Brain and Behavioral Modifications That Accompany the Onset of Motherhood

Parenting

Volumn 12, Issue 1, 2012, Pages 74-88

  Lambert, Kelly G ^a   Kinsley, Craig H ^b  

^a RANDOLPH MACON COLLEGE   (United States)

^b UNIVERSITY OF RICHMOND   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84857175761     PISSN: 15295192     EISSN: 15327922     Source Type: Journal    
DOI: 10.1080/15295192.2012.638868     Document Type: Article

References (100)

1. Barrett, J. and Fleming, A. S. 2011. Annual Research Review: All mothers are not created equal: Neural and psychobiological perspectives on mothering and the importance of individual differences. Journal of Child and Psychology and Psychiatry, 52: 368-397.
2. Birrell, J. M. and Brown, V. J. 2000. Medial frontal cortex mediates perceptual attentional set shifting in the rat. Journal of Neuroscience, 20: 4320-4324.
3. Bodensteiner, K. J., Cain, P., Ray, A. S. and Hamula, L. A. 2006. Effects of pregnancy on spatial cognition in female hooded Long-Evans rats. Hormones and Behavior, 9: 303-314.
4. Bridges, R. S. 2008. Neurobiology of the parental brain, New York, NY: Academic Press.
5. Bridges, R. S., Felicio, L. F., Pellerin, L. J., Stuer, A. M. and Mann, P. E. 1993. Prior parity reduces post-coital diurnal and nocturnal prolactin surges in rats. Life Sciences, 53: 439-445.
6. Bridges, R. S. and Grimm, C. T. 1982. Reversal of morphine disruption of maternal behavior by concurrent treatment with the opiate antagonist naloxone. Science, 218: 166-168.
7. Brunton, P. J. and Russell, J. A. 2008. The expectant brain: Adapting for motherhood. Nature Reviews Neuroscience, 9: 11-25.
8. Brunton, P. J., Russell, J. A. and Douglas, A. J. 2008. Adaptive responses of the maternal hypothalamic-pituitary-adrenal axis during pregnancy and lactation. Journal of Neuroendocrinology, 20: 764-776.
9. Brusco, J., Wittmann, R., de Azevedo, M. S., Lucion, A. B., Franci, C. R., Giovenardi, M., Rasia-Filho, A. A. 2008. 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. Neuroscience Letters, 438: 346-350.
10. Buckwalter, J. G., Buckwalter, D. K., Bluestein, B. W. and Stanczyk, F. Z. 2001. Pregnancy and post partum: Changes in cognition and mood. Progress in Brain Research, 133: 303-319.
11. Buckwalter, J. G., Stanczyk, F. Z., McCleary, C. A., Bluestein, B. W., Buckwalter, D. K. and Rankin, K. P. 1999. Pregnancy, the postpartum, and steroid hormones: Effects on cognition and mood. Psychoneuroendocrinology, 24: 69-84.
12. Byrnes, E. M. and Bridges, R. S. 2006a. Reproductive experience alters anxiety-like behavior in the female rat. Hormones and Behavior, 50: 70-76.
13. Byrnes, E. M. and Bridges, R. S. 2006b. Reproductive experience reduces the sedative, but not anxiolytic effects of diazepam. Psychoneuroendocrinology, 31: 988-996.
14. Cameron, N. M., Shahrokh, D., Del Corpo, A., Dhir, S. K., Szyf, M., Champagne, F. A., Meaney, M. J. 2008. Epigenetic programming of phenotypic variations in reproductive strategies in the rat through maternal care. Journal of Neuroendocrinology, 20: 795-801.
15. Corter, C. M. and Fleming, A. S. 2002. "Psychobiology of maternal behavior in human beings". In Handbook of parenting, Edited by: Bornstein, M. H. 87-116. Mahwah, NJ: Erlbaum.
16. De Brito Faturi, C., Teixeira-Silva, F. and Leite, J. G. 2006. The anxiolytic effect of pregnancy in rats is reversed by finasteride. Pharmacology, Biochemistry and Behavior, 85: 569-574.
17. De Weerth, C. and Buitelaar, J. K. 2005. Physiological stress reactivity in human pregnancy-A review. Neuroscience and Biobehavioral Reviews, 29: 295-312.
18. Fahrbach, S. E. and Pfaff, D. W. 1986. Effect of preoptic region implants of dilute estradiol on the maternal behavior of ovariectomized, nulliparous rats. Hormones and Behavior, 20: 354-363.
