methods - evaluation of outliers and comparison of calibration curves. BMC Biotechnol. 2005, 5:31.
13. Bystrova K., Ivanova V., Edhborg M., Matthiesen A.S., Ransjo-Arvidson A.B., Mukhamedrakhimov R., Uvnas-Moberg K., Widstrom A.M. Early contact versus separation: effects on mother-infant interaction one year later. Birth 2009, 36:97-109.
14. Calamandrei G., Keverne E.B. Differential expression of Fos protein in the brain of female mice dependent on pup sensory cues and maternal experience. Behav. Neurosci. 1994, 108:113-120.
15. Champagne F.A., Curley J.P. Maternal regulation of estrogen receptor alpha methylation. Curr. Opin. Pharmacol. 2008, 8:735-739.
16. Champagne F., Diorio J., Sharma S., Meaney M.J. Naturally occurring variations in maternal behavior in the rat are associated with differences in estrogen-inducible central oxytocin receptors. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:12736-12741.
17. Champagne F.A., Weaver I.C., Diorio J., Sharma S., Meaney M.J. Natural variations in maternal care are associated with estrogen receptor alpha expression and estrogen sensitivity in the medial preoptic area. Endocrinology 2003, 144:4720-4724.
18. Champagne F.A., Weaver I.C., Diorio J., Dymov S., Szyf M., Meaney M.J. Maternal care associated with methylation of the estrogen receptor-alpha1b promoter and estrogen receptor-alpha expression in the medial preoptic area of female offspring. Endocrinology 2006, 147:2909-2915.
19. Chapman D., Scott K. The impact of maternal intergenerational risk factors on adverse developmental outcomes. Dev. Rev. 2001, 305-325.
20. Cheung E., Schwabish M.A., Kraus W.L. Chromatin exposes intrinsic differences in the transcriptional activities of estrogen receptors alpha and beta. EMBO J. 2003, 22:600-611.
21. Covington H.E., Maze I., LaPlant Q.C., Vialou V.F., Ohnishi Y.N., Berton O., Fass D.M., Renthal W., Rush A.J., Wu E.Y., Ghose S., Krishnan V., Russo S.J., Tamminga C., Haggarty S.J., Nestler E.J. Antidepressant actions of histone deacetylase inhibitors. J. Neurosci. 2009, 29:11451-11460.
22. D'Cunha T.M., King S.J., Fleming A.S., Levy F. Oxytocin receptors in the nucleus accumbens shell are involved in the consolidation of maternal memory in postpartum rats. Horm. Behav. 2010, 59:14-21.
23. Duong V., Licznar A., Margueron R., Boulle N., Busson M., Lacroix M., Katzenellenbogen B.S., Cavailles V., Lazennec G. ERalpha and ERbeta expression and transcriptional activity are differentially regulated by HDAC inhibitors. Oncogene 2006, 25:1799-1806.
24. Ehret G., Buckenmaier J. Estrogen-receptor occurrence in the female mouse brain: effects of maternal experience, ovariectomy, estrogen and anosmia. J. Physiol. Paris 1994, 88:315-329.
25. Erlandsson K., Dsilna A., Fagerberg I., Christensson K. Skin-to-skin care with the father after cesarean birth and its effect on newborn crying and prefeeding behavior. Birth 2007, 34:105-114.
26. Fahrbach S.E., Morrell J.I., Pfaff D.W. Effect of varying the duration of pre-test cage habituation on oxytocin induction of short-latency maternal behavior. Physiol. Behav. 1986, 37:135-139.
27. Febo M., Numan M., Ferris C.F. Functional magnetic resonance imaging shows oxytocin activates brain regions associated with mother-pup bonding during suckling. J. Neurosci. 2005, 25:11637-11644.
28. Fleming A.S., Korsmit M. Plasticity in the maternal circuit: effects of maternal experience on Fos-Lir in hypothalamic, limbic, and cortical structures in the postpartum rat. Behav. Neurosci. 1996, 110:567-582.
