Maternal separation disrupts dendritic morphology of neurons in prefrontal cortex, hippocampus, and nucleus accumbens in male rat offspring

Journal of Chemical Neuroanatomy

Volumn 40, Issue 2, 2010, Pages 93-101

  Monroy, Elibeth ^a   Hernández Torres, Elizabeth ^a   Flores, Gonzalo ^a  

^a BENEMÉRITA UNIVERSIDAD AUTÓNOMA DE PUEBLA   (Mexico)

Author keywords

Golgi Cox stain; Human handling; Locomotor activity; Maternal separation; Neurodevelopment; Schizophrenia

Indexed keywords

ADULTHOOD; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL DENSITY; CELL STRUCTURE; CONTROLLED STUDY; DENDRITIC CELL; FEMALE; GOLGI STAIN; HIPPOCAMPUS; LOCOMOTION; MALE; MATERNAL CARE; MATERNAL DEPRIVATION; MOOD DISORDER; NERVE CELL; NONHUMAN; NUCLEUS ACCUMBENS; PREFRONTAL CORTEX; PREPUBERTY; PRIORITY JOURNAL; PROGENY; PYRAMIDAL NERVE CELL; RAT; ANALYSIS OF VARIANCE; ANIMAL; CELL SHAPE; CYTOLOGY; DENDRITE; DENDRITIC SPINE; MOTOR ACTIVITY; SILVER STAINING; SPRAGUE DAWLEY RAT;

ANALYSIS OF VARIANCE; ANIMALS; CELL SHAPE; DENDRITES; DENDRITIC SPINES; HIPPOCAMPUS; MALE; MATERNAL DEPRIVATION; MOTOR ACTIVITY; NEURONS; NUCLEUS ACCUMBENS; PREFRONTAL CORTEX; RATS; RATS, SPRAGUE-DAWLEY; SILVER STAINING;

EID: 77954816724     PISSN: 08910618     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jchemneu.2010.05.005     Document Type: Article

References (94)

