Hostname: page-component-cd9895bd7-gvvz8 Total loading time: 0 Render date: 2024-12-29T09:48:12.810Z Has data issue: false hasContentIssue false

The Effects of Maternal Deprivation on the Hippocampal Structure in Adult Rats

Published online by Cambridge University Press:  02 December 2014

Pınar Karakaş*
Affiliation:
Çukurova University, Faculty of Medicine, Department of Anatomy, Adana, Turkey
Memduha Gülhal Bozkır
Affiliation:
Çukurova University, Faculty of Medicine, Department of Anatomy, Adana, Turkey
Fahri Dere
Affiliation:
Çukurova University, Faculty of Medicine, Department of Anatomy, Adana, Turkey
Enver Melik
Affiliation:
Department of Physiology, Adana, Turkey
Emine Babar Melik
Affiliation:
Department of Physiology, Adana, Turkey
Mehmet Kaya
Affiliation:
Department of Histology-Embryology, Adana, Turkey
Sait Polat
Affiliation:
Department of Histology-Embryology, Adana, Turkey
*
Çukurova University, Faculty of Medicine, Department of Anatomy, 01330, Adana, Turkey
Rights & Permissions [Opens in a new window]

Abstract

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.
Objectives:

To examine the ultrastructural effects of maternal deprivation during developmental periods of limbi-chypothalamo-pituitary-adrenal system on hippocampal dendritic structures in adult rats.

Methods:

The experiments were carried out with male and female wistar rats in our department. The rats were mated and, after birth, the pups were divided into four groups. The first group (control group) pups remained undisturbed with their dam until postweaning day 22. Maternal deprived groups were separated from their dams for 24 hours at postnatal day 4, 9 and 18. The subjects were provided with food and water ad libitum until 3-months-of-age. At the third month, the rats were transcardially perfused, samples were taken from CA1 and CA3 regions of the hippocampus. Tissues were prepared for electron microscopy.

Results:

When the data were analyzed, there were no differences between male and female rats in both ultrastructure and semiquantitative analysis of axodendritic synapses. The ultrastructure of Group 1 was seen as normal while in the second Group some neurons nuclear envelope made deep invagination into the nucleus. Additionally, axodendritic synapses were found normal. In Group 3, micrographs and axodendritic synapses were showed normal structure. However, in Group 4 in some neurons invaginations were seen similar to Group 2. Axodendritic synapses were found to be normal.

Conclusion:

These experiments establish that MD in rats produces slight ultrastructural changes and decreases the number of synapses in CA1 and CA3 subregions of the hippocampus.

Type
Original Article
Copyright
Copyright © The Canadian Journal of Neurological 2009

