Changes in anxiety and cognition due to reproductive experience: A review of data from rodent and human mothers

Neuroscience and Biobehavioral Reviews

Volumn 34, Issue 3, 2010, Pages 452-467

  Macbeth, Abbe H ^a   Luine, Victoria N ^b  

^a NATIONAL INSTITUTE OF MENTAL HEALTH   (United States)

^b CITY UNIVERSITY OF NEW YORK   (United States)

Author keywords

Anxiety; Cognition; Memory; Neurochemistry; Postpartum; Pregnancy

Indexed keywords

3,4 DIHYDROXYPHENYLACETIC ACID; 4 HYDROXY 3 METHOXYPHENYLETHYLENE GLYCOL; 5 HYDROXYINDOLEACETIC ACID; BRAIN DERIVED NEUROTROPHIC FACTOR; CORTICOTROPIN; DOPAMINE; ESTRADIOL; HOMOVANILLIC ACID; MONOAMINE; NEUROTRANSMITTER; NORADRENALIN; OXYTOCIN; PROLACTIN; SEROTONIN;

ANIMAL BEHAVIOR; ANXIETY; ATTITUDE TO PREGNANCY; BEHAVIOR CHANGE; CHILDBIRTH; COGNITION; COGNITIVE DEFECT; COPING BEHAVIOR; FUNCTIONAL MORPHOLOGY; HIPPOCAMPUS; HUMAN; HUMAN VERSUS ANIMAL COMPARISON; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; MATERNAL BEHAVIOR; MATERNAL STRESS; MEMORY CONSOLIDATION; MEMORY DISORDER; METABOLITE; NERVE CELL LESION; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PARITY; PRIORITY JOURNAL; PUERPERAL DEPRESSION; PUERPERIUM; REPRODUCTION; REVIEW; SPATIAL MEMORY; THIRD TRIMESTER PREGNANCY; WORKING MEMORY;

ANIMALS; ANXIETY; COGNITION; FEMALE; HUMANS; MOTHERS; PARITY; POSTPARTUM PERIOD; PREGNANCY; REPRODUCTION;

EID: 72449205923     PISSN: 01497634     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neubiorev.2009.08.011     Document Type: Review

References (191)

1. Abou-Saleh M.T., Ghubash R., Karim L., Krymski M., and Bhai I. Hormonal aspects of postpartum depression. Psychoneuroendocrinology 23 (1998) 465-475
2. Agrati D., Zuluaga M.J., Fernandez-Guasti A., Meikle A., and Ferreira A. Maternal condition reduces fear behaviors but not the endocrine response to an emotional threat in virgin female rats. Horm. Behav. 53 (2008) 232-240
3. Ahokas A., Kaukoranta J., and Aito M. Effect of oestradiol on postpartum depression. Psychopharmacology (Berl.) 146 (1999) 108-110
4. Alonso M., Vianna M.R., Depino A.M., Mello e Souza T., Pereira P., Szapiro G., et al. BDNF-triggered events in the rat hippocampus are required for both short- and long-term memory formation. Hippocampus 12 (2002) 551-560
5. Altemus M. Neuropeptides in anxiety disorders. Effects of lactation. Ann. N. Y. Acad. Sci. 771 (1995) 697-707
6. Altemus M., Deuster P.A., Galliven E., Carter C.S., and Gold P.W. Suppression of hypothalmic-pituitary-adrenal axis responses to stress in lactating women. J. Clin. Endocrinol. Metab. 80 (1995) 2954-2959
7. Altemus M., Fong J., Yang R., Damast S., Luine V., and Ferguson D. Changes in cerebrospinal fluid neurochemistry during pregnancy. Biol. Psychiatry 56 (2004) 386-392
8. Altemus M., Redwine L.S., Leong Y.M., Frye C.A., Porges S.W., and Carter C.S. Responses to laboratory psychosocial stress in postpartum women. Psychosom. Med. 63 (2001) 814-821
9. Amico J.A., Johnston J.M., and Vagnucci A.H. Suckling-induced attenuation of plasma cortisol concentrations in postpartum lactating women. Endocr. Res. 20 (1994) 79-87
10. Astur R.S., Klein R.L., Mumby D.G., Protz D.K., Sutherland R.J., and Martin G.M. A role for olfaction in object recognition by normal and hippocampal-damaged rats. Neurobiol. Learn. Mem. 78 (2002) 186-191
11. Banasr M., Hery M., Brezun J.M., and Daszuta A. Serotonin mediates oestrogen stimulation of cell proliferation in the adult dentate gyrus. Eur. J. Neurosci. 14 (2001) 1417-1424
12. Bandelow B., Sojka F., Broocks A., Hajak G., Bleich S., and Ruther E. Panic disorder during pregnancy and postpartum period. Eur. Psychiatry 21 (2006) 495-500
13. Bellmann O. Hormonal regulation of lactation (author's transl). Klin. Padiatr. 188 (1976) 385-395
14. Berchtold N.C., Kesslak J.P., and Cotman C.W. Hippocampal brain-derived neurotrophic factor gene regulation by exercise and the medial septum. J. Neurosci. Res. 68 (2002) 511-521
15. Bevilaqua L., Ardenghi P., Schroder N., Bromberg E., Quevedo J., Schmitz P.K., et al. Agents that affect cAMP levels or protein kinase A activity modulate memory consolidation when injected into rat hippocampus but not amygdala. Braz. J. Med. Biol. Res. 30 (1997) 967-970
16. Bi R., Foy M.R., Vouimba R.M., Thompson R.F., and Baudry M. Cyclic changes in estradiol regulate synaptic plasticity through the MAP kinase pathway. Proc. Natl. Acad. Sci. U.S.A. 98 (2001) 13391-13395
17. Bodensteiner K.J., Cain P., Ray A.S., and Hamula L.A. Effects of pregnancy on spatial cognition in female Hooded Long-Evans rats. Horm. Behav. 49 (2006) 303-314
18. Brennan P.A., and Keverne E.B. Neural mechanisms of mammalian olfactory learning. Prog. Neurobiol. 51 (1997) 457-481
