Effects of aversive stress during brain development on hippocampal synaptic and behavioral responses to emotional stress at postadolescence

Japanese Journal of Neuropsychopharmacology

Volumn 27, Issue 1, 2007, Pages 19-27

  Koseki, Hiroyo ^a   Matsumoto, Machiko ^b   Togashi, Hiroko ^c   Yamaguchi, Taku ^b   Izumi, Takeshi ^b   Yoshioka, Mitsuhiro ^b   Fukushima, Kazuaki ^a  

^a HOKKAIDO UNIVERSITY   (Japan)

^b HOKKAIDO UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^c HEALTH SCIENCES UNIVERSITY OF HOKKAIDO   (Japan)

Author keywords

5 HT1A receptor; Brain development; Early postnatal stress; Emotional stress; Hippocampal CA1 field; Synaptic response

Indexed keywords

SEROTONIN 1A RECEPTOR;

ARTICLE; AVERSIVE BEHAVIOR; BEHAVIOR; BRAIN DEVELOPMENT; CONTROLLED STUDY; EMOTIONAL STRESS; FEAR; FOOTSHOCK; HIPPOCAMPUS; LONG TERM POTENTIATION; MENTAL STRESS; NONHUMAN; PERINATAL PERIOD; SYNAPTIC MEMBRANE;

AGE FACTORS; ANIMALS; BEHAVIOR, ANIMAL; ELECTRIC STIMULATION; EMOTIONS; FEMALE; FOOT; HIPPOCAMPUS; MALE; RATS; RATS, WISTAR; RECEPTOR, SEROTONIN, 5-HT1A; STRESS, PSYCHOLOGICAL; SYNAPTIC TRANSMISSION;

EID: 34047248718     PISSN: 13402544     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (63)