19. Fleming, A. S., Gonzalez, A., Afonso, V. M. and Lovic, V. 2008. "Plasticity in the maternal neural circuit: Experience, dopamine, and mothering". In Neurobiology of the parental brain, Edited by: Bridges, R. S. 519-535. New York, NY: Academic Press.
20. Fleming, A. S. and Rosenblatt, J. S. 1974. Maternal behavior in the virgin and lactating rat. Journal of Comparative and Physiological Psychology, 86: 957-972.
21. Fullgrabe, U. 2002. Psychologie der eigensicherung: Uberleben ist kein zufall [The psychology of self-protection: Survival is not an accident], Stuttgard, Germany: Verlag.
22. Galea, L. A., Ormerod, B. K., Sampath, S., Kostaras, X., Wilkie, D. M. and Phelps, M. T. 2000. Spatial working memory and hippocampal size across pregnancy in rats. Hormones and Behavior, 37: 86-95.
23. Gatewood, J. D., Morgan, M. D., Eaton, M., McNamara, I. M., Stevens, L. F., Macbeth, A. H., Kinsley, C. H. 2005. Motherhood mitigates aging-related decrements in learning and memory. Brain Research Bulletin, 66: 91-98.
24. Glynn, L. 2010. Giving birth to a new brain: Hormone exposures of pregnancy influence human memory. Psychoneuroendocrinology, 35: 1148-1155.
25. Gonzalez-Mariscal, G. and Kinsley, C. H. 2009. "From indifference to ardor: The onset, maintenance and meaning of the maternal brain". In Hormones, brain and behavior, 2nd, Edited by: Pfaff, D. W., Arnold, A. P., Etgen, A. M., Fahrbach, S. E. and Rubin, R. T. Vol. 1, 109-136. San Diego, CA: Academic Press.
26. Gubernick, D. 1981. "Parent and infant attachment in mammals". In Parental care in mammals, Edited by: Gubernick, D. and Klopfer, P. 243-305. New York, NY: Plenum Press.
27. Gubernick, D. and Klopfer, P. 1981. Parental care in mammals, New York, NY: Plenum Press.
28. Gubernick, D., Sengelaub, D. R. and Kurz, E. M. 1993. A neuroanatomical correlate of paternal behavior in the biparental California mouse (Peromyscus californicus). Behavioral Neuroscience, 107: 194-201.
29. Higgins, T., Everette, A., Fleming, D., Christon, L., Kinsley, C. H. and Lambert, K. G. June 2007. Maternal experience enhances neurobiological and behavioral responses in at attention set-shifting paradigm, June, Rio de Janeiro, Brazil: Poster presented at the International Behavioral Neuroscience Society.
30. Jacobs, L. F., Gaulin, S. J. C., Sherry, D. F. and Hoffman, G. E. 1990. Evolution of spatial cognition: Sex-specific patterns of spatial behavior predict hippocampal size. Proceedings of the National Academy of Sciences, 87: 6349-6352.
31. Janes, C., Casey, P., Huntsdale, C. and Angus, G. 1999. Memory in pregnancy. I: Subjective experiences and objective assessment of implicit, explicit and working memory in primigravid and primiparous women. Journal of Psychosomatic Obstetrics and Gynaecology, 20: 80-87.
32. Joels, M., Hesen, W., Karst, H. and de Kloet, E. R. 1994. Steroids and electrical activity in the brain. Journal of Steroid Biochemistry and Molecular Biology, 49: 391-398.
33. Kesner, R. P. and Dakis, M. 1995. Phencyclidine injections into the dorsal hippocampus disrupt long-term, but not short-term memory within a spatial learning task. Psychopharmacology, 120: 203-208.
34. Keverne, E. B. and Kendrick, K. M. 1990. "Neurochemical changes accompanying parturition and their significance for maternal behavior". In Mammalian parenting: Biochemical, neurobiological, and behavioral determinants, Edited by: Krasnegor, N. A. and Bridges, R. S. 281-304. New York, NY: Oxford University Press.
35. Keyser-Marcus, L., Stafisso-Sandoz, G., Gerecke, K., Jasnow, A., Nightingale, L., Lambert, K. G., Kinsley, C. H. 2001. Alterations of medial preoptic area neurons following pregnancy and pregnancy-like steroidal treatment in the rat. Brain Research Bulletin, 55: 737-745.
36. Kim, P., Leckman, J. F., Mayes, L. C., Feldman, R., Wang, X. and Swain, J. E. 2010. The plasticity of human maternal brain: Longitudinal changes in brain anatomy during the early postpartum period. Behavioral Neuroscience, 124: 695-700.
37. Kinsley, C. H. 1994. Developmental psychobiological influences on rodent parental behavior. Neuroscience and Biobehavioral Reviews, 18: 269-280.