19. Bridges R.S. Long-term effects of pregnancy and parturition upon maternal responsiveness in the rat. Physiol. Behav. 14 (1975) 245-249
20. Brindle P.M., Brown M.W., Brown J., Griffith H.B., and Turner G.M. Objective and subjective memory impairment in pregnancy. Psychol. Med. 21 (1991) 647-653
21. Brummelte S., Pawluski J.L., and Galea L.A. High post-partum levels of corticosterone given to dams influence postnatal hippocampal cell proliferation and behavior of offspring: a model of post-partum stress and possible depression. Horm. Behav. 50 (2006) 370-382
22. Brunton P.J., and Russell J.A. The expectant brain: adapting for motherhood. Nat. Rev. Neurosci. 9 (2008) 11-25
23. Brunton P.J., Russell J.A., and Douglas A.J. Adaptive responses of the maternal hypothalamic-pituitary-adrenal axis during pregnancy and lactation. J. Neuroendocrinol. 20 (2008) 764-776
24. Brusco J., Wittmann R., de Azevedo M.S., Lucion A.B., Franci C.R., Giovenardi M., et al. 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 (2008) 346-350
25. Buckwalter J.G., Buckwalter D.K., Bluestein B.W., and Stanczyk F.Z. Pregnancy and post partum: changes in cognition and mood. Prog. Brain Res. 133 (2001) 303-319
26. Buckwalter J.G., Stanczyk F.Z., McCleary C.A., Bluestein B.W., Buckwalter D.K., Rankin K.P., et al. Pregnancy, the postpartum, and steroid hormones: effects on cognition and mood. Psychoneuroendocrinology 24 (1999) 69-84
27. Byrnes E.M., and Bridges R.S. Reproductive experience alters anxiety-like behavior in the female rat. Horm. Behav. 50 (2006) 70-76
28. Byrnes E.M., Nephew B.C., and Bridges R.S. Neuroendocrine and behavioral adaptations following reproductive experience in the female rat. In: Bridges R.S. (Ed). Neurobiology of the Parental Brain (2007), Elsevier, Burlington 509-517
29. Calamandrei G., Wilkinson L.S., and Keverne E.B. Olfactory recognition of infants in laboratory mice: role of noradrenergic mechanisms. Physiol. Behav. 52 (1992) 901-907
30. Cameron N.M., Shahrokh D., Del Corpo A., Dhir S.K., Szyf M., Champagne F.A., et al. Epigenetic programming of phenotypic variations in reproductive strategies in the rat through maternal care. J. Neuroendocrinol. 20 (2008) 795-801
31. Carr B.R., Parker Jr. C.R., Madden J.D., MacDonald P.C., and Porter J.C. Maternal plasma adrenocorticotropin and cortisol relationships throughout human pregnancy. Am. J. Obstet. Gynecol. 139 (1981) 416-422
32. Carter C.S., and Altemus M. Integrative functions of lactational hormones in social behavior and stress management. Ann. N. Y. Acad. Sci. 807 (1997) 164-174
33. Carter C.S., Altemus M., and Chrousos G.P. Neuroendocrine and emotional changes in the post-partum period. Prog. Brain Res. 133 (2001) 241-249
34. Casey P., Huntsdale C., Angus G., and Janes C. Memory in pregnancy. II: Implicit, incidental, explicit, semantic, short-term, working and prospective memory in primigravid, multigravid and postpartum women. J. Psychosom. Obstet. Gynaecol. 20 (1999) 158-164
35. Casolini P., Domenici M.R., Cinque C., Alema G.S., Chiodi V., Galluzzo M., et al. Maternal exposure to low levels of corticosterone during lactation protects the adult offspring against ischemic brain damage. J. Neurosci. 27 (2007) 7041-7046
36. Chakraborty T.R., and Gore A.C. Aging-related changes in ovarian hormones, their receptors, and neuroendocrine function. Exp. Biol. Med. (Maywood) 229 (2004) 977-987
37. Chiodera P., Salvarani C., Bacchi-Modena A., Spallanzani R., Cigarini C., Alboni A., et al. Relationship between plasma profiles of oxytocin and adrenocorticotropic hormone during suckling or breast stimulation in women. Horm. Res. 35 (1991) 119-123
38. Correia L.L., and Linhares M.B. Maternal anxiety in the pre- and postnatal period: a literature review. Rev. Lat. Am. Enfermagem. 15 (2007) 677-683
39. Coutellier L., Friedrich A.C., Failing K., and Wurbel H. Variations in the postnatal maternal environment in mice: effects on maternal behaviour and behavioural and endocrine responses in the adult offspring. Physiol. Behav. 93 (2008) 395-407
40. Crawley R.A., Dennison K., and Carter C. Cognition in pregnancy and the first year post-partum. Psychol. Psychother. 76 (2003) 69-84
41. da Costa A.P., Wood S., Ingram C.D., and Lightman S.L. Region-specific reduction in stress-induced c-fos mRNA expression during pregnancy and lactation. Brain Res. 742 (1996) 177-184
42. Darnaudery M., Perez-Martin M., Del Favero F., Gomez-Roldan C., Garcia-Segura L.M., and Maccari S. Early motherhood in rats is associated with a modification of hippocampal function. Psychoneuroendocrinology 32 (2007) 803-812