1. Alquicer G., Morales-Medina J.C., Quirion R., Flores G. Postweaning social isolation enhances morphological changes in the neonatal ventral hippocampal lesion rats. J. Chem. Neuroanat. 2008, 35:179-187.
2. Andersen S.L., Teicher M.H. Delayed effects of early stress on hippocampal development. Neuropsychopharmacology 2004, 29:1988-1993.
3. Aylward R.L., Totterdell S. Neurons in the ventral subiculum, amygdala and entorhinal cortex which project to the nucleus accumbens: their input from somatostatin-immunoreactive boutons. J. Chem. Neuroanat. 1993, 6:31-42.
4. Bebbington P.E., Bhugra D., Brugha T., Singleton N., Farrell M., Jenkins R., Lewis G., Meltzer H. Psychosis, victimization and childhood disadvantage: evidence from the second British National Survey of Psychiatric Morbidity. Br. J. Psychiatry 2004, 185:220-226.
5. Bock J., Gruss M., Becker S., Braun K. Experience-induced changes of dendritic spine densities in the prefrontal and sensory cortex: correlation with developmental time windows. Cereb. Cortex 2005, 15:802-808.
6. Brake W.G., Zhang T.Y., Diorio J., Meaney M.J., Gratton A. Influence of early postnatal rearing conditions on mesocorticolimbic dopamine and behavioural responses to psychostimulants and stressors in adult rats. Eur. J. Neurosci. 2004, 19:1863-1874.
7. Burton C.L., Chatterjee D., Chatterjee-Chakraborty M., Lovic V., Grella S.L., Steiner M., Fleming A.S. Prenatal restraint stress and motherless rearing disrupts expression of plasticity markers and stress-induced corticosterone release in adult female Sprague-Dawley rats. Brain Res. 2007, 1158:28-38.
8. Bremner J.D., Randall P., Vermetten E., Staib L., Bronen R.A., Mazure C., Capelli S., McCarthy G., Innis R.B., Charney D.S. Magnetic resonance imaging-based measurement of hippocampal volume in posttraumatic stress disorder related to childhood physical and sexual abuse-a preliminary report. Biol. Psychiatry 1997, 41:23-32.
9. A and central benzodiazepine receptor levels and novelty-induced fearfulness in the rat. Neuropsychopharmacology 2000, 22:219-229.
10. Cerqueira J.J., Taipa R., Uylings H.B., Almeida O.F., Sousa N. Specific configuration of dendritic degeneration in pyramidal neurons of the medial prefrontal cortex induced by differing corticosteroid regimens. Cereb. Cortex 2007, 17:1998-2006.
11. Champagne F.A. Epigenetic mechanisms and the transgenerational effects of maternal care. Front. Neuroendocrinol. 2008, 29:386-397.
12. D'Amato F.R., Scalera E., Sarli C., Moles A. Pups call, mothers rush: does maternal responsiveness affect the amount of ultrasonic vocalizations in mouse pups?. Behav. Genet. 2005, 35:103-112.
13. Daniels W.M., Pietersen C.Y., Carstens M.E., Stein D.J. Maternal separation in rats leads to anxiety-like behavior and a blunted ACTH response and altered neurotransmitter levels in response to a subsequent stressor. Metab. Brain Dis. 2004, 19:3-14.
14. Faure J., Uys J.D., Marais L., Stein D.J., Daniels W.M. Early maternal separation alters the response to traumatization: resulting in increased levels of hippocampal neurotrophic factors. Metab. Brain Dis. 2007, 22:183-195.
15. Faure J., Uys J.D., Marais L., Stein D.J., Daniels W.M. Early maternal separation followed by later stressors leads to dysregulation of the HPA-axis and increases in hippocampal NGF and NT-3 levels in a rat model. Metab. Brain Dis. 2006, 21:181-188.
16. Flores G., Alquicer G., Silva-Gomez A.B., Zaldivar G., Stewart J., Quirion R., Srivastava L.K. Alterations in dendritic morphology of prefrontal cortical and nucleus accumbens neurons in post-pubertal rats after neonatal excitotoxic lesions of the ventral hippocampus. Neuroscience 2005, 133:463-470.