38. Kinsley, C. H., Bardi, M., Karelina, K., Rima, B., Christon, L., Friedenberg, J. and Griffin, G. 2008. Motherhood induces and maintains behavioral and neural plasticity across the lifespan in the rat. Archives of Sexual Behavior, 37: 43-56.
39. Kinsley, C. H., Bardi, M., Karelina, K., Rima, B., Christon, L., Friedenberg, J., Lambert, K. G. November 2006. Track, attack, consume: Pregnancy/parenthood induction of an improved predatory behavioral repertoire and accompanying neural enhancements in the rat, November, Atlanta, Georgia: Paper presented at the Society for Neuroscience Annual Meeting.
40. Kinsley, C. H. and Bridges, R. S. 1988. Parity associated reductions in behavioral sensitivity to opiates. Biology of Reproduction, 39: 270-278.
41. Kinsley, C. H. and Bridges, R. S. 1990. Morphine and reproductive condition alter olfactory preferences for pup and adult male odors in female rats. Developmental Psychobiology, 23: 331-347.
42. Kinsley, C. H., Kary, N. E., Hester, N. W., McNamara, I. M., Lambert, K. G. 2011. The mother as hunter: Significant reduction of foraging costs through enhancements of predation in maternal rats. Manuscript in preparation
43. Kinsley, C. H. and Lambert, K. G. 2006. The maternal brain: Pregnancy and motherhood change the structure of the female mammal's brain, making mothers attentive to their young and better at caring for them. Scientific American, 294 January: 72-79.
44. Kinsley, C. H. and Lambert, K. G. 2008. Reproduction-induced neuroplasticity: Natural behavioral and neuronal alterations associated with the production and care of offspring. Journal of Neuroendocrinology, 20: 515-525.
45. Kinsley, C. H., Madonia, L., Gifford, G. W., Tureski, K., Griffin, G. R., Lowry, C., Lambert, K. G. 1999. Motherhood improves learning and memory: Neural activity in rats is enhanced by pregnancy and the demands of rearing offspring. Nature, 402: 137-138.
46. Kinsley, C. H., Trainer, R., Stafisso-Sandoz, G., Quadros, P., Keyser-Marcus, L., Hearon, C., Lambert, K. G. 2006. Motherhood and pregnancy hormones modify concentrations of hippocampal neuronal dendritic spines. Hormones and Behavior, 49: 131-142.
47. Kuno, M. 1995. The synapse: Function, plasticity, and neurotrophism, New York, NY: Oxford University Press.
48. Lambert, K. G., Berry, A. E., Griffins, G., Amory-Meyers, L., Madonia-Lomas, L., Love, G. and Kinsley, C. H. 2005. Pup exposure differentially enhances foraging ability in primiparous and nulliparous rats. Physiology and Behavior, 84: 799-806.
49. Lambert, K. G. and Kinsley, C. H. 2008. "The neuroeconomics of motherhood: The costs and benefits of maternal investment". In The neurobiology of the parental brain, Edited by: Bridges, R. S. 481-492. New York, NY: Academic Press.
50. Lenzi, D., Trentini, C., Pantano, P., Macaluso, E., Iacoboni, M., Lenzi, G. I. and Ammaniti, M. 2009. Neural basis of maternal communication and emotional expression processing during infant preverbal stage. Cerebral Cortex, 19: 1124-1133.
51. Levitan, I. B. and Kaczmarek, L. K. 1991. The neuron: Cell and molecular biology, New York, NY: Oxford University Press.
52. Liu, Z., Gastard, M., Verina, T., Bora, S., Mouton, P. R. and Koliatsos, V. E. 2001. Estrogens modulate experimentally induced apoptosis of granule cells in the adult hippocampus. Journal of Comparative Neurology, 441: 1-8.
53. Lonstein, J. S. 2007. Regulation of anxiety during the postpartum period. Frontiers in Neuroendocrinology, 28: 15-41.
54. Lorberbaum, J. P., Newman, J. D., Dubno, J. R., Horwitz, A. R., Nahas, Z., Teneback, C. C., George, M. S. 1999. Feasibility of using fMRI to study mothers Responding to infant cries. Depression and Anxiety, 10: 99-104.
55. Love, G., Torrey, N., McNamara, I., Morgan, M., Banks, M., Hester, N. W., Lambert, K. G. 2005. Maternal experience produces long-lasting behavioral modifications in the rat. Behavioral Neuroscience, 119: 1084-1096.
