Effect of early life stress on serotonin responses in the hippocampus of young adult rats

Synapse

Volumn 53, Issue 1, 2004, Pages 11-19

  Van Riel, Els ^a   Van Gemert, Neeltje G ^a   Meijer, Onno C ^b,c   Joëls, Marian ^a  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

^b LEIDEN UNIVERSITY   (Netherlands)

^c LEIDEN UNIVERSITY   (Netherlands)

Author keywords

5 HT1A receptor; CA1 area; Corticosterone; Hyperpolarization; Maternal deprivation

Indexed keywords

CORTICOSTERONE; GLUCOCORTICOID RECEPTOR; MESSENGER RNA; MINERALOCORTICOID RECEPTOR; SEROTONIN; SEROTONIN 1A RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DEPOLARIZATION; FEMALE; GENE EXPRESSION; HIPPOCAMPUS; HYPERPOLARIZATION; HYPOPHYSIS ADRENAL SYSTEM; MALE; MATERNAL DEPRIVATION; MEMBRANE STEADY POTENTIAL; NERVE CELL STIMULATION; NEUROTRANSMISSION; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROCESSING; PYRAMIDAL NERVE CELL; RAT; SEROTONINERGIC SYSTEM; SEROTONINERGIC TRANSMISSION; SIGNAL TRANSDUCTION; STIMULUS RESPONSE; STRESS;

ANIMALS; ANIMALS, NEWBORN; ELECTROPHYSIOLOGY; FEMALE; HIPPOCAMPUS; IN SITU HYBRIDIZATION; MALE; MATERNAL DEPRIVATION; MEMBRANE POTENTIALS; NEURONS; ORGAN CULTURE TECHNIQUES; RATS; RATS, WISTAR; RECEPTOR, SEROTONIN, 5-HT1A; RECEPTORS, GLUCOCORTICOID; RECEPTORS, MINERALOCORTICOID; RNA, MESSENGER; SEROTONIN; STRESS, PSYCHOLOGICAL;

EID: 2542616761     PISSN: 08874476     EISSN: None     Source Type: Journal    
DOI: 10.1002/syn.20033     Document Type: Article

References (50)