1. Abraham, W. C. and Bear, M. F. (1996) Metaplasticity: The plasticity of synaptic plasticity. Trends Neurosci, 19: 126-130.
2. Abraham, I. M. and Kovacs, K. J. (2000) Postnatal handlings alters the acivation of stress-related neuronal circuitries. Eur J Neurosci, 12: 3003-3014.
3. Arnsten, A. F., Berridge, C. and Segal, D. S. (1985) Stress produces opioid-like effects in investigatory behavior. Pharmachol Biochem, 22: 803-809.
4. Avanzi, V., Silvia, R. C., Macedo, C. E. and Brandao, M. L. (2003) 5-HT mechanisms of median raphe nucleus in the conditioned freezing caused by light/foot-shock association. Physiol Behav, 78: 471-477.
5. Beique, J. C., Campell, B., Perring, P., Hamblin, M. W., Walker, P., Mladenovic, L. and Andrade, R. (2004a) Serotonergic regulation of membrane potential in developing rat prefrontal cortex. J Neurosci, 20: 4807-4817.
6. Beique, J. C., Chapin-Penick, E. M., Mladenovic, L. and Andrade, R. (2004b) Serotonergic facilitation of synaptic activity in the developing rat prefrontal cortex. J Physiol, 556: 739-754.
7. Bennett-Clarke, C. A., Leslie, M. J., Lane, R. D. and Rhoades, R. W. (1994) Effect of serotonin depletion on vibrissae-related patterns of thalamic afferents in the rat's somatosensory cortex. J Neurosci, 14: 7594-7617.
8. Bliss, T. V., Lancaster, B. and Wheal, H. V. (1983) Long-term potentiation in commissural and Schaffer projections to hippocampal CA1 call: An in vivo study in the rat. J Physiol, 341: 617-626.
9. Caldji, C., Diorio, J. and Meaney, M. J. (2000) Variations in maternal care in infancy regulate the development of stress reactivity. Biol Psychiatry, 48: 1164-1174.
10. Card, J. P., Levitt, P., Gluhovsky, M. and Rinaman, L. (2005) Early experience modifies the postnatal assembly of autonomic emotional motor circuits in rats. J Neurosci, 25: 9102-9111.
11. Cases, O., Vitalis, T., Seif, J., De Maeyer, E., Sotelo, C. and Gaspar, P. (1996) Lack of barrels in the somatosensory cortex of monoamine oxydase A-deficient mice: Role of a serotonin excess during the critical period. Neuron, 16: 297-307.
12. 2+ influx in rat basolateral amygdala via 5-HT1A receptors. Eur J Neurosci, 10: 2163-2172.
13. Chubakov, A. R., Gromova, E. A., Konovalov, G. V., Sarkisova, E. F. and Chumasov, E. I. (1986) The effects of serotonin on the morpho-functional development of rat cerebral neocortex in tissue culture. Brain Res, 369: 285-297.
14. Chubakov, A. R., Tsyganova, V. G. and Sarkisivav, E. F. (1993) The stimulating influence of the raphe nuclei on the morphofunctional development of the hippocampus during their combined cultivation. Neurosci Behav Physiol, 23: 271-276.
15. Czeh, B., Michaelis, T., Watanabe, T., Frahm, J., de Biurrun, G., van Kampen, M., Bartolomucci, A. and Fuchs, E. (2001) Stress-induced changes in cerebral metabolites, hippocampal volume, and cell proliferation are prevented by antidepressant treatment with tianeptine. Proc Natl Acad Sci USA, 98: 12796-12801.
16. Duman, R. S., Heninger, G. R. and Nestler, E. J. (1997) A molecular and cellular theory of depression. Arch Gen Psychiatry, 54: 607-608.
17. Edagawa, Y., Saito, H. and Abe, K. (1999) Stimulation of the 5-HT1A receptor selectivity suppresses NMDA receptor-mediated synaptic excitation in the rat visual cortex. Brain Res, 827: 225-228.
18. 1A receptor activation. Dev Brain Res, 114: 245-252.
19. Figgitt, D. P. and McClellan, K. J. (2000) Fluvoxamine. An updated review of its use in the management of adults with anxiety disorders. Drugs, 60: 925-954.
20. Foy, M. R., Stanton, M. E., Levine, S. and Thompson, R. F. (1987) Behavioral stress impairs long-term potentiation in rodent hippocampus. Behav Neural Biol, 48: 138-149.
21. Gross, C., Zhang, X., Stark, K., Ramboz, S., Oosting, R., Kirby, L., Santarelli, L., Beck, S. and Hen, R. (2002) Serotonin1A receptor acts during development to establish normal anxiety-like behavior in the adult. Nature, 416: 396-400.