17. Flores G., Barbeau D., Quirion R., Srivastava L.K. Decreased binding of dopamine D3 receptors in limbic subregions after neonatal bilateral lesion of rat hippocampus. J. Neurosci. 1996, 16:2020-2026.
18. Francis D.D., Meaney M.J. Maternal care and the development of stress responses. Curr. Opin. Neurobiol. 1999, 9:128-134.
19. Freund T.F., Powell J.F., Smith A.D. Tyrosine hydroxylase-immunoreactive boutons in synaptic contact with identified striatonigral neurons, with particular reference to dendritic spines. Neuroscience 1984, 13:1189-1215.
20. Freyd J.J., Putnam F.W., Lyon T.D., Becker-Blease K.A., Cheit R.E., Siegel N.B., Pezdek K. Psychology. The science of child sexual abuse. Science 2005, 308:501.
21. Gibb R., Kolb B. A method for vibratome sectioning of Golgi-Cox stained whole rat brain. J. Neurosci. Methods 1998, 79:1-4.
22. Greisen M.H., Altar C.A., Bolwig T.G., Whitehead R., Wörtwein G. Increased adult hippocampal brain-derived neurotrophic factor and normal levels of neurogenesis in maternal separation rats. J. Neurosci. Res. 2005, 79:772-778.
23. Groves P.M., Linder J.C., Young S.J. 5-Hydroxydopamine-labeled dopaminergic axons: three-dimensional reconstructions of axons, synapses and postsynaptic targets in rat neostriatum. Neuroscience 1994, 58:593-604.
24. Gos T., Bock J., Poeggel G., Braun K. Stress-induced synaptic changes in the rat anterior cingulate cortex are dependent on endocrine developmental time windows. Synapse 2008, 62:229-232.
25. Heidbreder C.A., Groenewegen H.J. The medial prefrontal cortex in the rat: evidence for a dorso-ventral distinction based upon functional and anatomical characteristics. Neurosci. Biobehav. Rev. 2003, 27:555-579.
26. Heim C., Nemeroff C.B. The role of childhood trauma in the neurobiology of mood and anxiety disorders: preclinical and clinical studies. Biol. Psychiatry 2001, 49:1023-1039.
27. Heim C., Nemeroff C.B. Neurobiology of early life stress: clinical studies. Semin. Clin. Neuropsychiatry 2002, 7:147-159.
28. Helmeke C., Ovtscharoff W., Poeggel G., Braun K. Juvenile emotional experience alters synaptic inputs on pyramidal neurons in the anterior cingulate cortex. Cereb. Cortex 2001, 11:717-727.
29. Herman J.P., Mueller N.K. Role of the ventral subiculum in stress integration. Behav. Brain Res. 2006, 174:215-224.
30. Holsboer F. The corticosteroid receptor hypothesis of depression. Neuropsychopharmacology 2000, 23:477-501.
31. Hofer M.A. Early relationships as regulators of infant physiology and behavior. Acta Paediatr. Suppl. 1994, 397:9-18.
32. Horner C.H., O'Regan M., Arbuthnott E. Neural plasticity of the hippocampal (CA1) pyramidal cell-quantitative changes in spine density following handling and injection for drug testing. Anatomy 1991, 174:229-238.
33. Jaworska N., Dwyer S.M., Rusak B. Repeated neonatal separation results in different neurochemical and behavioral changes in adult male and female Mongolian gerbils. Pharmacol. Biochem. Behav. 2008, 88:533-541.
34. Jay T.M., Witter M.P. Distribution of hippocampal CA1 and subicular efferents in the prefrontal cortex of the rat studied by means of anterograde transport of phaseolus vulgaris-leucoagglutinin. J. Comp. Neurol. 1991, 313:574-586.
35. Juarez I., Gratton A., Flores G. Ontogeny of altered dendritic morphology in the rat prefrontal cortex, hippocampus and nucleus accumbens following Caesarean delivery and birth anoxia. J. Comp. Neurol. 2008, 507:1734-1747.
36. Kaffman A., Meaney M.J. Neurodevelopmental sequelae of postnatal maternal care in rodents: clinical and research implications of molecular insights. J. Child Psychol. Psychiatry 2007, 48:224-244.
37. Kalb R.G. Regulation of motor neuron dendrite growth by NMDA receptor activation. Development 1994, 120:3063-3071.
