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

Rodent research suggests that pregnancy, motherhood and attendant offspring care affect changes in neural function and behaviors that are not directly maternal in nature, but involve cognition, affect, and responses to stress. Thus, female rats having had one pregnancy and bout of rearing (primiparous), or multiple pregnancies and bouts of rearing (multiparous), generally show greater resilience to stress, decreased anxiety, and better memory abilities than female rats that have never experienced motherhood (virgin or nulliparous). Moreover, some studies show that these neural changes remain long after the last pregnancy, persisting even into old age. In the current review, we will begin by discussing these behavioral and neural changes in rodents and provide some information concerning their possible mechanisms. Then we will review data from studies examining anxiety and cognition in postpartum human mothers. While this data is less conclusive than that from non-human animals, it appears that reproductive experience may confer some beneficial changes to human mothers in terms of lowering the anxiety/stress response and enhancing certain aspects of memory.

[1]  P. Gustavsson,et al.  Oxytocin, prolactin, milk production and their relationship with personality traits in women after vaginal delivery or Cesarean section. , 1998, Journal of psychosomatic obstetrics and gynaecology.

[2]  M. Numan,et al.  The connections of the medial preoptic region and maternal behavior in the rat , 1980, Physiology & Behavior.

[3]  G. Turner,et al.  Memory loss during pregnancy , 1993, British journal of obstetrics and gynaecology.

[4]  A. Fernández-Guasti,et al.  Experimental anxiety in the black and white model in cycling, pregnant and lactating rats , 2005, Physiology & Behavior.

[5]  K. Lambert,et al.  Motherhood mitigates aging-related decrements in learning and memory and positively affects brain aging in the rat , 2005, Brain Research Bulletin.

[6]  Olfactory recognition of infants in laboratory mice: Role of noradrenergic mechanisms , 1992, Physiology & Behavior.

[7]  A. Douglas,et al.  Adaptive Responses of the Maternal Hypothalamic‐Pituitary‐Adrenal Axis during Pregnancy and Lactation , 2008, Journal of neuroendocrinology.

[8]  A. D. Mayer,et al.  Hormonal basis during pregnancy for the onset of maternal behavior in the rat , 1988, Psychoneuroendocrinology.

[9]  D. Wilkie,et al.  Spatial Working Memory and Hippocampal Size across Pregnancy in Rats , 2000, Hormones and Behavior.

[10]  S. Breedlove,et al.  Got milk? Oxytocin triggers hippocampal plasticity , 2003, Nature Neuroscience.

[11]  V. Glover,et al.  Bmc Pregnancy and Childbirth Open Access Pregnant Women Become Insensitive to Cold Stress , 2022 .

[12]  R. Bridges Neurobiology of the parental brain , 2008 .

[13]  M. Furuta,et al.  Gestation-induced cell proliferation in the rat brain. , 2005, Brain research. Developmental brain research.

[14]  M. Banasr,et al.  Serotonin mediates oestrogen stimulation of cell proliferation in the adult dentate gyrus , 2001, The European journal of neuroscience.

[15]  S. File,et al.  Validation of open : closed arm entries in an elevated plus-maze as a measure of anxiety in the rat , 1985, Journal of Neuroscience Methods.

[16]  O. Almkvist,et al.  Temporary peripartal impairment in memory and attention and its possible relation to oxytocin concentration. , 1990, Life sciences.

[17]  K. Lambert,et al.  Reproduction‐Induced Neuroplasticity: Natural Behavioural and Neuronal Alterations Associated with the Production and Care of Offspring , 2008, Journal of neuroendocrinology.

[18]  M. Altemus,et al.  Changes in cerebrospinal fluid neurochemistry during pregnancy , 2004, Biological Psychiatry.

[19]  K. Karelina,et al.  Motherhood Induces and Maintains Behavioral and Neural Plasticity across the Lifespan in the Rat , 2008, Archives of sexual behavior.