29. Fleming A.S., Miceli M., Moretto D. Lesions of the medial preoptic area prevent the facilitation of maternal behavior produced by amygdala lesions. Physiol. Behav. 1983, 31:503-510.
30. Fleming A.S., Korsmit M., Deller M. Rat pups are potent reinforcers to the maternal animal: effects of experience, parity, hormones, and dopamine function. Psychobiology 1994, 22:44-53.
31. Fleming A.S., O'Day D.H., Kraemer G.W. Neurobiology of mother-infant interactions: experience and central nervous system plasticity across development and generations. Neurosci. Biobehav. Rev. 1999, 23:673-685.
32. Gammie S.C., Hasen N.S., Awad T.A., Auger A.P., Jessen H.M., Panksepp J.B., Bronikowski A.M. Gene array profiling of large hypothalamic CNS regions in lactating and randomly cycling virgin mice. Brain Res. Mol. Brain Res. 2005, 139:201-211.
33. Gandelman R. Maternal behavior in the mouse: effect of estrogen and progesterone. Physiol. Behav. 1973, 10:153-155.
34. Gandelman R. The ontogeny of maternal responsiveness in female Rockland-Swiss albino mice. Horm. Behav. 1973, 4:257-268.
35. Gandelman R., Vom Saal F.S. Pup-killing in mice: the effects of gonadectomy and testosterone administration. Physiol. Behav. 1975, 15:647-651.
36. Giordano A.L., Siegel H.I., Rosenblatt J.S. Nuclear estrogen receptor binding in the preoptic area and hypothalamus of pregnancy-terminated rats: correlation with the onset of maternal behavior. Neuroendocrinology 1989, 50:248-258.
37. Gray P., Brooks P.J. Effect of lesion location within the medial preoptic-anterior hypothalamic continuum on maternal and male sexual behaviors in female rats. Behav. Neurosci. 1984, 98:703-711.
38. Gundersen B.B., Blendy J.A. Effects of the histone deacetylase inhibitor sodium butyrate in models of depression and anxiety. Neuropharmacology 2009, 57:67-74.
39. Jacobson C.D., Terkel J., Gorski R.A., Sawyer C.H. Effects of small medial preoptic area lesions on maternal behavior: retrieving and nest building in the rat. Brain Res. 1980, 194:471-478.
40. Jin S.H., Blendy J.A., Thomas S.A. Cyclic AMP response element-binding protein is required for normal maternal nurturing behavior. Neuroscience 2005, 133:647-655.
41. Kalinichev M., Rosenblatt J.S., Morrell J.I. The medial preoptic area, necessary for adult maternal behavior in rats, is only partially established as a component of the neural circuit that supports maternal behavior in juvenile rats. Behav. Neurosci. 2000, 114:196-210.
42. Kendrick K.M., Da Costa A.P., Broad K.D., Ohkura S., Guevara R., Levy F., Keverne E.B. Neural control of maternal behaviour and olfactory recognition of offspring. Brain Res. Bull. 1997, 44:383-395.
43. Kennell J.H., Klaus M.H. Bonding: recent observations that alter perinatal care. Pediatr. Rev. 1998, 19:4-12.
44. Kennell J.H., Jerauld R., Wolfe H., Chesler D., Kreger N.C., McAlpine W., Steffa M., Klaus M.H. Maternal behavior one year after early and extended post-partum contact. Dev. Med. Child Neurol. 1974, 16:172-179.
45. Kim M.Y., Hsiao S.J., Kraus W.L. A role for coactivators and histone acetylation in estrogen receptor alpha-mediated transcription initiation. EMBO J. 2001, 20:6084-6094.
46. Kim P., Leckman J.F., Mayes L.C., Feldman R., Wang X., Swain J.E. The plasticity of human maternal brain: longitudinal changes in brain anatomy during the early postpartum period. Behav. Neurosci. 2010, 124:695-700.
47. Klaus M.H., Jerauld R., Kreger N.C., McAlpine W., Steffa M., Kennel J.H. Maternal attachment. Importance of the first post-partum days. N. Engl. J. Med. 1972, 286:460-463.
