Effects of brief stress exposure during early postnatal development in Balb/CByJ mice: II. Altered cortical morphology

Developmental Psychobiology

Volumn 54, Issue 7, 2012, Pages 723-735

  Hohmann, C F ^a   Beard, N A ^a   Kari Kari, P ^a   Jarvis, N ^a   Simmons, Q ^a  

^a MORGAN STATE UNIVERSITY   (United States)

Author keywords

Early experience; Neocortex; Rodent; Sex differences; Stress

Indexed keywords

CORTICOSTERONE;

ANIMAL; ANIMAL BEHAVIOR; ARTICLE; BAGG ALBINO MOUSE; BRAIN; BRAIN CORTEX; CASE CONTROL STUDY; FEMALE; MALE; MATERNAL DEPRIVATION; MENTAL STRESS; METABOLISM; MOUSE; NEWBORN; ORGAN SIZE; PATHOLOGY;

ANIMALS; ANIMALS, NEWBORN; BEHAVIOR, ANIMAL; BRAIN; CASE-CONTROL STUDIES; CEREBRAL CORTEX; CORTICOSTERONE; FEMALE; MALE; MATERNAL DEPRIVATION; MICE; MICE, INBRED BALB C; ORGAN SIZE; STRESS, PSYCHOLOGICAL;

ANIMALIA; MUS; RODENTIA;

EID: 84866437381     PISSN: 00121630     EISSN: 10982302     Source Type: Journal    
DOI: 10.1002/dev.21028     Document Type: Article

References (80)