38. Kikusui T., Mori Y. Behavioural and neurochemical consequences of early weaning in rodents. J. Neuroendocrinol. 2009, 21:427-431.
39. Knuth E.D., Etgen A.M. Long-term behavioral consequences of brief, repeated neonatal isolation. Brain Res. 2007, 1128:139-147.
40. Kuhn C.M., Schanberg S.M. Responses to maternal separation: mechanisms and mediators. Int. J. Dev. Neurosci. 1998, 16:261-270.
41. Ladd C.O., Huot R.L., Thrivikraman K.V., Nemeroff C.B., Plotsky P.M. Long-term adaptations in glucocorticoid receptor and mineralocorticoid receptor mRNA and negative feedback on the hypothalamo-pituitary-adrenal axis following neonatal maternal separation. Biol. Psychiatry 2004, 55:367-375.
42. Lehmann J., Feldon J. Long-term biobehavioral effects of maternal separation in the rat: consistent or confusing?. Rev. Neurosci. 2000, 11:383-408.
43. Levine S. Influence of psychological variables on the activity of the hypothalamic-pituitary-adrenal axis. Eur. J. Pharmacol. 2000, 405:149-160.
44. Lippmann M., Bress A., Nemeroff C.B., Plotsky P.M., Monteggia L.M. Long-term behavioural and molecular alterations associated with maternal separation in rats. Eur. J. Neurosci. 2007, 25:3091-3098.
45. Macri S., Würbel H. Developmental plasticity of HPA and fear responses in rats: a critical review of the maternal mediation hypothesis. Horm. Behav. 2006, 50:667-680.
46. Magariños A.M., Orchinik M., McEwen B.S. Morphological changes in the hippocampal CA3 region induced by non-invasive glucocorticoid administration: a paradox. Brain Res. 1998, 809:314-318.
47. Marais L., Hattingh S.M., Stein D.J., Daniels W.M. A proteomic analysis of the ventral hippocampus of rats subjected to maternal separation and escitalopram treatment. Metab. Brain Dis. 2009, 24:569-586.
48. Marin M.T., Planeta C.S. Maternal separation affects cocaine-induced locomotion and response to novelty in adolescent, but not in adult rats. Brain Res. 2004, 1013:83-90.
49. Martinez-Téllez R., Gomez-Villalobos M., de J., Flores G. Alteration in dendritic morphology of cortical neurons in rats with diabetes mellitus induced by streptozotocin. Brain Res. 2005, 1048:108-115.
50. Martinez-Tellez R., Hernandez-Torres E., Gamboa C., Flores G. Prenatal stress alters spiny density and dendritic length of neurons from nucleus accumbens and hippocampus in rat offspring. Synapse 2009, 63:794-804.
51. Maya Vetencourt J.F., Sale A., Viegi A., Baroncelli L., De Pasquale R., O'Leary O.F., Castrén E., Maffei L. The antidepressant fluoxetine restores plasticity in the adult visual cortex. Science 2008, 320:385-388.
52. McAllister A.K., Lo D.C., Katz L.C. Neurotrophins regulate dendritic growth in developing visual cortex. Neuron 1995, 15:791-803.
53. McAllister A.K., Katz L.C., Lo D.C. Neurotrophin regulation of cortical dendritic growth requires activity. Neuron 1996, 17:1057-1064.
54. McAllister A.K. Cellular and molecular mechanisms of dendrite growth. Cereb. Cortex 2000, 10:963-973.
55. Meaney M.J. Maternal care, gene expression, and the transmission of individual differences in stress reactivity across generations. Annu. Rev. Neurosci. 2001, 24:1161-1192.
56. Meaney M.J., Brake W., Gratton A. Environmental regulation of the development of mesolimbic dopamine systems: a neurobiological mechanism for vulnerability to drug abuse?. Psychoneuroendocrinology 2002, 27:127-138.
57. Meaney M.J., Mitchell J.B., Aitken D.H., Bhatnagar S., Bodnoff S.R., Iny L.J., Sarrieau A. The effects of neonatal handling on the development of the adrenocortical response to stress: implications for neuropathology and cognitive deficits in later life. Psychoneuroendocrinology 1991, 16:85-103.