48. Korzus E., Rosenfeld M.G., Mayford M. CBP histone acetyltransferase activity is a critical component of memory consolidation. Neuron 2004, 42:961-972.
49. Kuroda K.O., Meaney M.J., Uetani N., Fortin Y., Ponton A., Kato T. ERK-FosB signaling in dorsal MPOA neurons plays a major role in the initiation of parental behavior in mice. Mol. Cell. Neurosci. 2007, 36:121-131.
50. Kuroda K.O., Meaney M.J., Uetani N., Kato T. Neurobehavioral basis of the impaired nurturing in mice lacking the immediate early gene FosB. Brain Res. 2008, 1211:57-71.
51. Laplant Q., Nestler E.J. CRACKing the histone code: cocaine's effects on chromatin structure and function. Horm. Behav. 2010, 59:321-330.
52. Larsen C.M., Kokay I.C., Grattan D.R. Male pheromones initiate prolactin-induced neurogenesis and advance maternal behavior in female mice. Horm. Behav. 2008, 53:509-517.
53. Lee A.W., Brown R.E. Comparison of medial preoptic, amygdala, and nucleus accumbens lesions on parental behavior in California mice (Peromyscus californicus). Physiol. Behav. 2007, 92:617-628.
54. Lee A., Clancy S., Fleming A.S. 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. 2000, 108:215-231.
55. Leussis M.P., Bond T.L., Hawken C.M., Brown R.E. Attenuation of maternal behavior in virgin CD-1 mice by methylphenidate hydrochloride. Physiol. Behav. 2008, 95:395-399.
56. Levenson J.M., Sweatt J.D. Epigenetic mechanisms in memory formation. Nat. Rev. Neurosci. 2005, 6:108-118.
57. Levenson J.M., O'Riordan K.J., Brown K.D., Trinh M.A., Molfese D.L., Sweatt J.D. Regulation of histone acetylation during memory formation in the hippocampus. J. Biol. Chem. 2004, 279:40545-40559.
58. Lucas B.K., Ormandy C.J., Binart N., Bridges R.S., Kelly P.A. Null mutation of the prolactin receptor gene produces a defect in maternal behavior. Endocrinology 1998, 139:4102-4107.
59. Macbeth A.H., Stepp J.E., Lee H.J., Young W.S., Caldwell H.K. Normal maternal behavior, but increased pup mortality, in conditional oxytocin receptor knockout females. Behav. Neurosci. 2010, 124:677-685.
60. Malvaez M., Sanchis-Segura C., Vo D., Lattal K.M., Wood M.A. Modulation of chromatin modification facilitates extinction of cocaine-induced conditioned place preference. Biol. Psychiatry 2010, 67:36-43.
61. Mann M.A., Kinsley C., Broida J., Svare B. Infanticide exhibited by female mice: genetic, developmental and hormonal influences. Physiol. Behav. 1983, 30:697-702.
62. McLeod J., Sinal C.J., Perrot-Sinal T.S. Evidence for non-genomic transmission of ecological information via maternal behavior in female rats. Genes Brain Behav. 2007, 6:19-29.
63. Meddle S.L., Bishop V.R., Gkoumassi E., van Leeuwen F.W., Douglas A.J. Dynamic changes in oxytocin receptor expression and activation at parturition in the rat brain. Endocrinology 2007, 148:5095-5104.
64. Mifsud K.R., Gutierrez-Mecinas M., Trollope A.F., Collins A., Saunderson E.A., Reul J.M. Epigenetic mechanisms in stress and adaptation. Brain Behav. Immun. 2011, 25:1305-1315.
65. Minamiyama M., Katsuno M., Adachi H., Waza M., Sang C., Kobayashi Y., Tanaka F., Doyu M., Inukai A., Sobue G. Sodium butyrate ameliorates phenotypic expression in a transgenic mouse model of spinal and bulbar muscular atrophy. Hum. Mol. Genet. 2004, 13:1183-1192.
66. Nephew B.C., Bridges R.S., Lovelock D.F., Byrnes E.M. Enhanced maternal aggression and associated changes in neuropeptide gene expression in multiparous rats. Behav. Neurosci. 2009, 123:949-957.
