Exposure to chronic psychosocial stress and corticosterone in the rat: Effects on spatial discrimination learning and hippocampal protein kinase Cγ immunoreactivity

Hippocampus

Volumn 7, Issue 4, 1997, Pages 427-436

  Krugers, Harm J ^a,b   Douma, Bas R K ^a   Andringa, Gerda ^a   Bohus, Béla ^a   Korf, Jakob ^a   Luiten, Paul G M ^a  

^a UNIVERSITY OF GRONINGEN   (Netherlands)

^b UNIVERSITY OF AMSTERDAM   (Netherlands)

Author keywords

Corticosterone; Dentate gyrus; Hippocampus; Learning and memory; Protein kinase C; Spatial orientation; Stress

Indexed keywords

CORTICOSTERONE; PROTEIN KINASE C;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CORTICOSTERONE BLOOD LEVEL; HIPPOCAMPUS; HUMAN; LEARNING; MALE; MEMORY; NERVE CELL PLASTICITY; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; SPATIAL DISCRIMINATION; SPATIAL ORIENTATION; STRESS; WORKING MEMORY;

ADRENAL GLANDS; ANIMALS; ANTI-INFLAMMATORY AGENTS; ANTIBODY SPECIFICITY; BODY WEIGHT; CHRONIC DISEASE; CORTICOSTERONE; DENTATE GYRUS; DISCRIMINATION LEARNING; ISOENZYMES; MALE; MEMORY; ORGAN SIZE; PROTEIN KINASE C; RATS; RATS, WISTAR; SPATIAL BEHAVIOR; STRESS, PSYCHOLOGICAL; THYMUS GLAND;

EID: 0030844427     PISSN: 10509631     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1098-1063(1997)7:4<427::AID-HIPO8>3.0.CO;2-F     Document Type: Article

References (61)