1. Abel, K. M., Drake, R., & Goldstein J. M. (2010). Sex differences in schizophrenia. International Review of Psychiatry, 22(5), 417- 428.
2. Andersen S. L., & Teicher, M. H. (2004). Delayed effects of early stress on hippocampal development. Neuropsychopharmacology, 29(11), 1988- 1993.
3. Anisman H., & Zacharko, R. M. (1982). Depression, the predisposing influence of stress. Behavioral and Brain Sciences, 5, 89- 137.
4. Anisman, H., Zaharia, M. D., Meaney, M. J., & Merali, Z. (1998). Do early life events permanently alter behavioral and hormonal responses to stressors? International Journal of Developmental Neuroscience, 16(3-4), 149- 164.
5. Avishai-Eliner, S., Gilles, E. E., Eghbal-Ahmadi, M., Bar-El, Y., & Baram, T. Z. (2001). Altered regulation of gene and protein expression of hypothalamic-pituitary-adrenal axis components in an immature rat model of chronic stress. Journal of Neuroendocrinology, 13(9), 799- 807.
6. Avishai-Eliner, S., Yi, S.-J., Newth, C. J. L., & Baram, T. Z. (1995). Effects of maternal and sibling deprivation on basal and stress induced hypothalamic-pituitary-adrenal components in the infant rat. Neuroscience Letters, 192, 49- 52.
7. Bakos, J., Duncko, R., Makatsori, A., Pirnik, Z., Kiss, A., & Jezova, D. (2004). Prenatal immune challenge affects growth, behavior, and brain dopamine in offspring. Annals of the New York Academy of Sciences, 1018, 281- 287.
8. Baroncelli, L., Braschi, C., Spolidoro, M., Begenisic, T., Sale, A., & Maffei, L. (2010). Nurturing brain plasticity: Impact of environmental enrichment. Cell Death and Differentiation, 17(7), 1092- 1103.
9. Berger-Sweeney J., & Hohmann, C. F. (1997). Behavioral consequences of abnormal cortical development: Insights into developmental disabilities. Behavioural Brain Research, 86, 121- 142.
10. Bock, J., Gruss, M., Becker, S., & Braun, K. (2005). Experience-induced changes of dendritic spine densities in the prefrontal and sensory cortex: Correlation with developmental time windows. Cerebral Cortex, 15(6), 802- 808.
11. Boylan, C. B., Blue, M. E., & Hohmann, C. F. (2007). Modeling early cortical serotonergic deficits in autism. Behavioural Brain Research, 176, 94- 108.
12. Branchi, I., D'Andrea, I., Sietzema, J., Fiore, M., Di Fausto, V., Aloe, L., & Allleva, E. (2006). Early social enrichment augments adult hippocampal BDNF levels and survival of BrdU-positive cells while increasing anxiety- and "depression"-like behavior. Journal of Neuroscience Research, 83(6), 965- 973.
13. Braun, K., Antemano, R., Helmeke, C., Buchner, M., & Poeggel, G. (2009). Juvenile separation stress induces rapid region- and layer-specific changes in S100ss- and glial fibrillary acidic protein-immunoreactivity in astrocytes of the rodent medial prefrontal cortex. Neuroscience, 160(3), 629- 638.
14. Bredy, T. W., Humpartzoomian, R. A., Cain, D. P., & Meaney, M. J. (2003). Partial reversal of the effect of maternal care on cognitive function through environmental enrichment. Neuroscience, 118(2), 571- 576.
15. Brinks, V., van der Mark, M., de Kloet, R., & Oitzl, M. (2007). Emotion and Cognition in high and low stress sensitive mouse strains: A combined neuroendocrine and behavioral study in BALB/c and C57BL/6J mice. Frontiers in Behavioral Neuroscience, 1, 8.
16. Byers, D. M., Irwin, L. N., Moss, D. E., Sumaya, I. C., & Hohmann, C. F. (2005). Prenatal exposure to the acetylcholinesterase inhibitor methanesulfonyl fluoride alters forebrain morphology and gene expression. Brain Research Developmental Brain Research, 158(1-2), 13- 22.
17. Caldji, C., Diorio, J., & Meaney, M. J. (2000). Variations in maternal care in infancy regulate the development of stress reactivity. Biological Psychiatry, 48(12), 1164- 1174.
18. Champagne, D. L., Bagot, R. C., van Hasselt, F., Ramakers, G., Meaney, M. J., de Kloet, E. R., et al. (2008). Maternal care and hippocampal plasticity: Evidence for experience-dependent structural plasticity, altered synaptic functioning, and differential responsiveness to glucocorticoids and stress. Journal of Neuroscience, 28(23), 6037- 6045.
19. Chapillon, P., Manneche, C., Belzung, C., & Caston, J. (1999). Rearing environmental enrichment in two inbred strains of mice. Behavior Genetics, 29, 41- 46.