43. Dayan J. Clinical approach and epidemiological aspects of mood and anxiety disorders during pregnancy and postpartum. Review and synthesis. J. Gynecol. Obstet. Biol. Reprod. (Paris) 36 (2007) 549-561
44. de Brito Faturi C., Teixeira-Silva F., and Leite J.R. The anxiolytic effect of pregnancy in rats is reversed by finasteride. Pharmacol. Biochem. Behav. 85 (2006) 569-574
45. de Castilhos J., Forti C.D., Achaval M., and Rasia-Filho A.A. Dendritic spine density of posterodorsal medial amygdala neurons can be affected by gonadectomy and sex steroid manipulations in adult rats: a Golgi study. Brain Res. 1240 (2008) 73-81
46. de Groot R.H., Hornstra G., Roozendaal N., and Jolles J. Memory performance, but not information processing speed, may be reduced during early pregnancy. J. Clin. Exp. Neuropsychol. 25 (2003) 482-488
47. de Groot R.H., Vuurman E.F., Hornstra G., and Jolles J. Differences in cognitive performance during pregnancy and early motherhood. Psychol. Med. 36 (2006) 1023-1032
48. de Weerth C., and Buitelaar J.K. Physiological stress reactivity in human pregnancy-a review. Neurosci. Biobehav. Rev. 29 (2005) 295-312
49. Desan P.H., Woodmansee W.W., Ryan S.M., Smock T.K., and Maier S.F. Monoamine neurotransmitters and metabolites during the estrous cycle, pregnancy, and the postpartum period. Pharmacol. Biochem. Behav. 30 (1988) 563-568
50. Dickinson C., and Keverne E.B. Importance of noradrenergic mechanisms in the olfactory bulbs for the maternal behaviour of mice. Physiol. Behav. 43 (1988) 313-316
51. Dluzen D.E. Age-related changes in monoamines within the olfactory bulbs of the Fischer 344 male rat. Mech. Ageing Dev. 91 (1996) 37-45
52. Eberhard-Gran M., Eskild A., Tambs K., Samuelsen S.O., and Opjordsmoen S. Depression in postpartum and non-postpartum women: prevalence and risk factors. Acta Psychiatr. Scand. 106 (2002) 426-433
53. Eidelman A.I., Hoffmann N.W., and Kaitz M. Cognitive deficits in women after childbirth. Obstet. Gynecol. 81 (1993) 764-767
54. Ennaceur A., Neave N., and Aggleton J.P. Spontaneous object recognition and object location memory in rats: the effects of lesions in the cingulate cortices, the medial prefrontal cortex, the cingulum bundle and the fornix. Exp. Brain Res. 113 (1997) 509-519
55. Fajardo M.C., Florido J., Villaverde C., Oltras C.M., Gonzalez-Ramirez A.R., and Gonzalez-Gomez F. Plasma levels of beta-endorphin and ACTH during labor and immediate puerperium. Eur. J. Obstet. Gynecol. Reprod. Biol. 55 (1994) 105-108
56. Feldman R., Weller A., Zagoory-Sharon O., and Levine A. Evidence for a neuroendocrinological foundation of human affiliation: plasma oxytocin levels across pregnancy and the postpartum period predict mother-infant bonding. Psychol. Sci. 18 (2007) 965-970
57. Figueira R.J., Peabody M.F., and Lonstein J.S. Oxytocin receptor activity in the ventrocaudal periaqueductal gray modulates anxiety-related behavior in postpartum rats. Behav. Neurosci. 122 (2008) 618-628
58. Fleming A.S., Cheung U., Myhal N., and Kessler Z. Effects of maternal hormones on 'timidity' and attraction to pup-related odors in female rats. Physiol. Behav. 46 (1989) 449-453
59. Fleming A.S., Gavarth K., and Sarker J. Effects of transections to the vomeronasal nerves or to the main olfactory bulbs on the initiation and long-term retention of maternal behavior in primiparous rats. Behav. Neural. Biol. 57 (1992) 177-188
60. Fleming A.S., and Luebke C. Timidity prevents the virgin female rat from being a good mother: emotionality differences between nulliparous and parturient females. Physiol. Behav. 27 (1981) 863-868
61. Fleming A.S., and Rosenblatt J.S. Maternal behavior in the virgin and lactating rat. J. Comp. Physiol. Psychol. 86 (1974) 957-972
62. Fleming A.S., and Rosenblatt J.S. Olfactory regulation of maternal behavior in rats. I. Effects of olfactory bulb removal in experienced and inexperienced lactating and cycling females. J. Comp. Physiol. Psychol. 86 (1974) 221-232
63. Fleming A.S., and Sarker J. Experience-hormone interactions and maternal behavior in rats. Physiol. Behav. 47 (1990) 1165-1173
64. Frye C.A., and Walf A.A. Hippocampal 3alpha,5alpha-THP may alter depressive behavior of pregnant and lactating rats. Pharmacol. Biochem. Behav. 78 (2004) 531-540
65. Furuta M., and Bridges R.S. Gestation-induced cell proliferation in the rat brain. Brain Res. Dev. Brain Res. 156 (2005) 61-66
66. Galea L.A., Ormerod B.K., Sampath S., Kostaras X., Wilkie D.M., and Phelps M.T. Spatial working memory and hippocampal size across pregnancy in rats. Horm. Behav. 37 (2000) 86-95
67. Galea L.A., Uban K.A., Epp J.R., Brummelte S., Barha C.K., Wilson W.L., et al. Endocrine regulation of cognition and neuroplasticity: our pursuit to unveil the complex interaction between hormones, the brain, and behaviour. Can. J. Exp. Psychol. 62 (2008) 247-260