56. Macbeth, A. H., Gautreaux, C. and Luine, V. N. 2008. Pregnant rats show enhanced spatial memory, decreased anxiety, and altered levels of monoamingergic neurotransmitters. Brain Research, 19: 136-147.
57. Macbeth, A. H. and Luine, V. N. 2010. Changes in anxiety and cognition due to reproductive experience: A review of data from rodent and human mothers. Neuroscience and Biobehavioral Reviews, 34: 452-467.
58. MacLean, P. D. 1990. The Triune brain in evolution, New York, NY: Academic Press.
59. MacLean, P. D. and Newman, J. D. 1988. Role of midline frontolimbic cortex in production of the isolation call of squirrel. Brain Research, 450: 111-123.
60. Mann, P. E. and Bridges, R. S. 1992. Neural and endocrine sensitivities decline as a function of multiparity in the rat. Brain Research, 580: 241-248.
61. McEwen, B. S. 1991. Steroids affect neural activity by acting on the membrane and the genome. Trends in Pharmacological Science, 12: 141-147.
62. McEwen, B. S. and Woolley, C. S. 1994. Estradiol and progesterone regulate neuronal structure and synaptic connectivity in adult as well as developing brain. Experimental Gerontology, 29: 431-436.
63. Moltz, H., Lubin, M., Leon, M. and Numan, M. 1970. Hormonal induction of maternal behavior in the ovariectomized nulliparous rat. Physiology and Behavior, 5: 1373-1377.
64. Murphy, M. R., MacLean, P. D. and Hamilton, S. C. 1981. Species-typical behavior of hamsters deprived from birth of the neocortex. Science, 213: 459-461.
65. Numan, M. 1974. Medial preoptic area and maternal behavior in the female rat. Journal of Comparative and Physiological Psychology, 87: 746-759.
66. Numan, M. and Insel, T. R. 2003. The neurobiology of parental behavior, New York, NY: Springer-Verlag.
67. Numan, M. and Numan, M. J. 1995. 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. Behavioral Neuroscience, 109: 135-149.
68. Numan, M., Rosenblatt, J. S. and Komisaruk, B. R. 1977. Medial preoptic area and onset of maternal behavior in the rat. Journal of Comparative and Physiological Psychology, 91: 146-164.
69. Oatridge, A., Holdcroft, A., Saeed, N., Hajnal, J. V., Puri, B. K., Fusi, L. and Bydder, G. M. 2002. Change in brain size during and after pregnancy: Study in healthy women and women with preeclampsia. American Journal of Neuroradiology, 23: 19-26.
70. Orpen, B. G., Furman, N., Wong, P. Y. and Fleming, A. S. 1987. Hormonal influences on the duration of postpartum maternal responsiveness in the rat. Physiology and Behavior, 40: 307-315.
71. Pawluski, J. L. and Galea, L. A. 2005. Hippocampal morphology is differentially affected by reproductive experience in the mother. Journal of Neurobiology, 66: 71-81.
72. Pawluski, J. L., Vanderbyl, B. L., Ragan, K. and Galea, L. A. 2006. First reproductive experience persistently affects spatial reference and working memory in the mother and these effects are not due to pregnancy or 'mothering' alone. Behavioural Brain Research, 175: 157-165.
73. Pawluski, J. L., Walker, S. K. and Galea, L. A. 2006. Reproductive experience differentially affects spatial reference and working memory performance in the mother. Hormones and Behavior, 49: 143-149.
74. Pearson, R. M., Lightman, S. L. and Evans, J. 2009. Emotional sensitivity for motherhood: Late pregnancy is associated with enhanced accuracy to encode emotional faces. Hormones and Behavior, 56: 557-563.
75. Pedersen, C. A., Vadlamudi, S. V., Boccia, M. L. and Amico, J. A. 2006. Maternal behavior deficits in nulliparous oxytocin knockout mice. Genes Brain and Behavior, 5: 274-281.
76. Pellow, S., Chopin, P., File, S. E. and Briley, M. 1985. Validation of open:closed arm entries in an elevated plus-maze as a measure of anxiety in the rat. Journal of Neuroscience Methods, 14: 149-167.
77. Pfaff, D. W. 1981. "Electrophysiological effects of steroid hormones in brain tissue". In Neuroendocrinology of reproduction: Physiology and behavior, Edited by: Adler, N. T. 533-544. New York, NY: Plenum Press.
78. Pfaff, D. W. 1989. Patterns of steroid hormone effects on electrical and molecular events in hypothalamic neurons. Molecular Neurobiology, 3: 135-154.
79. Poser, C. M., Kassirer, M. R. and Peyser, J. M. 1986. Benign encephalopathy of pregnancy. Preliminary clinical observations. Acta Neurolgica Scandinavica, 73: 39-43.