20. Courchesne, E., Pierce, K., Schumann, C. M., Redcay, E., Buckwalter, J. A., Kennedy, D. P., et al. (2007). Mapping early brain development in autism. Neuron, 56(2), 399- 413.
21. Comeau, W. L., McDonald, R. J., & Kolb, B. E. (2010). Learning-induced alterations in prefrontal cortical dendritic morphology. Behavioural Brain Research, 214(1), 91- 101.
22. de Kloet, E. R., Joels, M., & Holsboer, F. (2005). Stress and the brain: From adaptation to disease. Nature Reviews Neuroscience, 6(6), 463- 475.
23. Del Angel-Meza, A. R., Ramirez-Cortes, L., Adame-Gonzalez, I. G., Gonzalez Burgos, I., & Beas-Zarate, C. (2002). Cerebral GABA release and GAD activity in protein- and tryptophan-restricted rats during development. International Journal of Developmental Neuroscience, 20(1), 47- 54.
24. Diamond, M. C., Law, F., Rhodes, H., Lindner, B., Rosenzweig, M. R., Krech, D, et al. (1966). Increases in cortical depth and glia numbers in rats subjected to enriched environment. Journal of Comparative Neurology, 128(1), 117- 126.
25. Diamond, M. C. (2001). Response of the brain to enrichment. Anais da Academia Brasileira de Ciencias, 73(2), 211- 220.
26. Ducottet C., & Belzung, C. (2004). Behavior in the elevated plus-maze predicts coping after subchronic mild stress in mice. Physiology and Behavior, 81(3), 417- 426.
27. Eastwood, S. L. (2004). The synaptic pathology of schizophrenia: Is aberant neurodevelopment and plasticity to blame? International Review of Neurobiology, 59, 47- 72.
28. Enthoven, L., de Kloet, E. R., & Oitzl, M. S. (2008). Differential development of stress system (re)activity at weaning dependent on time of disruption of maternal care. Brain Research, 1217, 62- 69.
29. Fombonne, E. (1999). The epidemiology of autism: A review. Psychological Medicine, 29(4), 769- 786.
30. Garoflos, E., Stamatakis, A., Rafrogianni, A., Pondiki, S., & Stylianopoulou, F. (2008). Neonatal handling on the first postnatal day leads to increased maternal behavior and fos levels in the brain of the newborn rat. Developmental Psychobiology, 50(7), 704- 713.
31. Gibb R., & Kolb, B. (2005). Neonatal handling alters brain organization but does not influence recovery from perinatal cortical injury. Behavioral Neuroscience, 119(5), 1375- 1383.
32. Gos, T., Bock, J., Poeggel, G., & Braun, K. (2008). Stress-induced synaptic changes in the rat anterior cingulate cortex are dependent on endocrine developmental time windows. Synapse, 62(3), 229- 232.
33. Greenough, W. T., Juraska, J. M., & Volkmar, F. R. (1979). Maze training effects on dendritic branching in occipital cortex of adult rats. Behavioral and Neural Biology, 26, 287- 297.
34. Heim C., & Nemeroff, C. B. (1999). The impact of early adverse experiences on brain systems involved in the pathophysiology of anxiety and affective disorders. Biological Psychiatry, 46(11), 1509- 1522.
35. Hohmann C. F., & Berger-Sweeney, J. (1998). Sexually dimorphic responses to neonatal basal forebrain lesions in mice: II. Cortical morphology. Journal of Neurobiology, 37(4), 595- 606.
36. Hohmann, C. F., Hodges, A., Beard, N., & Aneni, J. (2012). Effects of brief stress during early postnatal development in Balb/CByJ mice: I. Behavioral characterization. Developmental Psychobiology.
37. Hohmann, C. F., Richardson, C., Pitts, E., & Berger-Sweeney, J. (2000). Neonatal 5, 7-DHT lesions cause sex-specific changes in mouse cortical morphogenesis. Neural Plasticity, 7(4), 213- 232.
38. Hohmann, C. F., Walker, E. M., Boylan, C. B., & Blue, M. E. (2007). Neonatal serotonin depletion alters behavioral responses to spatial change and novelty. Brain Research, 1139, 163- 177.
39. Holmes, A., le Guisquet, A. M., Vogel, E., Millstein, R. A., Leman, S., & Belzung, C. (2005). Early life genetic, epigenetic and environmental factors shaping emotionality in rodents. Neuroscience and Biobehavioral Reviews, 29(8), 1335- 1346.
40. Huot, R. L., Plotsky, P. M., Lenox, R. H., & McNamara, R. K. (2002). Neonatal maternal separation reduces hippocampal mossy fiber density in adult Long Evans rats. Brain Research, 950(1-2), 52- 63.