[20]  B. Carr,et al.  Maternal plasma adrenocorticotropin and cortisol relationships throughout human pregnancy. , 1981, American journal of obstetrics and gynecology.

[21]  Jean Golding,et al.  The course of anxiety and depression through pregnancy and the postpartum in a community sample. , 2004, Journal of affective disorders.

[22]  J. Hajnal,et al.  Change in brain size during and after pregnancy: study in healthy women and women with preeclampsia. , 2002, AJNR. American journal of neuroradiology.

[23]  Frank Z. Stanczyk,et al.  Pregnancy, the postpartum, and steroid hormones: effects on cognition and mood , 1999, Psychoneuroendocrinology.

[24]  Samet Kose,et al.  Brain basis of early parent-infant interactions: psychology, physiology, and in vivo functional neuroimaging studies. , 2007, Journal of child psychology and psychiatry, and allied disciplines.

[25]  E. Rüther,et al.  Panic disorder during pregnancy and postpartum period , 2006, European Psychiatry.

[26]  J. Rosenblatt,et al.  Effects of Pregnancy Hormones on Maternal Responsiveness, Responsiveness to Estrogen Stimulation of Maternal Behavior, and the Lordosis Response to Estrogen Stimulation , 1998, Hormones and Behavior.

[27]  A. Fleming,et al.  The effects of adrenalectomy and corticosterone replacement on maternal behavior in the postpartum rat , 2004, Hormones and Behavior.

[28]  R. Bridges Long-term effects of pregnancy and parturition upon maternal responsiveness in the rat , 1975, Physiology & Behavior.

[29]  K. Berkley,et al.  Sex Differences in the Brain: From Genes to Behavior , 2007 .

[30]  Morris Moscovitch,et al.  Retrograde amnesia in rats with lesions to the hippocampus on a test of spatial memory , 2005, Neuropsychologia.

[31]  M. Aldegunde,et al.  Selective changes in the contents of noradrenaline, dopamine and serotonin in rat brain areas during aging , 1999, Journal of Neural Transmission.

[32]  L. Galea,et al.  First reproductive experience persistently affects spatial reference and working memory in the mother and these effects are not due to pregnancy or ‘mothering’ alone , 2006, Behavioural Brain Research.

[33]  E. Nissen,et al.  Postpartum maternal oxytocin release by newborns: effects of infant hand massage and sucking. , 2001, Birth.

[34]  J. Dayan Clinique et épidémiologie des troubles anxieux et dépressifs de la grossesse et du post-partum. Revue et synthèse , 2007 .

[35]  I. Neumann,et al.  Alterations in behavioral and neuroendocrine stress coping strategies in pregnant, parturient and lactating rats. , 2001, Progress in brain research.

[36]  M. W. Brown,et al.  Objective and subjective memory impairment in pregnancy , 1991, Psychological Medicine.

[37]  M. Numan,et al.  Medial preoptic area and maternal behavior in the female rat. , 1974, Journal of comparative and physiological psychology.

[38]  L. Hood,et al.  Isolation and characterization of a corticotropin-releasing hormone-like peptide from human placenta. , 1988, The Journal of clinical endocrinology and metabolism.

[39]  A. Fleming,et al.  Hormonal influences on the duration of postpartum maternal responsiveness in the rat , 1987, Physiology & Behavior.

[40]  Olivier Potvin,et al.  Performance on spatial working memory tasks after dorsal or ventral hippocampal lesions and adjacent damage to the subiculum. , 2006, Behavioral neuroscience.

[41]  S. Lightman,et al.  Gonadal steroid modulation of stress-induced hypothalamo-pituitary-adrenal activity and anxiety behavior: role of central oxytocin. , 2006, Endocrinology.

[42]  R. Morris Developments of a water-maze procedure for studying spatial learning in the rat , 1984, Journal of Neuroscience Methods.

[43]  J. Lonstein Reduced anxiety in postpartum rats requires recent physical interactions with pups, but is independent of suckling and peripheral sources of hormones , 2005, Hormones and Behavior.