68. Galler J.R., Harrison R.H., Ramsey F., Forde V., and Butler S.C. Maternal depressive symptoms affect infant cognitive development in Barbados. J. Child Psychol. Psychiatry 41 (2000) 747-757
69. Gammie S.C., Seasholtz A.F., and Stevenson S.A. Deletion of corticotropin-releasing factor binding protein selectively impairs maternal, but not intermale aggression. Neuroscience 157 (2008) 502-512
70. Gatewood J.D., Morgan M.D., Eaton M., McNamara I.M., Stevens L.F., Macbeth A.H., et al. Motherhood mitigates aging-related decrements in learning and memory and positively affects brain aging in the rat. Brain Res. Bull. 66 (2005) 91-98
71. Goodman J.H. Postpartum depression beyond the early postpartum period. J. Obstet. Gynecol. Neonatal. Nurs. 33 (2004) 410-420
72. Graham M.D., Rees S.L., Steiner M., and Fleming A.S. The effects of adrenalectomy and corticosterone replacement on maternal memory in postpartum rats. Horm. Behav. 49 (2006) 353-361
73. Grant K.A., McMahon C., and Austin M.P. Maternal anxiety during the transition to parenthood: a prospective study. J. Affect. Disord. 108 (2008) 101-111
74. Gregoire A.J., Kumar R., Everitt B., Henderson A.F., and Studd J.W. Transdermal oestrogen for treatment of severe postnatal depression. Lancet 347 (1996) 930-933
75. Guan X., and Dluzen D.E. Age related changes of social memory/recognition in male Fischer 344 rats. Behav. Brain Res. 61 (1994) 87-90
76. Guler O., Koken G.N., Emul M., Ozbulut O., Gecici O., Uguz F., et al. Course of panic disorder during the early postpartum period: a prospective analysis. Compr. Psychiatry 49 (2008) 30-34
77. Guler O., Sahin F.K., Emul H.M., Ozbulut O., Gecici O., Uguz F., et al. The prevalence of panic disorder in pregnant women during the third trimester of pregnancy. Compr. Psychiatry 49 (2008) 154-158
78. Heinrichs M., Meinlschmidt G., Neumann I., Wagner S., Kirschbaum C., Ehlert U., et al. Effects of suckling on hypothalamic-pituitary-adrenal axis responses to psychosocial stress in postpartum lactating women. J. Clin. Endocrinol. Metab. 86 (2001) 4798-4804
79. Henry J.D., and Rendell P.G. A review of the impact of pregnancy on memory function. J. Clin. Exp. Neuropsychol. 29 (2007) 793-803
80. Heron J., O'Connor T.G., Evans J., Golding J., and Glover V. The course of anxiety and depression through pregnancy and the postpartum in a community sample. J. Affect. Disord. 80 (2004) 65-73
81. Hohlagschwandtner M., Husslein P., Klier C., and Ulm B. Correlation between serum testosterone levels and peripartal mood states. Acta Obstet. Gynecol. Scand. 80 (2001) 326-330
82. Hunter L.P., Rychnovsky J.D., and Yount S.M. A selective review of maternal sleep characteristics in the postpartum period. J. Obstet. Gynecol. Neonatal. Nurs. 38 (2009) 60-68
83. Janes C., Casey P., Huntsdale C., and Angus G. Memory in pregnancy. I: Subjective experiences and objective assessment of implicit, explicit and working memory in primigravid and primiparous women. J. Psychosom. Obstet. Gynaecol. 20 (1999) 80-87
84. Jonas W., Johansson L.M., Nissen E., Ejdeback M., Ransjo-Arvidson A.B., and Uvnas-Moberg K. Effects of Intrapartum Oxytocin Administration and Epidural Analgesia on the Concentration of Plasma Oxytocin and Prolactin, in Response to Suckling During the Second Day Postpartum. Breastfeed Med. (2009)
85. Jonas W., Nissen E., Ransjo-Arvidson A.B., Matthiesen A.S., and Uvnas-Moberg K. Influence of oxytocin or epidural analgesia on personality profile in breastfeeding women: a comparative study. Arch. Womens Ment. Health 11 (2008) 335-345
86. Kammerer M., Adams D., Castelberg Bv B., and Glover V. Pregnant women become insensitive to cold stress. BMC Pregnancy Childbirth 2 (2002) 8
87. Keenan P.A., Yaldoo D.T., Stress M.E., Fuerst D.R., and Ginsburg K.A. Explicit memory in pregnant women. Am. J. Obstet. Gynecol. 179 (1998) 731-737
88. Kesner R.P., Lee I., and Gilbert P. A behavioral assessment of hippocampal function based on a subregional analysis. Rev. Neurosci. 15 (2004) 333-351
89. Kinsley C.H., Bardi M., Karelina K., Rima B., Christon L., Friedenberg J., et al. Motherhood induces and maintains behavioral and neural plasticity across the lifespan in the rat. Arch. Sex Behav. 37 (2008) 43-56
90. Kinsley C.H., and Lambert K.G. The maternal brain. Sci. Am. 294 (2006) 72-79
91. Kinsley C.H., and Lambert K.G. Reproduction-induced neuroplasticity: natural behavioural and neuronal alterations associated with the production and care of offspring. J. Neuroendocrinol. 20 (2008) 515-525
92. Kinsley C.H., Madonia L., Gifford G.W., Tureski K., Griffin G.R., Lowry C., et al. Motherhood improves learning and memory. Nature 402 (1999) 137-138