41. Jeanmonod, D., Rice, F. L., & Van der Loos, H. (1981). Mouse somatosensory cortex: Alterations in the barrelfield following receptor injury at different early postnatal ages. Neuroscience, 6(8), 1503- 1535.
42. Juul-Dam, N., Townsend, J., & Courchesne, E. (2001). Prenatal, perinatal, and neonatal factors in autism, pervasive developmental disorder-not otherwise specified, and the general population. Pediatrics, 107(4), E63.
43. Kaffman A., & Meaney, M. J. (2007). Neurodevelopmental sequelae of postnatal maternal care in rodents: Clinical and research implications of molecular insights. Journal of Child Psychology and Psychiatry, 48(3-4), 224- 244.
44. Kalia, M. (2005). Neurobiological basis of depression: An update. Metabolism, 54( 5 Suppl 1), 24- 27.
45. Kinney, D. K., Munir, K. M., Crowley, D. J., & Miller, A. M. (2008). Prenatal stress and risk for autism. Neuroscience and Biobehavioral Reviews, 32(8), 1519- 1532.
46. Kolb B., & Cioe, J. (2001). Cryoanethesia on postnatal day 1, but not day 10, affects adult behavior and cortical morphology in rats. Brain Research Developmental Brain Research, 130(1), 9- 14.
47. Kolb, B., Cioe, J., & Comeau, W. (2008). Contrasting effects of motor and visual spatial learning tasks on dendritic arborization and spine density in rats. Neurobiology of Learning and Memory, 90(2), 295- 300.
48. Koo, J. W., Park, C. H., Choi, S. H., Kim, N. J., Kim, H., Choe, J. C., et al. (2003). The postnatal environment can counteract prenatal effects on cognitive ability, cell proliferation and synaptic protein expression. FASEB J, 17, 1556- 1582.
49. Knuth E. D., & Etgen, A. M. (2005). Corticosterone secretion induced by chronic isolation in neonatal rats is sexually dimorphic and accompanied by elevated ACTH. Hormones and Behavior, 47(1), 65- 75.
50. Krasnova, I. N., Betts, E. S., Dada, A., Jefferson, A., Ladenheim, B., Becker, K. G., et al. (2007). Neonatal dopamine depletion induces changes in morphogenesis and gene expression in the developing cortex. Neurotoxicity Research, 11(2), 107- 130.
51. Ladd, C. O., Thrivikraman, K. V., Huot, R. L., & Plotsky, P. M. (2005). Differential neuroendocrine responses to chronic variable stress in adult Long Evans rats exposed to handling-maternal separation as neonates. Psychoneuroendocrinology 30(6), 520- 533.
52. Leung A., & Chue, P. (2000). Sex differences in schizophrenia, review of the literature. Acta Psychiatrica Scandinavica 401( Suppl), 3- 38.
53. Levine, S. (2002). Regulation of the hypothalamic-pituitary-adrenal axis in the neonatal rat: The role of maternal behavior. Neurotoxicity Research, 4(5-6), 557- 564.
54. Liu, D., Diorio, J., Francis, D., & Meaney, J. M. (2000). Maternal care, hippocampal synaptogenesis and cognitive development in rats. Nature Neuroscience, 3(8), 799- 806.
55. Liu, D., Diorio, J., Tannenbaum, B., Caldji, C., Francis, D., Freedman, A, et al. (1997). Maternal care, hippocampal glucocorticoid receptors, and hypothalamic-pituitary-adrenal responses to stress. Science, 277(5332), 1659- 1662.
56. McEwen, B. S. (2004). Protection and damage from acute and chronic stress: Allostasis and allostatic overload and relevance to the pathophysiology of psychiatric disorders. Annals of the New York Academy of Sciences, 1032, 1- 7.
57. Meaney, M. J., Diorio, J., Francis, D., Widdowson, J., LaPlante, P., Caldji, C., et al. (1996). Early environmental regulation of forebrain glucocorticoid receptor gene expression: Implications for adrenocortical responses to stress. Developmental Neuroscience, 18(1-2), 49- 72.
58. Meerlo, P., Horwath, K. M., Nagy, G. M., Bohus, B., & Koolhas, J. M. (1999). The influence of postnatal handling on adult neuroendocrine and behavioral stress reactivity. Journal of Neuroendocrinology, 11(12), 925- 933.
59. Moncek, F., Duncko, R., Johansson, B. B., & Jezova, D. (2004). Effect of environmental enrichment on stress related systems in rats. Journal of Neuroendocrinology, 16(5), 423- 431.
60. Musholt, K., Cirillo, G., Cavaliere, C., Rosaria Bianco, M., Bock, J., Helmeke, C., et al. (2009). Neonatal separation stress reduces glial fibrillary acidic protein- and S100beta-immunoreactive astrocytes in the rat medial precentral cortex. Developmental Neurobiology, 69(4), 203- 211.