[44]  J. Henry,et al.  A review of the impact of pregnancy on memory function , 2007, Journal of clinical and experimental neuropsychology.

[45]  H. Sobajima,et al.  Maternity blues and attachment to children in mothers of full‐term normal infants , 2000 .

[46]  Paul E. Gilbert,et al.  A Behavioral Assessment of Hippocampal Function Based on a Subregional Analysis , 2004, Reviews in the neurosciences.

[47]  J. Lonstein,et al.  MOTHER-INFANT TOUCH, NEUROCHEMISTRY, AND POSTPARTUM ANXIETY , 2008 .

[48]  S. Linnarsson,et al.  Learning Deficit in BDNF Mutant Mice , 1997, The European journal of neuroscience.

[49]  A. Fleming,et al.  Timidity prevents the virgin female rat from being a good mother: Emotionality differences between nulliparous and parturient females , 1981, Physiology & Behavior.

[50]  K. Lambert,et al.  Motherhood and the hormones of pregnancy modify concentrations of hippocampal neuronal dendritic spines , 2006, Hormones and Behavior.

[51]  E. Vuurman,et al.  Differences in cognitive performance during pregnancy and early motherhood , 2006, Psychological Medicine.

[52]  A. Rasia-Filho,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 , 2008, Neuroscience Letters.

[53]  D. Fuerst,et al.  Explicit memory in pregnant women. , 1998, American journal of obstetrics and gynecology.

[54]  R. Askin,et al.  Course of obsessive-compulsive disorder during early postpartum period: a prospective analysis of 16 cases. , 2007, Comprehensive psychiatry.

[55]  V. Luine,et al.  Pregnant rats show enhanced spatial memory, decreased anxiety, and altered levels of monoaminergic neurotransmitters , 2008, Brain Research.

[56]  M. Altemus,et al.  Suppression of hypothalmic-pituitary-adrenal axis responses to stress in lactating women. , 1995, The Journal of clinical endocrinology and metabolism.

[57]  A. Rasia-Filho,et al.  Dendritic spine density of posterodorsal medial amygdala neurons can be affected by gonadectomy and sex steroid manipulations in adult rats: A Golgi study , 2008, Brain Research.

[58]  R. Morris,et al.  Place navigation impaired in rats with hippocampal lesions , 1982, Nature.

[59]  J. Morrell,et al.  Exposure to pups influences the strength of maternal motivation in virgin female rats , 2008, Physiology & Behavior.

[60]  J. Rychnovsky,et al.  A selective review of maternal sleep characteristics in the postpartum period. , 2009, Journal of obstetric, gynecologic, and neonatal nursing : JOGNN.

[61]  M. Leon,et al.  Hormonal induction of maternal behavior in the ovariectomized nulliparous rat. , 1970, Physiology & behavior.

[62]  Sheng-tian Li,et al.  Oxytocin improves long-lasting spatial memory during motherhood through MAP kinase cascade , 2003, Nature Neuroscience.

[63]  P. Cain,et al.  Effects of pregnancy on spatial cognition in female Hooded Long–Evans rats , 2006, Hormones and Behavior.

[64]  L. Galea,et al.  Offspring-exposure reduces depressive-like behaviour in the parturient female rat , 2009, Behavioural Brain Research.

[65]  P. Casey,et al.  Memory in pregnancy. I: Subjective experiences and objective assessment of implicit, explicit and working memory in primigravid and primiparous women. , 1999, Journal of psychosomatic obstetrics and gynaecology.

[66]  E. Keverne,et al.  The importance of olfactory bulb noradrenalin for maternal recognition in sheep , 1985, Physiology & Behavior.

[67]  L. Torner Role of Prolactin in the Behavioral and Neuroendocrine Stress Adaptations During Lactation , 2008 .

[68]  A. Eidelman,et al.  Cognitive deficits in women after childbirth. , 1993, Obstetrics and gynecology.