93. Kinsley C.H., Trainer R., Stafisso-Sandoz G., Quadros P., Marcus L.K., Hearon C., et al. Motherhood and the hormones of pregnancy modify concentrations of hippocampal neuronal dendritic spines. Horm. Behav. 49 (2006) 131-142
94. Lambert K.G., Berry A.E., Griffins G., Amory-Meyers E., Madonia-Lomas L., Love G., et al. Pup exposure differentially enhances foraging ability in primiparous and nulliparous rats. Physiol. Behav. 84 (2005) 799-806
95. Lambert K.G., and Kinsley C.H. The neuroeconomics of motherhood: the costs and benefits of maternal investment. In: Bridges R.S. (Ed). Neurobiology of the Parental Brain (2007), Elsevier, Burlington 481-491
96. LeDoux J. The amygdala. Curr. Biol. 17 (2007) R868-R874
97. Lemaire V., Billard J.M., Dutar P., George O., Piazza P.V., Epelbaum J., et al. Motherhood-induced memory improvement persists across lifespan in rats but is abolished by a gestational stress. Eur. J. Neurosci. 23 (2006) 3368-3374
98. Lemon N., and Manahan-Vaughan D. Dopamine D1/D5 receptors gate the acquisition of novel information through hippocampal long-term potentiation and long-term depression. J. Neurosci. 26 (2006) 7723-7729
99. Leuner B., Mirescu C., Noiman L., and Gould E. Maternal experience inhibits the production of immature neurons in the hippocampus during the postpartum period through elevations in adrenal steroids. Hippocampus 17 (2007) 434-442
100. Leuner B., and Shors T.J. Learning during motherhood: a resistance to stress. Horm. Behav. 50 (2006) 38-51
101. Levine A., Zagoory-Sharon O., Feldman R., and Weller A. Oxytocin during pregnancy and early postpartum: individual patterns and maternal-fetal attachment. Peptides 28 (2007) 1162-1169
102. Levy F., Gervais R., Kindermann U., Orgeur P., and Piketty V. Importance of beta-noradrenergic receptors in the olfactory bulb of sheep for recognition of lambs. Behav. Neurosci. 104 (1990) 464-469
103. Levy F., Keller M., and Poindron P. Olfactory regulation of maternal behavior in mammals. Horm. Behav. 46 (2004) 284-302
104. Linnarsson S., Bjorklund A., and Ernfors P. Learning deficit in BDNF mutant mice. Eur. J. Neurosci. 9 (1997) 2581-2587
105. Lonstein J.S. Reduced anxiety in postpartum rats requires recent physical interactions with pups, but is independent of suckling and peripheral sources of hormones. Horm. Behav. 47 (2005) 241-255
106. Lonstein J.S. Regulation of anxiety during the postpartum period. Front. Neuroendocrinol. 28 (2007) 115-141
107. Lonstein J.S., and Miller S.M. Mother-infant touch, neurochemistry, and postpartum anxiety. In: Bridges R.S. (Ed). Neurobiology of the Parental Brain (2007), Elsevier, Burlington 145-162
108. Love G., Torrey N., McNamara I., Morgan M., Banks M., Hester N.W., et al. Maternal experience produces long-lasting behavioral modifications in the rat. Behav. Neurosci. 119 (2005) 1084-1096
109. Luine V., Bowling D., and Hearns M. Spatial memory deficits in aged rats: contributions of monoaminergic systems. Brain Res. 537 (1990) 271-278
110. Luine V.N., and Dohanich G. Sex differences in cognitive function in rodents. In: Becker J.B., Berkley K.J., Geary N., et al. (Eds). Sex Differences in the Brain: From Genes to Behavior (2008), Oxford University Press, New York 227-252
111. Macbeth A.H., Gautreaux C., and Luine V.N. Pregnant rats show enhanced spatial memory, decreased anxiety, and altered levels of monoaminergic neurotransmitters. Brain Res. 1241 (2008) 136-147
112. Macbeth A.H., Scharfman H.E., Maclusky N.J., Gautreaux C., and Luine V.N. Effects of multiparity on recognition memory, monoaminergic neurotransmitters, and brain-derived neurotrophic factor (BDNF). Horm. Behav. 54 (2008) 7-17
113. Matthiesen A.S., Ransjo-Arvidson A.B., Nissen E., and Uvnas-Moberg K. Postpartum maternal oxytocin release by newborns: effects of infant hand massage and sucking. Birth 28 (2001) 13-19
114. Mickes L., Wixted J.T., Shapiro A., and Michael Scarff J. The effects of pregnancy on memory: recall is worse but recognition is not. J. Clin. Exp. Neuropsychol. (2008) 1-8
115. Miguez J.M., Aldegunde M., Paz-Valinas L., Recio J., and Sanchez-Barcelo E. Selective changes in the contents of noradrenaline, dopamine and serotonin in rat brain areas during aging. J. Neural. Transm. 106 (1999) 1089-1098
116. Moltz H., Lubin M., Leon M., and Numan M. Hormonal induction of maternal behavior in the ovariectomized nulliparous rat. Physiol. Behav. 5 (1970) 1373-1377
117. Monks D.A., Lonstein J.S., and Breedlove S.M. Got milk? Oxytocin triggers hippocampal plasticity. Nat. Neurosci. 6 (2003) 327-328