67. Noirot E. The onset of maternal behavior in rat, hamsters and mice. Advances in the Study of Behavior 1972, 107-145. Academic Press, New York. D.S. Lehrman, R.A. Hinde, E. Shaw (Eds.).
68. Numan M. Medial preoptic area and maternal behavior in the female rat. J. Comp. Physiol. Psychol. 1974, 87:746-759.
69. Numan M. Hypothalamic neural circuits regulating maternal responsiveness toward infants. Behav. Cogn. Neurosci. Rev. 2006, 5:163-190.
70. Numan M., Callahan E.C. The connections of the medial preoptic region and maternal behavior in the rat. Physiol. Behav. 1980, 25:653-665.
71. Numan M., Numan M.J. Expression of Fos-like immunoreactivity in the preoptic area of maternally behaving virgin and postpartum rats. Behav. Neurosci. 1994, 108:379-394.
72. Numan M., Numan M.J. Importance of pup-related sensory inputs and maternal performance for the expression of Fos-like immunoreactivity in the preoptic area and ventral bed nucleus of the stria terminalis of postpartum rats. Behav. Neurosci. 1995, 109:135-149.
73. Numan M., Numan M.J. Projection sites of medial preoptic area and ventral bed nucleus of the stria terminalis neurons that express Fos during maternal behavior in female rats. J. Neuroendocrinol. 1997, 9:369-384.
74. Numan M.I., Insel T.R. The Neurobiology of Parental Behavior 2003, Springer-Verlag, New York.
75. Numan M., Rosenblatt J.S., Komisaruk B.R. Medial preoptic area and onset of maternal behavior in the rat. J. Comp. Physiol. Psychol. 1977, 91:146-164.
76. Numan M., Corodimas K.P., Numan M.J., Factor E.M., Piers W.D. Axon-sparing lesions of the preoptic region and substantia innominata disrupt maternal behavior in rats. Behav. Neurosci. 1988, 102:381-396.
77. Numan M., Numan M.J., Marzella S.R., Palumbo A. Expression of c-fos, fos B, and egr-1 in the medial preoptic area and bed nucleus of the stria terminalis during maternal behavior in rats. Brain Res. 1998, 792:348-352.
78. O'Connor S., Vietze P.M., Sherrod K.B., Sandler H.M., Altemeier W.A. Reduced incidence of parenting inadequacy following rooming-in. Pediatrics 1980, 66:176-182.
79. Ogawa S., Eng V., Taylor J., Lubahn D.B., Korach K.S., Pfaff D.W. Roles of estrogen receptor-alpha gene expression in reproduction-related behaviors in female mice. Endocrinology 1998, 139:5070-5081.
80. Ogawa S., Chan J., Chester A.E., Gustafsson J.A., Korach K.S., Pfaff D.W. Survival of reproductive behaviors in estrogen receptor beta gene-deficient (betaERKO) male and female mice. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:12887-12892.
81. Okabe S., Nagasawa M., Kihara T., Kato M., Harada T., Koshida N., Mogi K., Kikusui T. The effects of social experience and gonadal hormones on retrieving behavior of mice and their responses to pup ultrasonic vocalizations. Zoolog. Sci. 2011, 27:790-795.
82. Orpen B.G., Fleming A.S. Experience with pups sustains maternal responding in postpartum rats. Physiol. Behav. 1987, 40:47-54.
83. Orpen B.G., Furman N., Wong P.Y., Fleming A.S. Hormonal influences on the duration of postpartum maternal responsiveness in the rat. Physiol. Behav. 1987, 40:307-315.
84. Patisaul H.B., Scordalakes E.M., Young L.J., Rissman E.F. Oxytocin, but not oxytocin receptor, is rRegulated by oestrogen receptor beta in the female mouse hypothalamus. J. Neuroendocrinol. 2003, 15:787-793.
85. Pedersen C.A., Caldwell J.D., Walker C., Ayers G., Mason G.A. Oxytocin activates the postpartum onset of rat maternal behavior in the ventral tegmental and medial preoptic areas. Behav. Neurosci. 1994, 108:1163-1171.