[69]  A. Widström,et al.  Maternal analgesia during labor disturbs newborn behavior: effects on breastfeeding, temperature, and crying. , 2001, Birth.

[70]  J. Buckwalter,et al.  Pregnancy and post partum: changes in cognition and mood. , 2001, Progress in brain research.

[71]  M. Boccia,et al.  Maternal behavior deficits in nulliparous oxytocin knockout mice , 2006, Genes, brain, and behavior.

[72]  A. Ferreira,et al.  Motivational aspects of maternal anxiolysis in lactating rats , 2005, Psychopharmacology.

[73]  M. Altemus Neuropeptides in Anxiety Disorders , 1995 .

[74]  L. Galea,et al.  Reproductive experience differentially affects spatial reference and working memory performance in the mother , 2006, Hormones and Behavior.

[75]  S. Lightman,et al.  Region-specific reduction in stress-induced c-fos mRNA expression during pregnancy and lactation , 1996, Brain Research.

[76]  Rayson J. Figueira,et al.  Oxytocin receptor activity in the ventrocaudal periaqueductal gray modulates anxiety-related behavior in postpartum rats. , 2008, Behavioral neuroscience.

[77]  A. Walf,et al.  Hippocampal 3α,5α-THP may alter depressive behavior of pregnant and lactating rats , 2004, Pharmacology Biochemistry and Behavior.

[78]  C. Meltzer,et al.  Postpartum depression: The clinical disorder and application of PET imaging research methods. , 2008 .

[79]  I. Izquierdo,et al.  Agents that affect cAMP levels or protein kinase A activity modulate memory consolidation when injected into rat hippocampus but not amygdala. , 1997, Brazilian journal of medical and biological research = Revista brasileira de pesquisas medicas e biologicas.

[80]  M. Altemus,et al.  Chapter 17 Neuroendocrine and emotional changes in the post-partum period , 2001 .

[81]  A. Fleming,et al.  Experience-hormone interactions and maternal behavior in rats , 1990, Physiology & Behavior.

[82]  H. Scharfman,et al.  Effects of multiparity on recognition memory, monoaminergic neurotransmitters, and brain-derived neurotrophic factor (BDNF) , 2008, Hormones and Behavior.

[83]  Christopher Gregg,et al.  Pregnancy-Stimulated Neurogenesis in the Adult Female Forebrain Mediated by Prolactin , 2003, Science.

[84]  M. Altemus,et al.  Integrative Functions of Lactational Hormones in Social Behavior and Stress Management a , 1997, Annals of the New York Academy of Sciences.

[85]  A. Vagnucci,et al.  Suckling-induced attenuation of plasma cortisol concentrations in postpartum lactating women. , 1994, Endocrine research.

[86]  R. Crawley,et al.  Cognition in pregnancy and the first year post-partum. , 2003, Psychology and psychotherapy.

[87]  A. Ahokas,et al.  Effect of oestradiol on postpartum depression , 1999, Psychopharmacology.

[88]  C. Pedersen,et al.  Oxytocin induces maternal behavior in virgin female rats. , 1982, Science.

[89]  A. Fleming,et al.  Effects of maternal hormones on ‘timidity’ and attraction to pup-related odors in female rats , 1989, Physiology and Behavior.

[90]  Mark Olfson,et al.  Psychiatric disorders in pregnant and postpartum women in the United States. , 2008, Archives of general psychiatry.

[91]  H. Würbel,et al.  Variations in the postnatal maternal environment in mice: Effects on maternal behaviour and behavioural and endocrine responses in the adult offspring , 2008, Physiology & Behavior.

[92]  C. Frye,et al.  Estrous cycle, pregnancy, and parity enhance performance of rats in object recognition or object placement tasks. , 2008, Reproduction.

[93]  M. Abou-Saleh,et al.  HORMONAL ASPECTS OF POSTPARTUM DEPRESSION , 1998, Psychoneuroendocrinology.

[94]  Y. Kuwabara,et al.  Effects of pregnancy and labor on oxytocin levels in human plasma and cerebrospinal fluid. , 1985, Endocrinologia japonica.