References

1. Fuchs, E, Flügge, G, Ohl, F, Lucassen, P, Vollmann-Honsdorf, GK, Michaelis, T. Psychosocial stress, glucocorticoids, and structural alterations in the tree shrew hippocampus. Physiol Behav. 2001; 73:28591.Google Scholar
2. Magarinos, AM, McEwen, BS. Stress-induced atrophy of apical dendrites of hippocampal CA3c neurons: comparison of stressors. J Neurosci. 1995; 69:838.CrossRefGoogle ScholarPubMed
3. Fuchs, E, Uno, H, Flügge, G. Chronic psychosocial stress induces morphological alterations in hippocampal pyramidal neurons of the tree shrew. Brain Res. 1995; 673:7582.CrossRefGoogle ScholarPubMed
4. Lopez, JF, Akil, H, Watson, SJ. Role of biological and psychological factors in early development and their impact on adult life. Biol Psychiatry. 1999; 46:146171.Google Scholar
5. Lehmann, J, Pryce, CR, Bettschen, D, Feldon, J. The maternal separation paradigm and adult emotionality and cognition in male and female wistar rats. Pharmacol Biochem Behav. 1999; 64:70515.CrossRefGoogle ScholarPubMed
6. Schmidt, M, Okimoto, DK, Dent, W, Gordon, MK, Levine, S. Maternal regulation of the hypothalamic-pituitary-adrenal axis in the 20-day-old rat: consequences of laboratory weaning. J Neuroendocrinol. 2002; 14:4507.CrossRefGoogle ScholarPubMed
7. Francis, DD, Meaney, MJ. Maternal care and the development of stress responses. Curr Opin Neurobiol. 1999; 9:12834.CrossRefGoogle ScholarPubMed
8. Ganong, WF. Adrenal medulla and adrenal cortex. In: Review of medical physiology. 18th ed. Appleton and Lange; p. 347.Google Scholar
9. Lambert, KG, Buckelew, SK, Staffiso-Sandoz, G, Gaffga, S, Carpenter, W, Fisher, J, et al. Activity-stress induces atrophy of apical dendrites of hippocampal pyramidal neurons in male rats. Physiol Behav. 1998; 65:439.CrossRefGoogle ScholarPubMed
10. Wallenstein, GV, Eichenbaum, H, Hassehno, ME. The hippocampus as an associator of discontiguous events. Trends Neurosci. 1998; 21:31723.CrossRefGoogle ScholarPubMed
11. Moser, MB, Trommald, M, Andersen, P. An increase in dendritic spine density on hippocampal CA1 pyramidal cells following spatial learning in adult rats suggests the formation of new synapses. Proc Natl Acad Sci. 1994; 91:126735.CrossRefGoogle ScholarPubMed
12. Magarinos, AM, McEwen, BS, Flügge, G, Fuchs, E. Chronic psychosocial stress causes apical dendritic atrophy of hippocampal CA3 pyramidal neurons in subordinate tree shrews. J Neurosci. 1996; 16:353440.CrossRefGoogle ScholarPubMed
13. Magarinos, AM, Verdugo, JMG, McEwen, BS. Chronic stress alters synaptic terminal structure in hippocampus. Proc Natl Acad Sci. 1997; 94:140028.CrossRefGoogle ScholarPubMed
14. Zito, K, Murthy, VN. Dendritic spines. Curr Biol. 2002; 12:R5.CrossRefGoogle ScholarPubMed
15. Dunaevsky, A, Tashiro, A, Majewska, A, Mason, C, Yuste, R. Developmental regulation of spine motility in the mammalian central nervous system. Proc Natl Acad Sci. 1999; 96:1343843.CrossRefGoogle ScholarPubMed
16. Segal, M. Rapid plasticity of dendritic spine: hints to possible functions. Prog Neurobiol. 2001; 63:6170.CrossRefGoogle ScholarPubMed
17. Shors, TJ, Chua, C, Falduto, J. Sex differences and opposite effects of stress on dendritic spine density in the male versus female hippocampus. J Neurosci. 2001; 21:62927.CrossRefGoogle ScholarPubMed
18. Harris, KM. Calcium from internal stores modifies dendritic spine shape. Proc Natl Acad Sci. 1999; 96:1221315.CrossRefGoogle ScholarPubMed
19. Reid, C. The role of dendritic spines: comparing the complex with the simple. Eur J Pharmacol. 2002; 447:1736.CrossRefGoogle ScholarPubMed
20. Spacek, J, Harris, KM. Three-dimensional organization of cell adhesion junctions at synapses and dendritic spines in area CA1 of the rat hippocampus. J Comp Neurol. 1998; 393:5868.3.0.CO;2-P>CrossRefGoogle ScholarPubMed
21. Boyer, C, Schikorski, T, Stevens, CF. Comparison of hippocampal dendritic spines in culture and in brain. J Neurosci. 1998; 18: 5294300.CrossRefGoogle ScholarPubMed
22. Segal, M. Dendritic spines for neuroprotection: a hypothesis. Trends Neurosci. 1995; 18:46871.CrossRefGoogle ScholarPubMed
23. Galea, LAM, McEwen, BS, Tanapat, P, Deak, T, Spencer, RL, Dhabhar, FS. Sex differences in dendritic atrophy of CA3 pyramidal neurons in response to chronic restraint stress. J Neurosci. 1997; 81:68997.CrossRefGoogle ScholarPubMed
24. Papa, M, Segal, M. Morphological plasticity in dendritic spines of cultured hippocampal neurons. J Neurosci. 1996; 71:100511.CrossRefGoogle ScholarPubMed