22. Heim, C. and Nemeroff, C. B. (2001) The role of childhood trauma in the neurobiology of mood and anxiety disorders: Preclinical and clinical studies. Biol Psychiatry, 49: 1023-1039.
23. Japanese source
24. Huot, R. L., Thrivikraman, K. V., Meaney, M. J. and Plotsky, P. M. (2001) Development of adult ethanol preference and anxiety as a consequence of neonatal maternal separation in Long Evans rats and reversal with antidepressant treatment. Psychopharmachology (Berl), 158: 366-373.
25. Huot, R. L., Plotsky, P. M., Lenox, R. H. and McNamara, R. K. (2002) Neonatal maternal separation reduces hippocampal mossy fiber density in adult Long Evans rats. Brain Res., 950: 52-63.
26. Janusonis, S., Gluncic, V. and Rakic, P. (2004) Early serotonergic projections to Cajal-Retzius cells: Relevance for cortical development. J Neurosci, 24: 1652-1659.
27. Kim, J. J., Foy, M. R. and Thompson, R. F. (1996) Behavioral stress modifies hippocampal plasticity through N-methyl-D-aspartate receptor activation. Proc Natl Acad Sci USA, 93: 4750-4753.
28. Kondoh, M., Shiga, T. and Okado, N. (2004) Regulation of dendrite formation of Purkinje cells by serotonin through serotonin1A and serotonin2A receptors in culture. Neurosci Res, 48: 101-109.
29. Lauder, J. M. (1985) Roles for neurotransmitters in development: Possible interaction with drugs during the fetal and neonatal periods. Prog Clin Biol Res, 163: 375-380.
30. Lauder, J. M., Wallace, J. A. and Krebs, H. (1981) Roles for serotonin in neuroembryogenesis. Adv Exp Med Biol, 133: 477-506.
31. Lauder, J. M., Wallace, J. A., Wilkie, M. B., DiNome, A. and Krebs, H. (1983) Roles for serotonin in neurogenesis. Monogr Neura Sci, 9: 3-10.
32. Lemaire, V., Koehl, M., Le Moal, M. and Abrous, D. N. (2000) Prenatal stress produces learning deficits associated with an inhibition of neurogenesis in the hippocampus. Proc Natl Acad Sci, 97: 11032-11037.
33. Lidov, H. G. and Molliver, M. E. (1982) An immunohistochemical study of serotonin neuron development in the rat: Ascending pathways and terminal fields. Brain Res Bull, 8: 389-430.
34. Malberg, J. E. and Duman, R. S. (2003) Cell proliferation in adult hippocampus is decreased by inescapable stress: Reversal by fluoxetine treatment. Neuropsychopharmachology, 28: 1562-1571.
35. Malberg, J. E., Eisch, A. J., Nestler, E. J. and Duman, R. S. (2000) Chronic antidepressant treatment increases neurogenesis in adult rat hippocampus. J Neurosci, 20: 9104-9110.
36. Manahan-Vaughan, D. and Braunewell, K. H. (1999) Novelty acquisition is associated with induction of hippocampal long-term depression. Proc Natl Acad Sci USA, 96: 8739-8744.
37. Matsumoto, M., Togashi, H., Ohashi, S., Tachibana, K., Yamaguchi, T. and Yoshioka, M. (2004) Serotonergic modulation of psychological stress-induced alteration in synaptic plasticity in the rat hippocampal CA1 field. Bain Res, 1022: 221-225.
38. Matsumoto, M., Tachibana, K., Togashi, H., Tahara, K., Kojima, T., Yamaguchi, T. and Yoshioka, M. (2005) Chronic treatment with milnacipran reverses the impairment of synaptic plasticity induced by conditioned fear stress. Psychopharmachology (Berl), 179: 606-612.
39. Mazer, C., Muneyyirci, J., Tahney, K., Raio, N., Borella, A. and Whitaker-Azmitia, P. M. (1997) Serotonin depletion during synaptogenesis leads to decreased synaptic density and learning deficits in the adult rat. A model of neurodevelopmental disorders with cognitive deficits. Brain Res, 760: 68-73.
40. McAllister-Williams, R. H., Ferrier, I. N. and Young, A. H. (1998) Mood and neuropsychological function in depression: The role of corticosteroids and serotonin. Psychol Med, 28: 573-584.
41. Mirescu, C., Peters, J. D. and Gould, E. (2004) Early life experience alters response of adult neurogenesis to stress. Nat Neurosci, 7: 841-846.
42. 1A agonist tandospirone, on hippocampal long-term potentiation in vivo. Pharmacol Biochem Behav, 69: 367-372.