[95]  Gordon W. Gifford,et al.  Motherhood improves learning and memory , 1999, Nature.

[96]  L. Galea,et al.  The Role of Reproductive Experience on Hippocampal Function and Plasticity , 2008 .

[97]  K. Lambert,et al.  The maternal brain. , 2006, Scientific American.

[98]  S. Maier,et al.  Monoamine neurotransmitters and metabolites during the estrous cycle, pregnancy, and the postpartum period , 1988, Pharmacology Biochemistry and Behavior.

[99]  Erich Seifritz,et al.  Differential sex-independent amygdala response to infant crying and laughing in parents versus nonparents , 2003, Biological Psychiatry.

[100]  M. Tu,et al.  Multiparity Reveals the Blunting Effect of Breastfeeding on Physiological Reactivity to Psychological Stress , 2006, Journal of neuroendocrinology.

[101]  A. Fernández-Guasti,et al.  Maternal condition reduces fear behaviors but not the endocrine response to an emotional threat in virgin female rats , 2008, Hormones and Behavior.

[102]  J. Henry,et al.  Prospective-memory functioning is affected during pregnancy and postpartum , 2008, Journal of clinical and experimental neuropsychology.

[103]  G. Dohanich,et al.  Sex Differences in Cognitive Function in Rodents , 2007 .

[104]  J. Rosenblatt Prepartum and postpartum regulation of maternal behaviour in the rat. , 1975, Ciba Foundation symposium.

[105]  J. Aggleton,et al.  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 , 1997, Experimental Brain Research.

[106]  N. Kakee,et al.  A Six-month Follow-up Study of Maternal Anxiety and Depressive Symptoms among Japanese , 2008, Journal of epidemiology.

[107]  J. Studd,et al.  Transdermal oestrogen for treatment of severe postnatal depression , 1996, The Lancet.

[108]  I. Izquierdo,et al.  BDNF–triggered events in the rat hippocampus are required for both short‐ and long‐term memory formation , 2002, Hippocampus.

[109]  E. Byrnes,et al.  Neuroendocrine and Behavioral Adaptations Following Reproductive Experience in the Female Rat , 2008 .

[110]  Importance of noradrenergic mechanisms in the olfactory bulbs for the maternal behaviour of mice , 1988, Physiology & Behavior.

[111]  C. Granrose,et al.  Psychophysiological response of breast- and bottle-feeding mothers to their infants' signals. , 1985, Psychophysiology.

[112]  P. Dutar,et al.  Motherhood‐induced memory improvement persists across lifespan in rats but is abolished by a gestational stress , 2006, The European journal of neuroscience.

[113]  J. Lonstein Regulation of anxiety during the postpartum period , 2007, Frontiers in Neuroendocrinology.

[114]  J. Goodman Postpartum depression beyond the early postpartum period. , 2004, Journal of obstetric, gynecologic, and neonatal nursing : JOGNN.

[115]  M. Szyf,et al.  Epigenetic Programming of Phenotypic Variations in Reproductive Strategies in the Rat Through Maternal Care , 2008, Journal of neuroendocrinology.

[116]  J. Jolles,et al.  Memory Performance, but not Information Processing Speed, may be Reduced During Early Pregnancy , 2003, Journal of clinical and experimental neuropsychology.

[117]  K. Uvnäs‐Moberg,et al.  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. , 2009, Breastfeeding medicine : the official journal of the Academy of Breastfeeding Medicine.

[118]  M. Linhares,et al.  Maternal anxiety in the pre- and postnatal period: a literature review. , 2007, Revista latino-americana de enfermagem.

[119]  S. Porges,et al.  Responses to Laboratory Psychosocial Stress in Postpartum Women , 2001, Psychosomatic medicine.

[120]  K. Lambert,et al.  Single or multiple reproductive experiences attenuate neurobehavioral stress and fear responses in the female rat , 2003, Physiology & Behavior.