118. Morris R. Developments of a water-maze procedure for studying spatial learning in the rat. J. Neurosci. Methods 11 (1984) 47-60
119. Morris R.G., Garrud P., Rawlins J.N., and O'Keefe J. Place navigation impaired in rats with hippocampal lesions. Nature 297 (1982) 681-683
120. Moscovitch M., Rosenbaum R.S., Gilboa A., Addis D.R., Westmacott R., Grady C., et al. Functional neuroanatomy of remote episodic, semantic and spatial memory: a unified account based on multiple trace theory. J. Anat. 207 (2005) 35-66
121. Moses-Kolko E.L., Meltzer C.C., Berga S.L., and Wisner K.L. Postpartum depression: the clinical disorder and application of pet imaging research methods. In: Bridges R.S. (Ed). Neurobiology of the Parental Brain (2007), Elsevier, Burlington 175-199
122. Nagata M., Nagai Y., Sobajima H., Ando T., Nishide Y., and Honjo S. Maternity blues and attachment to children in mothers of full-term normal infants. Acta Psychiatr. Scand. 101 (2000) 209-217
123. Neumann I.D. Alterations in behavioral and neuroendocrine stress coping strategies in pregnant, parturient and lactating rats. Prog. Brain Res. 133 (2001) 143-152
124. Neumann I.D., and Bosch O.J. Maternal stress adaptations peripartum: mom's innate anxiety determines maternal care and aggression. In: Bridges R.S. (Ed). Neurobiology of the Parental Brain (2007), Elsevier, Burlington 115-130
125. Neumann I.D., Torner L., and Wigger A. Brain oxytocin: differential inhibition of neuroendocrine stress responses and anxiety-related behaviour in virgin, pregnant and lactating rats. Neuroscience 95 (2000) 567-575
126. Nissen E., Gustavsson P., Widstrom A.M., and Uvnas-Moberg K. Oxytocin, prolactin, milk production and their relationship with personality traits in women after vaginal delivery or Cesarean section. J. Psychosom. Obstet. Gynaecol. 19 (1998) 49-58
127. Numan M. Medial preoptic area and maternal behavior in the female rat. J. Comp. Physiol. Psychol. 87 (1974) 746-759
128. Numan M., and Callahan E.C. The connections of the medial preoptic region and maternal behavior in the rat. Physiol. Behav. 25 (1980) 653-665
129. Oatridge A., Holdcroft A., Saeed N., Hajnal J.V., Puri B.K., Fusi L., et al. Change in brain size during and after pregnancy: study in healthy women and women with preeclampsia. AJNR Am. J. Neuroradiol. 23 (2002) 19-26
130. Ochedalski T., Subburaju S., Wynn P.C., and Aguilera G. Interaction between oestrogen and oxytocin on hypothalamic-pituitary-adrenal axis activity. J. Neuroendocrinol. 19 (2007) 189-197
131. Ochedalski T., Zylinska K., Laudanski T., and Lachowicz A. Corticotrophin-releasing hormone and ACTH levels in maternal and fetal blood during spontaneous and oxytocin-induced labour. Eur. J. Endocrinol. 144 (2001) 117-121
132. Olton D.S., and Papas B.C. Spatial memory and hippocampal function. Neuropsychologia 17 (1979) 669-682
133. Orpen B.G., Furman N., Wong P.Y., and Fleming A.S. Hormonal influences on the duration of postpartum maternal responsiveness in the rat. Physiol. Behav. 40 (1987) 307-315
134. Paris J.J., and Frye C.A. Estrous cycle, pregnancy, and parity enhance performance of rats in object recognition or object placement tasks. Reproduction 136 (2008) 105-115
135. Parsons T.D., Thompson E., Buckwalter D.K., Bluestein B.W., Stanczyk F.Z., and Buckwalter J.G. Pregnancy history and cognition during and after pregnancy. Int. J. Neurosci. 114 (2004) 1099-1110
136. Pawluski J.L., Brummelte S., Barha C.K., Crozier T.M., and Galea L.A. Effects of steroid hormones on neurogenesis in the hippocampus of the adult female rodent during the estrous cycle, pregnancy, lactation and aging. Front. Neuroendocrinol. (2009)
137. Pawluski J.L., Charlier T.D., Lieblich S.E., Hammond G.L., and Galea L.A. Reproductive experience alters corticosterone and CBG levels in the rat dam. Physiol. Behav. 96 (2009) 108-114
138. Pawluski J.L., and Galea L.A. Hippocampal morphology is differentially affected by reproductive experience in the mother. J. Neurobiol. 66 (2006) 71-81
139. Pawluski J.L., and Galea L.A. Reproductive experience alters hippocampal neurogenesis during the postpartum period in the dam. Neuroscience 149 (2007) 53-67
140. Pawluski J.L., and Galea L.A.M. The role of reproductive experience on hippocampal function and plasticity. In: Bridges R.S. (Ed). Neurobiology of the Parental Brain (2007), Elsevier, Burlington 493-508
141. Pawluski J.L., Lieblich S.E., and Galea L.A. Offspring-exposure reduces depressive-like behaviour in the parturient female rat. Behav. Brain Res. 197 (2009) 55-61
142. Pawluski J.L., Vanderbyl B.L., Ragan K., and Galea L.A. 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 (2006) 157-165