43. Nibuya, M., Nestler, E. J. and Duman, R. S. (1996) Chronic antidepressant administration increases the expression of cAMP response element binding protein (CREB) in rat hippocampus. J Neurosci, 16: 2365-2372.
44. O'Connor, P. and Chipkin, R. E. (1984) Comparisons between warm and cold water swim stress in mice. Life Sc, 35: 631-639.
45. Okado, N., Cheng, L., Tanatsugu, Y., Hamada, S. and Hamaguchi, K. (1993) Synaptic loss following removal of serotonergic fibers in newly hatched and adult chickens. J Neurobiol, 24: 687-698.
46. Plotsky, P. M. and Meaney, M. J. (1993) Early, postnatal experience alters hypothalamic corticotropin-releasing factor (CRF) mRNA, median eminence CRF content and stress-induced release in adult rats. Mol Brain Res, 18: 195-200.
47. Pokk, P. and Vali, M. (2001) Small platform stress increases exploratory activity of mice in staircase test. Prog Neuropsychopharmachol Biol Psychiatry, 25: 1435-1444.
48. Roche, M., Commons, K. G., Peoples, A. and Valentino, R. J. (2003) Circuitry underlying regulation of the serotonergic system by swim stress. J Neurosci, 23: 970-977.
49. Rueter, L. E. and Jacobs, B. L. (1996) A microdialysis examination of serotonin release in the rat forebrain induced by behavioral/environmental manipulations. Brain Res, 739: 57-69.
50. Schreiber, R., Melon, C. and de Vry, J. (1998) The role of 5-HT receptor subtypes in the anxiolytic effects of selective serotonin reuptake inhibitors in the rat ultrasonic vocalization test. Psychopharmacology, 135: 383-391.
51. Shakesby, A. C., Anwyl, R. and Rowan, M. J. (2002) Overcoming the effects of stress on synaptic plasticity in the intact hippocampus: Rapid actions of serotonergic and antidepressant agents. J Neurosci, 22: 3638-3644.
52. Shors, T. J., Seib, T. B., Levine, S. and Thompson, R. F. (1989) Inescapable versus escapable shock modulates long-term potentiation in the rat hippocampus. Science, 244: 224-226.
53. Shors, T. J., Gallegos, R. A. and Breindl, A. (1997) Transient and persistent conscequences of acute stress on long-term potentiation (LTP), synaptic efficacy, theta rhythms and bursts in area CA1 of the hippocampus. Synapse, 26: 209-217.
54. Shors, T. J., Miesegaes, G., Beylin, A., Zhao, M., Rydel, T. and Gould, E. (2001) Neurogenesis in the adults is involved in the formation of trace memories. Nature, 410: 372-376.
55. Smith, M. A., Makino, S., Kvetnansky, R. and Post, R. M. (1995) Stress and glucocorticoids affect the expression of brain-derived neurotrophic factor and neurotrophin-3 mRNAs in the hippocampus. J Neurosci, 15: 1768-1777.
56. 1A receptors. Hippocampus, 14: 143-147.
57. van Riel, E., van Gemert, N. G., Meijer, O. C. and Joels, M. (2004) Effect of early life stress on serotonin responses in the hippocampus of young adult rats. Synapse, 53: 11-19.
58. Von Frijtag, J. C., Kamal, A., Reijmers, L. G., Schrama, L. H., van den Bos, R. and Spruijt, B. M. (2001) Chronic imipramine treatment partially reverses the long-term changes of hippocampal synaptic plasticity in socially stressed rats. Neurosci Lett, 309: 153-156.
59. Xu, L., Anwyl, R. and Rowan, M. J. (1997) Behavioral stress facilitates the induction of long-term depression in the hippocampus. Nature, 387: 497-500.
60. 1A receptors mediate the effects of 5-HT on developing dentate granule cells. Dev Brain Res, 98: 185-190.
61. Yan, W., Wilson, C. C. and Haring, J. H. (1997b) Effects of neonatal serotonin depletion on the development of rat dentate granule cells. Dev Brain Res, 98: 177-184.
62. Yoshioka, M., Matsumoto, M., Togashi, H. and Saito, H. (1995) Effects of conditioned fear stress on 5-HT release in the rat prefrontal cortex. Pharmacol Biochem Behav, 51: 515-519.
63. Zhang, Z. W. (2003) Serotonin induces tonic firing in layer V pyramidal neurons of rat prefrontal cortex. J Neurosci, 23: 3373-3384.