[121]  K. Klepp,et al.  The impact of maternal negative affectivity and general self-efficacy on breastfeeding: the Norwegian Mother and Child Cohort Study. , 2008, The Journal of pediatrics.

[122]  Orna Zagoory-Sharon,et al.  Oxytocin during pregnancy and early postpartum: Individual patterns and maternal–fetal attachment , 2007, Peptides.

[123]  L. Galea,et al.  Effects of steroid hormones on neurogenesis in the hippocampus of the adult female rodent during the estrous cycle, pregnancy, lactation and aging , 2009, Frontiers in Neuroendocrinology.

[124]  A. Rasia-Filho,et al.  Influence of sex, estrous cycle and motherhood on dendritic spine density in the rat medial amygdala revealed by the Golgi method , 2004, Neuroscience.

[125]  G. Winocur,et al.  Functional neuroanatomy of remote episodic, semantic and spatial memory: a unified account based on multiple trace theory , 2005, Journal of anatomy.

[126]  A. Fleming,et al.  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. , 1992, Behavioral and neural biology.

[127]  P. Poindron,et al.  Olfactory regulation of maternal behavior in mammals , 2004, Hormones and Behavior.

[128]  K. Uvnäs‐Moberg,et al.  Epidural analgesia: breast-feeding success and related factors. , 2009, Midwifery.

[129]  J. Studd,et al.  Transdermal oestrogen for treatment of severe postnatal depression , 1996, The Lancet.

[130]  Matthew E Hudson,et al.  Wasp Gene Expression Supports an Evolutionary Link Between Maternal Behavior and Eusociality , 2007, Science.

[131]  J. Wixted,et al.  The effects of pregnancy on memory: Recall is worse but recognition is not , 2009, Journal of clinical and experimental neuropsychology.

[132]  A. Gore,et al.  Aging-Related Changes in Ovarian Hormones, Their Receptors, and Neuroendocrine Function , 2004, Experimental biology and medicine.

[133]  K. Uvnäs‐Moberg,et al.  Influence of oxytocin or epidural analgesia on personality profile in breastfeeding women: a comparative study , 2008, Archives of Women's Mental Health.

[134]  E. Byrnes,et al.  Reproductive experience alters anxiety-like behavior in the female rat , 2006, Hormones and Behavior.

[135]  Flávia Teixeira-Silva,et al.  The anxiolytic effect of pregnancy in rats is reversed by finasteride , 2006, Pharmacology Biochemistry and Behavior.

[136]  L. Galea,et al.  Hippocampal morphology is differentially affected by reproductive experience in the mother. , 2006, Journal of neurobiology.

[137]  Christelle Rochefort,et al.  Enriched Odor Exposure Increases the Number of Newborn Neurons in the Adult Olfactory Bulb and Improves Odor Memory , 2002, The Journal of Neuroscience.

[138]  J. Florido,et al.  Plasma levels of β-endorphin and ACTH during labor and immediate puerperium , 1994 .

[139]  L. Galea,et al.  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 , 2006, Hormones and Behavior.

[140]  Orna Zagoory-Sharon,et al.  Evidence for a Neuroendocrinological Foundation of Human Affiliation , 2007, Psychological science.

[141]  J. Buckwalter,et al.  PREGNANCY HISTORY AND COGNITION DURING AND AFTER PREGNANCY , 2004, The International journal of neuroscience.

[142]  M. Boccia,et al.  Oxytocin antagonism alters rat dams' oral grooming and upright posturing over pups , 2003, Physiology & Behavior.

[143]  R Gervais,et al.  Importance of beta-noradrenergic receptors in the olfactory bulb of sheep for recognition of lambs. , 1990, Behavioral neuroscience.

[144]  A. Fleming,et al.  The effects of adrenalectomy and corticosterone replacement on maternal memory in postpartum rats , 2006, Hormones and Behavior.

[145]  D. Dluzen Age-related changes in monoamines within the olfactory bulbs of the Fischer 344 male rat , 1996, Mechanisms of Ageing and Development.