61. Nunez, J. L., Kim, B. Y., & Juraska, J. M. (1998). Neonatal cryoanesthesia affects the morphology of the visual cortex in the adult rat. Developmental Brain Research, 111(1), 89- 98.
62. Picker, J. D., Yang, R., Ricceri, L., & Berger-Sweeney, J. (2006). An altered neonatal behavioral phenotype in Mecp2 mutant mice. Neuroreport, 17(5), 541- 544.
63. Priebe, K., Brake, W. G., Romeo, R. D., Sisti, H. M., Mueller, A., McEwen, B. S., et al. (2006). Maternal influences on adult stress and anxiety-like behavior in C57BL/6J and BALB/CJ mice: A cross-fostering study. Developmental Psychobiology, 48(1), 95- 96.
64. Rapoport, J. L., Addington, A. M., Frangou, S., & Psych, M. R. (2005). The neurodevelopmental model of schizophrenia: Update 2005. Molecular Psychiatry 10(5), 434- 449.
65. Resnick, O., Miller, M., Forbes, W., Hall, R., Kemper, T., Bronzino, J., et al. (1979). Developmental protein malnutrition: Influences on the central nervous system of the rat. Neuroscience and Biobehavioral Reviews, 3(4), 233- 246.
66. Ricceri, L., Hohmann, C., & Berger-Sweeney, J. (2002). Early neonatal 192 IgG saporin induces learning impairments and disrupts cortical morphogenesis in rats. Brain Research, 954(2), 160- 172.
67. Ricceri, L., Usiello, A., Valanzano, A., Calamandrei, G., Frick, K., & Berger-Sweeney, J. (1999). Neonatal 192 IgG-saporin lesions of basal forebrain cholinergic neurons selectively impair response to spatial novelty in adult rats. Behavioral Neuroscience, 113(6), 1204- 1215.
68. Rosenfeld, P., Suchecki, D., & Levine, S. (1992). Multifactorial regulation of the hypothalamic-pituitary-adrenal axis during development. Neuroscience and Biobehavioral Reviews, 16(4), 553- 568.
69. Rosenzweig M. R., & Bennet, E. L. (1996). Psychobiology of plasticity: Effects of training and experience on brain and behavior. Behaviour Brain Research, 78, 57- 65.
70. Sanchez, M. M., Ladd, C. O., & Plotsky, P. M. (2001). Early adverse experience as a developmental risk factor for later psychopathology: Evidence from rodent and primate models. Development and Psychopathology, 13(3), 419- 449.
71. Sapolsky R. M., & Meaney, M. J. (1986). Maturation of the adrenocortical stress response: Neuroendocrine control mechanisms and the stress hyporesponsive period. Brain Research, 396(1), 64- 76.
72. Schmidt, M. V., Levine, S., Alam, S., Harbich, D., Sterlemann, V., Ganea, K., et al. (2006). Metabolic signals modulate hypothalamic-pituitary-adrenal axis activation during maternal separation of the neonatal mouse. Journal of Neuroendocrinology, 18(11), 865- 874.
73. Seckl J. R., & Meaney, M. J. (2004). Glucocorticoid programming. Annals of the New York Academy of Sciences, 1032, 63- 84.
74. Shanks, N., Griffiths, J., & Anisman, H. (1994). Norepinephrine and serotonin alterations following chronic stressor exposure: Mouse strain differences. Pharmacology, Biochemistry and Behavior, 49(1), 57- 65.
75. Suchecki, D., Rosenfeld, P., & Levine, S. (1993). Maternal regulation of the hypothalamic-pituitary-adrenal axis in the infant rat: The roles of feeding and stroking. Brain Research Developmental Brain Research, 75(2), 185- 192.
76. van Oers, H. J., de Kloet, E. R., Whelan, T., & Levine, S. (1998). Maternal deprivation effect on the infant's neural stress markers is reversed by tactile stimulation and feeding but not by suppressing corticosterone. Journal of Neuroscience, 18(23), 10171- 10179.
77. van Praag, H., Kempermann, G., & Gage, F. H. (2000). Neural consequences of environmental enrichment. Nature Reviews Neuroscience, 1(3), 191- 198.
78. Walsh, R. N. (1981). Effects of environmental complexity and deprivation on brain anatomy and histology: A review. International Journal of Neuroscience, 12(1), 33- 51.
79. Zaharia, M. D., Kulczycki, J., Shanks, N., Meaney, M. J., & Anisman, H. (1996). The effects of early postnatal stimulation on Morris water-maze acquisition in adult mice: Genetic and maternal factors. Psychopharmacology (Berlin), 128(3), 227- 239.
80. Zhang, L. X., Levine, S., Dent, G., Zhan, Y., Xing, G., Okimoto, D., et al. (2002). Maternal deprivation increases cell death in the infant rat brain. Brain Research Developmental Brain Research, 133(1), 1- 11.