58. Morales-Medina J.C., Sanchez F., Flores G., Dumont Y., Quirion R. Morphological reorganization after repeated corticosterone administration in the hippocampus, nucleus accumbens and amygdala in the rat. J. Chem. Neuroanat. 2009, 38:266-272.
59. Mullen P.E., Martin J.L., Anderson J.C., Romans S.E., Herbison G.P. The long-term impact of the physical, emotional, and sexual abuse of children: a community study. Child Abuse Negl. 1996, 20:7-21.
60. Noguchi T., Sekiguchi M., Sugisaki T., Tsukada Y., Shimai K. Faulty development of cortical neurons in the Snell dwarf cerebrum. Brain Res. 1983, 312:125-138.
61. Noguchi T., Sugisaki T. Abnormal neuronal growth in the little (lit) cerebrum. Exp. Neurol. 1985, 89:274-278.
62. Newport D.J., Stowe Z.N., Nemeroff C.B. Parental depression: animal models of an adverse life event. Am. J. Psychiatry 2002, 159:1265-1283.
63. Ognibene E., Adriani W., Caprioli A., Ghirardi O., Ali S.F., Aloe L., Laviola G. The effect of early maternal separation on brain derived neurotrophic factor and monoamine levels in adult heterozygous reeler mice. Prog. Neuropsychopharmacol. Biol. Psychiatry 2008, 32:1269-1276.
64. Pascual R., Zamora-León S.P. Effects of neonatal maternal deprivation and postweaning environmental complexity on dendritic morphology of prefrontal pyramidal neurons in the rat. Acta Neurobiol. Exp. (Wars) 2007, 67:471-479.
65. Paxinos G., Watson C. The Rat Brain in Stereotaxic Coordinates 1986, Academic Press, New York. 2nd edition.
66. Pickering C., Gustafsson L., Cebere A., Nylander I., Liljequist S. Repeated maternal separation of male Wistar rats alters glutamate receptor expression in the hippocampus but not the prefrontal cortex. Brain Res. 2006, 1099:101-108.
67. Plotsky P.M., Meaney M.J. Early, postnatal experience alters hypothalamic corticotropin-releasing factor (CRF) mRNA, median eminence CRF content and stress-induced release in adult rats. Brain Res. Mol. Brain Res. 1993, 18:195-200.
68. Plotsky P.M., Thrivikraman K.V., Nemeroff C.B., Caldji C., Sharma S., Meaney M.J. Long-term consequences of neonatal rearing on central corticotropin-releasing factor systems in adult male rat offspring. Neuropsychopharmacology 2005, 30:2192-2204.
69. Pryce C.R., Feldon J. Long-term neurobehavioural impact of the postnatal environment in rats: manipulations, effects and mediating mechanisms. Neurosci. Biobehav. Rev. 2003, 27:57-71.
70. Rajan I., Witte S., Cline H.T. NMDA receptor activity stabilizes presynaptic retinotectal axons and postsynaptic optic tectal cell dendrites in vivo. J. Neurobiol. 1999, 38:357-368.
71. Renard G.M., Rivarola M.A., Suarez M.M. Sexual dimorphism in rats: effects of early maternal separation and variable chronic stress on pituitary-adrenal axis and behavior. Int. J. Dev. Neurosci. 2007, 25:373-379.
72. Rivarola M.A., Suárez M.M. Early maternal separation and chronic variable stress in adulthood changes the neural activity and the expression of glucocorticoid receptor in limbic structures. Int. J. Dev. Neurosci. 2009, 27:567-574.
73. Robinson T.E., Kolb B. Persistent structural modifications in nucleus accumbens and prefrontal cortex neurons produced by previous experience with amphetamine. J. Neurosci. 1997, 17:8491-8497.
74. Roceri M., Hendriks W., Racagni G., Ellenbroek B.A., Riva M.A. Early maternal deprivation reduces the expression of BDNF and NMDA receptor subunits in rat hippocampus. Mol. Psychiatry 2002, 7:609-6016.
75. Rosenfeld P., Wetmore J.B., Levine S. Effects of repeated maternal separations on the adrenocortical response to stress of preweanling rats. Physiol. Behav. 1992, 52:787-791.
76. Sanchez M.M., Ladd C.O., Plotsky P.M. Early adverse experience as a developmental risk factor for later psychopathology: evidence from rodent and primate models. Dev. Psychopathol. 2001, 13:419-449.