86. Pedersen C.A., Vadlamudi S.V., Boccia M.L., Amico J.A. Maternal behavior deficits in nulliparous oxytocin knockout mice. Genes Brain Behav. 2006, 5:274-281.
87. Pederson D.R., Gleason K.E., Moran G., Bento S. Maternal attachment representations, maternal sensitivity, and the infant-mother attachment relationship. Dev. Psychol. 1998, 34:925-933.
88. Ragnauth A.K., Devidze N., Moy V., Finley K., Goodwillie A., Kow L.M., Muglia L.J., Pfaff D.W. Female oxytocin gene-knockout mice, in a semi-natural environment, display exaggerated aggressive behavior. Genes Brain Behav. 2005, 4:229-239.
89. Riccio A. Dynamic epigenetic regulation in neurons: enzymes, stimuli and signaling pathways. Nat. Neurosci. 2010, 13:1330-1337.
90. Roozendaal B., Hernandez A., Cabrera S.M., Hagewoud R., Malvaez M., Stefanko D.P., Haettig J., Wood M.A. Membrane-associated glucocorticoid activity is necessary for modulation of long-term memory via chromatin modification. J. Neurosci. 2010, 30:5037-5046.
91. Scanlan V.F., Byrnes E.M., Bridges R.S. Reproductive experience and activation of maternal memory. Behav. Neurosci. 2006, 120:676-686.
92. Seifritz E., Di Salle F., Esposito F., Bilecen D., Neuhoff J.G., Scheffler K. Sustained blood oxygenation and volume response to repetition rate-modulated sound in human auditory cortex. NeuroImage 2003, 20:1365-1370.
93. Stack E.C., Balakrishnan R., Numan M.J., Numan M. A functional neuroanatomical investigation of the role of the medial preoptic area in neural circuits regulating maternal behavior. Behav. Brain Res. 2002, 131:17-36.
94. Stefanko D.P., Barrett R.M., Ly A.R., Reolon G.K., Wood M.A. Modulation of long-term memory for object recognition via HDAC inhibition. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:9447-9452.
95. Stern J.M., Mackinnon D.A. Postpartum, hormonal, and nonhormonal induction of maternal behavior in rats: effects on T-maze retrieval of pups. Horm. Behav. 1976, 7:305-316.
96. Stolzenberg D.S., Rissman E.F. Oestrogen-independent, experience-induced maternal behaviour in female mice. J. Neuroendocrinol. 2011, 23:345-354.
97. Sweatt J.D. Experience-dependent epigenetic modifications in the central nervous system. Biol. Psychiatry 2009, 65:191-197.
98. Takayanagi Y., Yoshida M., Bielsky I.F., Ross H.E., Kawamata M., Onaka T., Yanagisawa T., Kimura T., Matzuk M.M., Young L.J., Nishimori K. Pervasive social deficits, but normal parturition, in oxytocin receptor-deficient mice. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:16096-16101.
99. Thomas S.A., Palmiter R.D. Impaired maternal behavior in mice lacking norepinephrine and epinephrine. Cell 1997, 91:583-592.
100. Vecsey C.G., Hawk J.D., Lattal K.M., Stein J.M., Fabian S.A., Attner M.A., Cabrera S.M., McDonough C.B., Brindle P.K., Abel T., Wood M.A. Histone deacetylase inhibitors enhance memory and synaptic plasticity via CREB:CBP-dependent transcriptional activation. J. Neurosci. 2007, 27:6128-6140.
101. Yeh S.H., Lin C.H., Gean P.W. Acetylation of nuclear factor-kappaB in rat amygdala improves long-term but not short-term retention of fear memory. Mol. Pharmacol. 2004, 65:1286-1292.
102. Zhu H., Huang Q., Xu H., Niu L., Zhou J.N. Antidepressant-like effects of sodium butyrate in combination with estrogen in rat forced swimming test: involvement of 5-HT(1A) receptors. Behav. Brain Res. 2009, 196:200-206.