143. Pawluski J.L., Walker S.K., and Galea L.A. Reproductive experience differentially affects spatial reference and working memory performance in the mother. Horm. Behav. 49 (2006) 143-149
144. Payne J.L., Palmer J.T., and Joffe H. A reproductive subtype of depression: conceptualizing models and moving toward etiology. Harv. Rev. Psychiatry 17 (2009) 72-86
145. Pedersen C.A., Ascher J.A., Monroe Y.L., and Prange Jr. A.J. Oxytocin induces maternal behavior in virgin female rats. Science 216 (1982) 648-650
146. Pedersen C.A., and Boccia M.L. Oxytocin antagonism alters rat dams' oral grooming and upright posturing over pups. Physiol. Behav. 80 (2003) 233-241
147. Pedersen C.A., Vadlamudi S.V., Boccia M.L., and Amico J.A. Maternal behavior deficits in nulliparous oxytocin knockout mice. Genes Brain Behav. 5 (2006) 274-281
148. Pellow S., Chopin P., File S.E., and Briley M. Validation of open:closed arm entries in an elevated plus-maze as a measure of anxiety in the rat. J. Neurosci. Methods 14 (1985) 149-167
149. Pereira M., Uriarte N., Agrati D., Zuluaga M.J., and Ferreira A. Motivational aspects of maternal anxiolysis in lactating rats. Psychopharmacology (Berl.) 180 (2005) 241-248
150. Pissonnier D., Thiery J.C., Fabre-Nys C., Poindron P., and Keverne E.B. The importance of olfactory bulb noradrenalin for maternal recognition in sheep. Physiol. Behav. 35 (1985) 361-363
151. Poser C.M., Kassirer M.R., and Peyser J.M. Benign encephalopathy of pregnancy. Preliminary clinical observations. Acta Neurol. Scand. 73 (1986) 39-43
152. Potvin O., Allen K., Thibaudeau G., Dore F.Y., and Goulet S. Performance on spatial working memory tasks after dorsal or ventral hippocampal lesions and adjacent damage to the subiculum. Behav. Neurosci. 120 (2006) 413-422
153. Ransjo-Arvidson A.B., Matthiesen A.S., Lilja G., Nissen E., Widstrom A.M., and Uvnas-Moberg K. Maternal analgesia during labor disturbs newborn behavior: effects on breastfeeding, temperature, and crying. Birth 28 (2001) 5-12
154. Rasia-Filho A.A., Fabian C., Rigoti K.M., and Achaval M. Influence of sex, estrous cycle and motherhood on dendritic spine density in the rat medial amygdala revealed by the Golgi method. Neuroscience 126 (2004) 839-847
155. Rees S.L., Panesar S., Steiner M., and Fleming A.S. The effects of adrenalectomy and corticosterone replacement on maternal behavior in the postpartum rat. Horm. Behav. 46 (2004) 411-419
156. Rendell P.G., and Henry J.D. Prospective-memory functioning is affected during pregnancy and postpartum. J. Clin. Exp. Neuropsychol. (2008) 1-7
157. Rochefort C., Gheusi G., Vincent J.D., and Lledo P.M. Enriched odor exposure increases the number of newborn neurons in the adult olfactory bulb and improves odor memory. J. Neurosci. 22 (2002) 2679-2689
158. Rosenblatt J.S. Prepartum and postpartum regulation of maternal behaviour in the rat. Ciba Found. Symp. (1975) 17-37
159. Rosenblatt J.S., Mayer A.D., and Giordano A.L. Hormonal basis during pregnancy for the onset of maternal behavior in the rat. Psychoneuroendocrinology 13 (1988) 29-46
160. Rosenblatt J.S., Olufowobi A., and Siegel H.I. Effects of pregnancy hormones on maternal responsiveness, responsiveness to estrogen stimulation of maternal behavior, and the lordosis response to estrogen stimulation. Horm. Behav. 33 (1998) 104-114
161. Ruscio M.G., Sweeny T.D., Hazelton J.L., Suppatkul P., Boothe E., and Carter C.S. Pup exposure elicits hippocampal cell proliferation in the prairie vole. Behav. Brain. Res. 187 (2008) 9-16
162. Sasaki A., Tempst P., Liotta A.S., Margioris A.N., Hood L.E., Kent S.B., et al. Isolation and characterization of a corticotropin-releasing hormone-like peptide from human placenta. J. Clin. Endocrinol. Metab. 67 (1988) 768-773
163. Sato Y., Kato T., and Kakee N. A six-month follow-up study of maternal anxiety and depressive symptoms among Japanese. J. Epidemiol. 18 (2008) 84-87
164. Scharfman H.E., and MacLusky N.J. Estrogen and brain-derived neurotrophic factor (BDNF) in hippocampus: complexity of steroid hormone-growth factor interactions in the adult CNS. Front. Neuroendocrinol. 27 (2006) 415-435
165. Seifritz E., Esposito F., Neuhoff J.G., Luthi A., Mustovic H., Dammann G., et al. Differential sex-independent amygdala response to infant crying and laughing in parents versus nonparents. Biol. Psychiatry 54 (2003) 1367-1375
166. Seip K.M., and Morrell J.I. Exposure to pups influences the strength of maternal motivation in virgin female rats. Physiol. Behav. 95 (2008) 599-608
167. Shanks N., Windle R.J., Perks P., Wood S., Ingram C.D., and Lightman S.L. The hypothalamic-pituitary-adrenal axis response to endotoxin is attenuated during lactation. J. Neuroendocrinol. 11 (1999) 857-865