80. Rasia-Filho, A. A., Fabian, C., Rigoti, K. M. and Achaval, M. 2004. Influence of sex, estrous cycle and motherhood on dendritic spine density in the rat medial amygdala revealed by the Golgi method. Neuroscience, 126: 839-847.
81. Rosenblatt, J. S. 1975. Prepartum and postpartum regulation of maternal behaviour in the rat. Ciba Foundation Symposium, 33: 17-37.
82. Rosenblatt, J. S., Mayer, A. D. and Giordano, A. L. 1988. Hormonal basis during pregnancy for the onset of maternal behavior in the rat. Psychoneuroendocrinology, 13: 29-46.
83. Rosenblatt, J. S., Olufowobi, A. and Siegel, H. I. 1998. Effects of pregnancy hormones on maternal responsiveness, responsiveness to estrogen stimulation of maternal behavior, and the lordosis response to estrogen stimulation. Hormones and Behavior, 33: 104-114.
84. Seifritz, E., Esposito, F., Neuhoff, J. G., Luthi, A., Mustovic, H., Dammann, G., DiSalle, F. 2003. Differential sex-independent amygdale response to infant crying and laughing in parents versus nonparents. Biological Psychiatry, 54: 1367-1375.
85. Seip, K. M. and Morrell, J. I. 2008. Exposure to pups influences the strength of maternal motivation in virgin female rats. Physiology and Behavior, 95: 599-608.
86. Silber, M., Almkvist, O., Larsson, B. and Uvnas-Moberg, K. 1990. Temporary peripartal impairment in memory and attention and its possible relation to oxytocin concentration. Life Sciences, 47: 57-65.
87. Slotnick, B. M. and Nigrosh, B. J. 1975. Maternal behavior of mice with cingulate cortical, amygdala, or septal lesions. Journal of Comparative and Physiological Psychology, 88: 118-127.
88. Stamm, J. S. 1955. The function of median cerebral cortex in maternal behavior of rats. Journal of Comparative and Physiological Psychology, 48: 347-356.
89. Svare, B. and Gandelman, R. 1976. Suckling stimulation induces aggression in virgin female mice. Nature, 260: 606-608.
90. Swain, J. E. 2008. Interpretations of the brain imaging of early parent-infant interactions. Psychiatry, 5: 28-36.
91. Swain, J. E. 2011. The human parental brain: In vivo neuroimaging. Progress in Neuropsychopharmacology and Biological Psychiatry, 35: 1242-1254.
92. Swain, J. E. and Lorberbaum, J. P. 2008. "Imaging the human parental brain". In Neurobiology of the parental brain, Edited by: Bridges, R. S. 83-100. New York, NY: Academic Press.
93. Swain, J. E., Lorberbaum, J. P., Kose, S. and Strathearn, L. 2007. Brain basis of early parent-infant interactions: Psychology, physiology, and in vivo functional neuroimaging studies. Journal of Child Psychology and Psychiatry, 48: 262-287.
94. Swain, J. E., Tasgin, E., Mayes, L. C., Feldman, R., Constable, R. T. and Leckman, J. F. 2008. Cesarean delivery affects maternal brain responses to own baby cry. Journal of Child Psychology and Psychiatry, 49: 1042-1052.
95. Terkel, J. and Rosenblatt, J. S. 1968. Maternal behavior induced by maternal blood plasma injected into virgin rats. Journal of Comparative and Physiological Psychology, 65: 369-380.
96. Wartella, J., Amory, E., MacBeth, A. H., McNamara, I., Stevens, L., Madonia, L., Kinsley, C. H. 2003. Single or multiple reproductive experiences attenuate neurobehavioral stress and fear responses in the female rat. Physiology and Behavior, 79: 373-381.
97. Wiesner, B. P. and Sheard, N. M. 1933. Maternal behavior in the rat, London, England: Oliver & Boyd.
98. Woolley, C. S. 1998. Estrogen-mediated structural and functional synaptic plasticity in the female rat hippocampus. Hormones and Behavior, 34: 140-148.
99. Woolley, C. S., Gould, E., Frankfurt, M. and McEwen, B. S. 1990. Naturally occurring fluctuation in dendritic spine density on adult hippocampal pyramidal neurons. Journal of Neuroscience, 10: 4035-4039.
100. Woolley, C. S. and McEwen, B. S. 1993. Roles of estradiol and progesterone in the regulation of hippocampal dendritic spine density during the estrous cycle in the rat. Journal of Comparative Neurology, 336: 293-306.