1. Akana SF, Scribner KA, Bradbury MJ, Strack AM, Walker CD, Dallman MF. 1992. Feedback sensitivity of the rat hypothalamo-pituitary-adrenal axis and its capacity to adjust to exogeneous corticosterone. Endocrinology 131:585-594.
2. Andrade R, Nicoll RA. 1987. Pharmacologically distinct actions of serotonin on single pyramidal neurones of the rat hippocampus recorded in vitro. J Physiol 394:99-124.
3. 1A receptor-mediated hyperpolarization in area CA1 hippocampal pyramidal neurons. Neuropsychopharmacology 14:27-33.
4. Chen SC, Ehrhard P, Goldowitz D, Smeyne RJ. 1997. Developmental expression of the GIRK family of inward rectifying potassium channels: implications for abnormalities in the weaver mutant mouse. Brain Res 778:251-264.
5. Cirulli F, Adriani W, Laviola G. 1997. Sexual segragation in infant mice: behavioral and neuroendocrine responses to d-amphetamine administration. Psychopharmacology 134:140-152.
6. Francis DD, Diorio J, Plotsky PM, Meaney MJ. 2002. Environmental enrichment reverses the effects of maternal separation on stress reactivity. J Neurosci 15:7840-7843.
7. Gasparini S, DiFrancesco D. 1999. Action of serotonin on the hyperpolarization-activated cation current (Ih) in rat CA1 hippocampal neurons. Eur J Neurosci 11:3093-3100.
8. Ghadimi BM, Jarolimek W, Misgeld U. 1994. Effects of serotonin on hilar neurons and granule cell inhibition in the guinea pig hippocampal slice. Brain Res 633:27-32.
9. Gross C, Zhuang X, Stark K, Ramboz S, Oosting R, Kirby L, Santarelli L, Beck S, Hen R. 2002. Serotonin-1A receptor acts during development to establish normal anxiety-like behavior in the adult. Nature 416:396-400.
10. Heim C, Nemeroff C. 2001. The role of childhood trauma in the neurobiology of mood and anxiety disorders: preclinical and clinical studies. Biol Psychiatry 49:1023-1039.
11. Henning SJ. 1978. Plasma concentrations of total and free corticosterone during development in the rat. Am J Physiol 235(5):E451-456.
12. 1A responsiveness in CA1 pyramidal neurons by in vivo activation of corticosteroid receptors. J Neuroendocrinol 8:433-438.
13. Joels M, De Kloet ER. 1990. Mineralocorticoid receptor-mediated changes in membrane properties of rat CA1 pyramidal neurons in vitro. Proc Natl Acad Sci USA 87:4495-4498.
14. Joels M, De Kloet ER. 1991. Effect of corticosteroid hormones on electrical activity in rat hippocampus. J Steroid Biochem Mol Biol 40:83-86.
15. Joels M, Hesen W, De Kloet ER. 1991. Mineralocorticoid hormones suppress serotonin-induced hyperpolarization of rat hippocampal CA1 neurons. J Neurosci 11:2288-2294.
16. Karten YJ, Nair SM, van Essen L, Sibug R, Joels M. 1999. Long-term exposure to high corticosterone levels attenuates serotonin responses in rat hippocampal CA1 neurons. Proc Natl Acad Sci USA 96:13456-13461.
17. Ladd CO, Huot RL, Trivikraman KV, Nemeroff CB, Meaney MJ, Plotsky PM. 2000. Long-term behavioral and neuroendocrine adaptations to adverse early experience. Prog Brain Res 122:81-103.
18. Lehmann J, Russig H, Feldon J, Pryce CR. 2002. Effect of a single maternal separation at different pup ages on the corticosterone stress response in adult and aged rats. Pharmacol Biochem Behav 73:141-145.
19. Levine S. 1994. The ontogeny of the hypothalamic-pituitary-adrenal axis: the influence of maternal factors. In: De Kloet ER, Azmitia EC, Landfield PW, editors. Brain corticosteroid receptors. Studies on the mechanism, function and neurotoxicity of corticosteroid action. Ann NY Acad Sci vol 746. p 275-293.
20. McAllister-Williams R, Ferrier I, Young A. 1998. Mood and neuropsychological function in depression: the role of corticosteroids and serotonin. Psychol Med 28:573-584.
21. McCormick JA, Lyons V, Jacobson MD, Noble J, Diorio J, Nyirenda M, Weaver S, Ester W, Yau JLW, Meaney MJ, Seckl JR, Chapman KE. 2000. 5′-heterogeneity of glucocorticoid receptor messenger RNA is tissue specific: differential regulation of variant transcripts by early life events. Mol Endocrinol 14:506-517.
22. Meaney MJ, Aitken DH. 1985. The effects of early postnatal handling on hippocampal glucocorticoid receptor concentrations: temporal parameters. Dev Brain Res 22:301-304.
23. Meaney MJ, Sapolsky RM, McEwen BS. 1985. The development of the glucocorticoid receptor system in the rat limbic brain: I. Ontogeny and autoregulation. Brain Research 350:159-164.
24. 1A receptors and behavioral coping with stress in adult offspring. Behav Neurosci 115:1111-1117.