25. Suchecki, D, Nelson, DY, Van Oers, H, Levine, S. Activation and inhibition of the hypothalamic-pituitary-adrenal axis of the neonatal rat: effects of maternal deprivation. Psychoneuroendocrinol. 1995; 20:16982.CrossRefGoogle ScholarPubMed
26. Roceri, M, Cirulli, F, Pessina, C, Peretto, P, Racagni, G, Riva, MA. Postnatal repeated maternal deprivation produces age-dependent changes of brain-derived neurotrophic factor expression in selected rat brain regions. Biol Psychiatry. 2004; 55:70814.CrossRefGoogle ScholarPubMed
27. Workel, JO, Oitzl, MS, Ledeboer, A, de Kloet, ER. The Brown Norway rat displays enhanced stress-induced ACTH reactivity at day 18 after 24-h maternal deprivation at day 3. Brain Res Dev Brain Res. 1997; 103:199203.Google Scholar
28. Greisen, MH, Altar, CA, Bolwig, TG, Whitehead, R, Wörtwein, G. Increased adult hippocampal brain-derived neurotrophic factor and normal levels of neurogenesis in maternal separation rat. J Neurosci Res. 2005; 79:7728.CrossRefGoogle Scholar
29. Levine, S. Influence of psychological variables on the activity of the hypothalamic-pituitary-adrenal axis. Eur J Pharmacol. 2000; 405:14960.CrossRefGoogle ScholarPubMed
30. Ellenbroek, BA, Cools, AR. Early maternal deprivation and prepulse inhibition. The role of the postdeprivation environment. Pharmacol Biochem Behav. 2002; 73:17784.CrossRefGoogle ScholarPubMed
31. Levine, S. Primary social relationships influence the development of the hypothalamic-pituitary-adrenal axis in the rat. Physiol Behav. 2001; 73:25560.CrossRefGoogle ScholarPubMed
32. Gould, E, Tanapat, P. Stress and hippocampal neurogenesis. Biol Psychiatry. 1999; 46:14729.CrossRefGoogle ScholarPubMed
33. Oitzl, MS, Workel, JO, Fluttert, M, Frösch, F, de Kloet, ER. Maternal deprivation affects behaviour from youth to senescence: amplification of individual differences in spatial learning and memory in senescent Brown Norway rats. Eur J Neurosci. 2000; 12:377180.CrossRefGoogle ScholarPubMed
34. Schmidt, M, Enthoven, L, van der Mark, M, Levine, S, de Kloet, ER, Oitzl, MS. The postnatal development of the hypothalamic-pituitary-adrenal axis in the mouse. Int J Devl Neurosci. 2003; 21:12532.CrossRefGoogle ScholarPubMed
35. Schmidt, M, Enthoven, L, van Woezik, JHG, Levine, S, de Kloet, ER, Oitzl, MS. The dynamics of the hypothalamic-pituitary-adrenal axis during maternal deprivation. J Neuroendocrinol. 2004; 16: 527.CrossRefGoogle ScholarPubMed
36. Kuhn, CM, Schanberg, SM. Responses to maternal separation: mechanisms and mediators. Int J Devl Neurosci. 1998; 16: 26170.CrossRefGoogle ScholarPubMed
37. Magarinos, AM, McEwen, BS. Stress-induced atrophy of apical dendrites of hippocampal CA3c neurons: involvement of glucocorticoid secretion and excitatory aminoacid receptors. J Neurosci. 1995; 69:8998.Google Scholar
38. McEwen, BS. Effects of adverse experiences for brain structure and function. Biol Psychiatry. 2000; 48:72131.CrossRefGoogle ScholarPubMed
39. Andersen, SL, Teicher, MH. Delayed effects of early stress on hippocampal development. Neuropsychopharmacol. 2004; 29: 198893.CrossRefGoogle ScholarPubMed
40. Poeggel, G, Helmeke, C, Abraham, A, Schwabe, T, Friedrich, P, Braun, K. Juvenile emotional experience alters synaptic composition in the rodent cortex, hippocampus, and lateral amygdala. Proc Natl Acad Sci. 2003; 100:1613742.Google Scholar
41. Lehmann, J, Russig, H, Feldom, J, Pryce, CR. Effect of a single maternal separation at different pup ages on the corticosterone stress response in adult and aged rats. Pharmacol Biochem Behav. 2002; 73:1415.Google Scholar
42. Brunson, KL, Eghbal-Ahmadi, M, Bender, R, Chen, Y, Baram, TZ. Long-term, progressive hippocampal cell loss and dysfunction induced by early-life administration of corticotropin-releasing hormone reproduce the effects of early-life stress. Proc Natl Acad Sci. 2001; 98:885661.Google Scholar
43. Trommald, M, Hulleberg, G. Dimensions and density of dendritic spines from rat dentate granule cells based on reconstructions from serial electron micrographs. J Comp Neurol. 1997; 377: 1528.3.0.CO;2-M>CrossRefGoogle ScholarPubMed
44. Fiala, JC, Feinberg, M, Popov, V, Harris, KM. Synaptogenesis via dendritic filopodia in developing hippocampal area CA1. J Neurosci. 1998; 18:890011.CrossRefGoogle ScholarPubMed
45. Ellenbroek, BA, Cools, AR. The long-term effects of maternal deprivation depend on the genetic background. Neuropsychopharmacol. 2000; 23:99106.Google Scholar
46. Van Oers, HJJ, de Kloet, ER, Levine, S. Early vs. late maternal deprivation differentially alters the endocrine and hypothalamic responses to stress. Dev Brain Res. 1998; 111:24552.Google Scholar