[146]  J. Rosenblatt,et al.  Olfactory regulation of maternal behavior in rats. I. Effects of olfactory bulb removal in experienced and inexperienced lactating and cycling females. , 1974, Journal of comparative and physiological psychology.

[147]  H. Scharfman,et al.  Estrogen and brain-derived neurotrophic factor (BDNF) in hippocampus: Complexity of steroid hormone-growth factor interactions in the adult CNS , 2006, Frontiers in Neuroendocrinology.

[148]  J. Payne,et al.  A reproductive subtype of depression: conceptualizing models and moving toward etiology. , 2009, Harvard review of psychiatry.

[149]  V. Luine,et al.  Spatial memory deficits in aged rats: contributions of monoaminergic systems , 1990, Brain Research.

[150]  T. Shors,et al.  Learning during motherhood: A resistance to stress , 2006, Hormones and Behavior.

[151]  C. Kirschbaum,et al.  Effects of suckling on hypothalamic-pituitary-adrenal axis responses to psychosocial stress in postpartum lactating women. , 2001, The Journal of clinical endocrinology and metabolism.

[152]  C. Poser,et al.  Benign encephalopathy of pregnancy Preliminary clinical observations , 1986, Acta neurologica Scandinavica.

[153]  N. Lemon,et al.  Dopamine D1/D5 Receptors Gate the Acquisition of Novel Information through Hippocampal Long-Term Potentiation and Long-Term Depression , 2006, The Journal of Neuroscience.

[154]  C. Cotman,et al.  Hippocampal brain‐derived neurotrophic factor gene regulation by exercise and the medial septum , 2002, Journal of neuroscience research.

[155]  E. Gould,et al.  Maternal experience inhibits the production of immature neurons in the hippocampus during the postpartum period through elevations in adrenal steroids , 2007, Hippocampus.

[156]  J. Russell,et al.  The expectant brain: adapting for motherhood , 2008, Nature Reviews Neuroscience.

[157]  C. Salvarani,et al.  Relationship between plasma profiles of oxytocin and adrenocorticotropic hormone during suckling or breast stimulation in women. , 1991, Hormone research.

[158]  G. M. Martin,et al.  A Role for Olfaction in Object Recognition by Normal and Hippocampal-Damaged Rats , 2002, Neurobiology of Learning and Memory.

[159]  S. Lightman,et al.  Endocrine and Behavioural Responses to Noise Stress:Comparison of Virgin and Lactating Female Ratsduring Non‐Disrupted Maternal Activity , 1997, Journal of neuroendocrinology.

[160]  W. Tyler,et al.  From acquisition to consolidation: on the role of brain-derived neurotrophic factor signaling in hippocampal-dependent learning. , 2002, Learning & memory.

[161]  R. Askin,et al.  The prevalence of panic disorder in pregnant women during the third trimester of pregnancy. , 2008, Comprehensive psychiatry.

[162]  C. Klier,et al.  Correlation between serum testosterone levels and peripartal mood states , 2001, Acta obstetricia et gynecologica Scandinavica.

[163]  S. A. Stevenson,et al.  Deletion of corticotropin-releasing factor binding protein selectively impairs maternal, but not intermale aggression , 2008, Neuroscience.

[164]  K. Lambert,et al.  The Neuroeconomics Of Motherhood , 2008 .

[165]  Richard F. Thompson,et al.  Cyclic changes in estradiol regulate synaptic plasticity through the MAP kinase pathway , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[166]  K. Lambert,et al.  Maternal experience produces long-lasting behavioral modifications in the rat. , 2005, Behavioral neuroscience.

[167]  S. C. Butler,et al.  Maternal depressive symptoms affect infant cognitive development in Barbados. , 2000, Journal of child psychology and psychiatry, and allied disciplines.

[168]  E. Wilson The Insect Societies , 1974 .