77. Scott H.J., Stebbing M.J., Walters C.E., McLenachan S., Ransome M.I., Nichols N.R., Turnley A.M. Differential effects of SOCS2 on neuronal differentiation and morphology. Brain Res. 2006, 1067:138-145.
78. Sholl D.A. Dendritic organization in the neurons of the visual and motor cortices on the cat. J. Anat. 1953, 87:387-406.
79. Silva-Gómez A.B., Rojas D., Juarez I., Flores G. Decreased dendritic spine density on prefrontal cortical and hippocampal pyramidal neurons in postweaning social isolation rats. Brain Res. 2003, 983:128-136.
80. Slotten H.A., Kalinichev M., Hagan J.J., Marsden C.A., Fone K.C. Long-lasting changes in behavioural and neuroendocrine indices in the rat following neonatal maternal separation: gender-dependent effects. Brain Res. 2006, 1097:123-132.
81. Solis O., Limón D.I., Flores-Hernández J., Flores G. Alterations in dendritic morphology of the prefrontal cortical and striatum neurons in the unilateral 6-OHDA-rat model of Parkinson's disease. Synapse 2007, 61:450-458.
82. Solis O., Vazquez-Roque R.A., Camacho-Abrego I., de la Cruz F., Zamudio S., Flores G. Decreased dendritic spine density of neurons of the prefrontal cortex and nucleus accumbens and enhanced amphetamine sensitivity in postpubertal rats after a neonatal amygdala lesion. Synapse 2009, 63:1143-1159.
83. Spivey J., Barrett D., Padilla E., Gonzalez-Lima F. Mother-infant separation leads to hypoactive behavior in adolescent Holtzman rats. Behav. Processes 2008, 79:59-65.
84. Stevenson C.W., Halliday D.M., Marsden C.A., Mason R. Early life programming of hemispheric lateralization and synchronization in the adult medial prefrontal cortex. Neuroscience 2008, 155:852-863.
85. Sullivan R.M., Gratton A. Prefrontal cortical regulation of hypothalamic-pituitary-adrenal function in the rat and implications for psychopathology: side matters. Psychoneuroendocrinology 2002, 27:99-114.
86. Swain J.E., Lorberbaum J.P., Kose S., Strathearn L. Brain basis of early parent-infant interactions: psychology, physiology, and in vivo functional neuroimaging studies. J. Child Psychol. Psychiatry 2007, 48:262-287.
87. Thierry A.M., Gioanni Y., Degenetais E., Glowinski J. Hippocampo-prefrontal cortex pathway: anatomical and electrophysiological characteristics. Hippocampus 2000, 10:411-419.
88. Vega E., Gomez-Villalobos M., de J., Flores G. Alteration in dendritic morphology of pyramidal neurons from the prefrontal cortex of rats with renovascular hypertension. Brain Res. 2004, 1021:112-118.
89. Vogel M.W., Prittie J. Purkinje cell dendritic arbors in chick embryos following chronic treatment with an N-methyl-d-aspartate receptor antagonist. J. Neurobiol. 1995, 26:537-552.
90. Vouimba R.M., Yaniv D., Richter-Levin G. Glucocorticoid receptors and beta-adrenoceptors in basolateral amygdala modulate synaptic plasticity in hippocampal dentate gyrus, but not in area CA1. Neuropharmacology 2007, 52:244-252.
91. Vythilingam M., Heim C., Newport J., Miller A.H., Anderson E., Bronen R., Brummer M., Staib L., Vermetten E., Charney D.S., Nemeroff C.B., Bremner J.D. Childhood trauma associated with smaller hippocampal volume in women with major depression. Am. J. Psychiatry 2002, 159:2072-2080.
92. Weinstock M. The long-term behavioural consequences of prenatal stress. Neurosci. Biobehav. Rev. 2008, 32:1073-1086.
93. Wellman C.L. Dendritic reorganization in pyramidal neurons in medial prefrontal cortex after chronic corticosterone administration. J. Neurobiol. 2001, 49:245-253.
94. Woolley C.S., Gould E., McEwen B.S. Exposure to excess glucocorticoids alters dendritic morphology of adult hippocampal pyramidal neurons. Brain Res. 1990, 531:225-231.