168. Sharp K., Brindle P.M., Brown M.W., and Turner G.M. Memory loss during pregnancy. Br. J. Obstet. Gynaecol. 100 (1993) 209-215
169. Shingo T., Gregg C., Enwere E., Fujikawa H., Hassam R., Geary C., et al. Pregnancy-stimulated neurogenesis in the adult female forebrain mediated by prolactin. Science 299 (2003) 117-120
170. Silber M., Almkvist O., Larsson B., and Uvnas-Moberg K. Temporary peripartal impairment in memory and attention and its possible relation to oxytocin concentration. Life Sci. 47 (1990) 57-65
171. Swain J.E., Lorberbaum J.P., Kose S., and Strathearn L. Brain basis of early parent-infant interactions: psychology, physiology, and in vivo functional neuroimaging studies. J. Child. Psychol. Psychiatry 48 (2007) 262-287
172. Takeda S., Kuwabara Y., and Mizuno M. Effects of pregnancy and labor on oxytocin levels in human plasma and cerebrospinal fluid. Endocrinol. Jpn. 32 (1985) 875-880
173. Tanila H., Taira T., Piepponen T.P., and Honkanen A. Effect of sex and age on brain monoamines and spatial learning in rats. Neurobiol. Aging 15 (1994) 733-741
174. Tomizawa K., Iga N., Lu Y.F., Moriwaki A., Matsushita M., Li S.T., et al. Oxytocin improves long-lasting spatial memory during motherhood through MAP kinase cascade. Nat. Neurosci. 6 (2003) 384-390
175. Torner L. Role of prolactin in the behavioral and neuroendocrine stress adaptations during lactation. In: Bridges R.S. (Ed). Neurobiology of the Parental Brain (2007), Elsevier, Burlington 131-143
176. Torvaldsen S., Roberts C.L., Simpson J.M., Thompson J.F., and Ellwood D.A. Intrapartum epidural analgesia and breastfeeding: a prospective cohort study. Int. Breastfeed J. 1 (2006) 24
177. Toth A.L., Varala K., Newman T.C., Miguez F.E., Hutchison S.K., Willoughby D.A., et al. Wasp gene expression supports an evolutionary link between maternal behavior and eusociality. Science 318 (2007) 441-444
178. Tu M.T., Lupien S.J., and Walker C.D. Multiparity reveals the blunting effect of breastfeeding on physiological reactivity to psychological stress. J. Neuroendocrinol. 18 (2006) 494-503
179. Tyler W.J., Alonso M., Bramham C.R., and Pozzo-Miller L.D. From acquisition to consolidation: on the role of brain-derived neurotrophic factor signaling in hippocampal-dependent learning. Learn. Mem. 9 (2002) 224-237
180. Uguz F., Gezginc K., Zeytinci I.E., Karatayli S., Askin R., Guler O., et al. Obsessive-compulsive disorder in pregnant women during the third trimester of pregnancy. Compr. Psychiatry 48 (2007) 441-445
181. Uguz F., Gezginc K., Zeytinci I.E., Karatayli S., Askin R., Guler O., et al. Course of obsessive-compulsive disorder during early postpartum period: a prospective analysis of 16 cases. Compr. Psychiatry 48 (2007) 558-561
182. Vesga-Lopez O., Blanco C., Keyes K., Olfson M., Grant B.F., and Hasin D.S. Psychiatric disorders in pregnant and postpartum women in the United States. Arch. Gen. Psychiatry 65 (2008) 805-815
183. Wartella J., Amory E., Lomas L.M., Macbeth A., McNamara I., Stevens L., et al. Single or multiple reproductive experiences attenuate neurobehavioral stress and fear responses in the female rat. Physiol. Behav. 79 (2003) 373-381
184. Wiesenfeld A.R., Malatesta C.Z., Whitman P.B., Granrose C., and Uili R. Psychophysiological response of breast- and bottle-feeding mothers to their infants' signals. Psychophysiology 22 (1985) 79-86
185. Wiklund I., Norman M., Uvnas-Moberg K., Ransjo-Arvidson A.B., and Andolf E. Epidural analgesia: breast-feeding success and related factors. Midwifery 25 (2009) e31-e38
186. Wilson E.O. The Insect Societies (1971), Belknap, Cambridge
187. Windle R.J., Gamble L.E., Kershaw Y.M., Wood S.A., Lightman S.L., and Ingram C.D. Gonadal steroid modulation of stress-induced hypothalamo-pituitary-adrenal activity and anxiety behavior: role of central oxytocin. Endocrinology 147 (2006) 2423-2431
188. Windle R.J., Wood S., Shanks N., Perks P., Conde G.L., da Costa A.P., et al. Endocrine and behavioural responses to noise stress: comparison of virgin and lactating female rats during non-disrupted maternal activity. J. Neuroendocrinol. 9 (1997) 407-414
189. Winocur G., Moscovitch M., Caruana D.A., and Binns M.A. Retrograde amnesia in rats with lesions to the hippocampus on a test of spatial memory. Neuropsychologia 43 (2005) 1580-1590
190. Ystrom E., Niegel S., Klepp K.I., and Vollrath M.E. The impact of maternal negative affectivity and general self-efficacy on breastfeeding: the Norwegian Mother and Child Cohort Study. J. Pediatr. 152 (2008) 68-72
191. Zuluaga M.J., Agrati D., Pereira M., Uriarte N., Fernandez-Guasti A., and Ferreira A. Experimental anxiety in the black and white model in cycling, pregnant and lactating rats. Physiol. Behav. 84 (2005) 279-286