[169]  Timothy D. Sweeny,et al.  Pup exposure elicits hippocampal cell proliferation in the prairie vole , 2008, Behavioural Brain Research.

[170]  P. Brennan,et al.  NEURAL MECHANISMS OF MAMMALIAN OLFACTORY LEARNING , 1997, Progress in Neurobiology.

[171]  D. Olton,et al.  Spatial memory and hippocampal function , 1979, Neuropsychologia.

[172]  J. Epp,et al.  Endocrine regulation of cognition and neuroplasticity: our pursuit to unveil the complex interaction between hormones, the brain, and behaviour. , 2008, Canadian journal of experimental psychology = Revue canadienne de psychologie experimentale.

[173]  H. Tanila,et al.  Effect of sex and age on brain monoamines and spatial learning in rats , 1994, Neurobiology of Aging.

[174]  A. Eskild,et al.  Depression in postpartum and non‐postpartum women: prevalence and risk factors , 2002, Acta psychiatrica Scandinavica.

[175]  R. Askin,et al.  Obsessive-compulsive disorder in pregnant women during the third trimester of pregnancy. , 2007, Comprehensive psychiatry.

[176]  P. Casey,et al.  Memory in pregnancy. II: Implicit, incidental, explicit, semantic, short-term, working and prospective memory in primigravid, multigravid and postpartum women. , 1999, Journal of Psychosomatic Obstetrics and Gynaecology.

[177]  D. Dluzen,et al.  Age related changes of social memory/recognition in male fischer 344 rats , 1994, Behavioural Brain Research.

[178]  T. Laudański,et al.  Corticotrophin-releasing hormone and ACTH levels in maternal and fetal blood during spontaneous and oxytocin-induced labour. , 2001, European journal of endocrinology.

[179]  Catherine McMahon,et al.  Maternal anxiety during the transition to parenthood: a prospective study. , 2008, Journal of affective disorders.

[180]  S. Lightman,et al.  The Hypothalamic‐Pituitary‐Adrenal Axis Response to Endotoxin is Attenuated During Lactation , 1999, Journal of neuroendocrinology.

[181]  J. Rosenblatt,et al.  Maternal behavior in the virgin and lactating rat. , 1974, Journal of comparative and physiological psychology.

[182]  L. Garcia-Segura,et al.  Early motherhood in rats is associated with a modification of hippocampal function , 2007, Psychoneuroendocrinology.

[183]  K. Lambert,et al.  Pup exposure differentially enhances foraging ability in primiparous and nulliparous rats , 2005, Physiology & Behavior.

[184]  Judy M Simpson,et al.  Intrapartum epidural analgesia and breastfeeding: a prospective cohort study , 2006, International breastfeeding journal.

[185]  I. Neumann,et al.  Maternal Stress Adaptations Peripartum , 2008 .

[186]  L. Galea,et al.  Reproductive experience alters hippocampal neurogenesis during the postpartum period in the dam , 2007, Neuroscience.

[187]  L. Galea,et al.  Reproductive experience alters corticosterone and CBG levels in the rat dam , 2009, Physiology & Behavior.

[188]  R. Askin,et al.  Course of panic disorder during the early postpartum period: a prospective analysis. , 2008, Comprehensive psychiatry.

[189]  I. Neumann,et al.  Brain oxytocin: differential inhibition of neuroendocrine stress responses and anxiety-related behaviour in virgin, pregnant and lactating rats , 1999, Neuroscience.

[190]  S. Subburaju,et al.  Interaction Between Oestrogen and Oxytocin on Hypothalamic‐Pituitary‐Adrenal Axis Activity , 2007, Journal of neuroendocrinology.

[191]  F. Nicoletti,et al.  Maternal Exposure to Low Levels of Corticosterone during Lactation Protects the Adult Offspring against Ischemic Brain Damage , 2007, The Journal of Neuroscience.

[192]  J. Buitelaar,et al.  Physiological stress reactivity in human pregnancy—a review , 2005, Neuroscience & Biobehavioral Reviews.