25. Modell S, Lauer C, Schreiber W, Huber J, Krieg J, Holsboer F. 1998. Hormonal response pattern in the combined DEX-CRH test is stable over time in subjects at high familial risk for affective disorders. Neuropsychopharmacology 18:253-262.
26. Moore CL, Morelli GA. 1979. Mother rats interact differently with male and female offspring. J Comp Physiol Psychol 93:677-684.
27. 1A receptor-mediated response in CA1 hippocampal pyramidal cells. Neuropsychopharmacology 23:419-427.
28. Oitzl M, Workel J, Fluttert M, Frosch F, De Kloet E. 2000. 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 12:3771-3780.
29. Petitto J, Quade D, Evans D. 1992. Relationship of object loss during development to hypothalamic-pituitary-adrenal axis function during major affective illness later in life. Psychiatry Res 44:227-236.
30. Piguet P, Galvan M. 1994. Transient and long-lasting actions of 5-HT on rat dentate gyrus neurones in vitro. J Physiol 481:629-639.
31. 1A receptor mRNA expression and binding in the rat hippocampus. Brain Res Mol Brain Res 53:285-290.
32. Reul JMHM, De Kloet ER. 1985. Two receptor systems for corticosterone in rat brain: microdistribution and differential occupation. Endocrinology 117:2505-2511.
33. Reul JMHM, Van den Bosch FR, De Kloet ER. 1987a. Differential response of type I and type II corticosteroid receptors to changes in plasma steroid level and circadian rhythmicity. Neuroendocrinology 45:407-412.
34. Reul JMHM, Van den Bosch FR, De Kloet ER. 1987b. Relative occupation of type-I and type-II corticosteroid receptors in rat brain following stress and dexamethasone treatment: functional implications. J Endocr 115:459-467.
35. Robertson KD, Wolffe AP. 2000. DNA methylation in health and disease. Nat Rev Genet 1:11-19.
36. Rots NY, De Jong J, Workel JO, Levine S, Cools AR, De Kloet ER. 1996. Neonatal maternally deprived rats have as adults elevated basal pituitary-adrenal activity and enhanced susceptibility to apomorphine. J Neuroendocrinol 8:501-506.
37. Schwartzkroin PA. 1975. Characteristics of CAl neurons recorded intracellularly in the hippocampal in vitro slice preparation. Brain Res 85:423-436.
38. 1A receptor expression in the CA1 and CA3 areas of senescent Brown Norway rats. Brain Res 912:95-98.
39. Stein M, Walker J, Anderson G, Hazen A, Ross C, Eldridge G, Forde D. 1996. Childhood physical and sexual abuse in patients with anxiety disorders and in a community sample. Am J Psychiatry 153:275-277.
40. Stokes P. 1995. The potential role of excessive cortisol induced by HPA hyperfunction in the pathogenesis of depression. Eur Neuropsychopharmacol (Suppl):77-82.
41. Sutanto R, Rosenfeld P, De Kloet ER, Levine S. 1996. Long-term effects of neonatal maternal deprivation and ACTH on hippocampal mineralocorticoid and glucocorticoid receptors. Dev Brain Res 92: 156-163.
42. Van Oers HJJ, De Kloet ER, 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. J Neurosci 1810171-10179.
43. Van Riel E, Meijer OC, Veenema AH, Joels M. 2002. Hippocampal serotonin responses in short and long attack latency mice. J Neuroendocrinol 14:234-239.
44. Van Riel E, Meijer OC, Steenbergen PJ, Joels M. 2003. Chronic unpredictable stress causes attenuation of serotonin responses in cornu ammonis 1 pyramidal neurons. Neuroscience 120:649-658.
45. Vazquez DM, Van Oers H, Levine S, Akil H. 1996. Regulation of glucocorticoid and mineralocorticoid receptor mRNAs in the hippocampus of the maternally deprived rat. Brain Res 731:79-90.
46. Vazquez DM, Lopez JF, Van Oers H, Watson SJ, Levine S. 2000. Maternal deprivation regulates serotonin 1A and 2A receptors in the infant rat. Brain Res 855:76-82.
47. Vazquez DM, Eskandari R, Zimmer CA, Levine S, Lopez JF. 2002. Brain 5-HT receptor system in the stressed infant rat: implications for vulnarability to substance abuse. Psychoneuroendocrinology 27: 245-272.
48. Weaver ICG, La Plante P, Weaver S, Parent A, Sharma S, Diorio J, Chapman KE, Seckl JR, Szyf M, Meaney MJ. 2001. Early environmental regulation of hippocampal glucocorticoid receptor gene expression: characterization of ontracellular mediators and potential genomic target sites. Mol Cell Endocrinol 185:205-218.
49. Workel JO, Oitzl MS, Ledeboer A, De Kloet ER. 1997. 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 103:199-203.
50. Workel JO, Oitzl MS, Fluttert M, Lesscher H, Karssen A, De Kloet ER. 2001. Differential and age-dependent effects of maternal deprivation on the hypothalamic-pituitary-adrenal axis of Brown-Norway rats from youth to senescence. J Neuroendocrinol 13:569-580.