1. Abeliovich A, Paylor R, Chen C, Kim JJ, Wehner JM,Tonegawa S. PKCγ mutant nice exhibit mild deficits in spatial and contextual learning. Cell 1993;75:1263-1271.
2. Amaral D. Emerging principles of intrinsic hippocampal organization. Curr Opin Neurobiol 1993;3:225-229.
3. Abel I, KadarT, Silbermann M, Levy A. The effects of long-term corticosterone administration on hippocampal morphology and cognitive performance of middle-aged rats. Brain Res 1994;657:227-235.
4. Beldhuis HJA, Everts HGJ, Van der Zee EA, Luiten PGM, Bonus B. Amygdala kindling-induced seizures selectively impair spatial memory. 1. Behavioral characteristics and effects on hippocampal neuronal protein kinase C isofoms. Hippocampus 1992;2:397-410.
5. Bennet MC, Diamond DM, Fleshner M, Rose GM. Serum corticosterone level predicts the magnitude of hippocampal primed burst potentiation and depression in urethane-anaesthetized rats. Psychobiology 1991;19:301-307.
6. Blanchard DC, Sakai RR, McEwen BS, Weiss SM, Blanchard RJ. Subordination stress: Behavioral, brain and neuro-endocrine correlates. Behav Brain Res 1993;58:113-121.
7. Bodnoff SR, Humphreys AG, Lehman JC, Diamond DM, Rose GM, Meaney MJ. Enduring effects of chronic corticosterone treatment on spatial learning, synaptic plasticity, and hippocampal neuropathology in young and mid-aged rats. J Neurosci 1995;15:61-69.
8. Bonus B. Humoral modulation of learning and memory processes: Physiological significance of brain and peripheral mechanisms. In: Delacour J, ed The memory system of the brain Singapore: World Scientific Publishing, 1994:337-364.
9. Cazaubon S, Marais R, Parker P, Strosberg AD. Monoclonal antibodies to protein kinase Cγ . Functional relationship between epitopes and cofactor binding sates. Eur J Biochem 1989;182:401-406.
10. Cazaubon S, Webster C, Camoin L, Strosberg AD, Parker P. Effector dependent conformational changes in protein kinase Cγ through epitope mapping with inhibitory monoclonal antibodies. Eur J Biochem 1990;194:799-804.
11. Dachir S, Kadar T, Robinzon B, Levy A. Cognitive deficits induced in young rats by long term corticosterone administration. Behav Neurol Biol 1993;60:103-109.
12. De Goeij DCE, Dijkstra H, Tilders FJH. Chronic psychosocial stress enhances vasopressin, but not corticotropin releasing factor, in the external zone of the median eminence of male rats: Relationship to subordinate status. Endocrinology 1992;131:847-853.
13. Diamond DM, Rose GM. Exposure to a novel environment interferes with the induction of hippocampal primed burst potentiation in the behaving rat. Psychobiology 1990;18:273-281.
14. Diamond DM, Bennett MC, Fleshner M, Rose GM. Inverted-U relationship between the level of peripheral corticosterone and the magnitude of hippocampal primed burst potentiation. Hippocampus 1992;2:421-430.
15. Diamond DM, Fleshner M, Rose GM. Psychological stress repeatedly blocks hippocampal primed burst potentiation in behaving rats. Behav Brain Res 1994;62:1-9.
16. Foy MR, Stanton ME, Levine S, Thompson RF. Behavioral stress impairs long-term potentiation in rodent hippocampus. Behav Neural Biol 1987;48:138-149.
17. Huang FL, Yoshida Y, Nakabayashi H, Young WS, Huang KP. Immunocytochemical localisation of protein kinase C isozymes in rat brain. J Neurosci 1988;8:4734-4744.
18. Kerr DS, Huggett AM, Abraham WC. Modulation of hippocampal long-term potentiation and long-term depression by corticosteroid receptor activation. Psychobiology 1994;22:123-133.
19. Koolhaas JM, Hermann PM, Kemperman C, Bohus B, Van den Hoofdakker RH, Beersma DGM. Single social interaction leading to defeat in male rat induces a gradual but long-lasting behavioral change: A model of depression? Neurosci Res Commun 1990;7:35-41.
20. Krugers HJ, Koolhaas JM, Medema RM, Korf J. Prolonged subordination stress increases calbindin-D28k immunoreactrvity in the rat hippocampal CA1 area Brain Res 1996;729:289-293.
21. Luine VN, Spencer RL, McEwen BS. Effects of chronic corticosterone ingestion on spatial memory performance and hippocampal serotonergic function. Brain Res 1993;616:65-70.
22. Luine V, Villegas M, Martinez C, McEwen BS. Repeated stress causes impairments of spatial memory performance. Brain Res 1994;639:167-170.
23. Magarinos AM, McEwen BS. Stress-induced atrophy of apical dendrites of hippocampal CA3c neurons: Involvement of glucocorticoid secretion and excitatory arnino acid receptors. Neuroscience 1995;69:89-98.
24. McEwen BS, Sapolsky RM. Stress and cognitive function. Curr Opin Neurobiol 1995;5:205-216.
25. McNaughton BL, Barnes CA, Rao G, Baldwin J, Rasmussen M. Long-term enhancement of hippocampal synaptic transmission and the acquisition of spatial information. J Neurosci 1986;6:563-571.
26. Meyer JS, Micco DJ, Stephenson BS, Krey LC, McEwen BS. Subcutaneous implantation method for chronic glucocorticoid replacement therapy Physiol Behav 1979;22:867-870.
27. Moghaddam B. Stress preferentially increases extraneuronal levels of excitatory amino- acids in the prefrontal cortex: Comparison to hippocampus and basal ganglia. J Neurochem 1993;60:1650-1657.
28. Nadel L. The hippocampus and space revisited. Hippocampus 1991;1: 221-229.
29. Nogués X, Jaftard R, Micheau J. Investigations on the role of hippocampal protein kinase C on memory processes: Pharmacological approach. Behav Brain Res 1996;75:139-146.
30. Oades RD, Isaacson RL. The development of food search behaviour in rats: The effects of hippocampal damage and haloperidol. Behav Biol 1987;24:327-337.
31. Oitzl MS, de Kloet ER. Selective corticosteroid antagonists modulate specific aspects of spatial orientation learning. Behav Neurosci 1992;106:62-71
32. O'Keefe J, Nadel L. The hippocampus as a cognitive map. London: Oxford University Press, 1978.
33. Olds JL, Anderson ML, McPhie DL, Staten LD, Alkon DL. Imaging of memory specific changes in the distribution of protein kinase C in the hippocampus. Science 1989;245:866-869.
34. Olds JL, Golski S, McPhie DL, Olton D, Mishkin M, Alkon DL. Discrimination learning alters the distribution of protein kinase C in the hippocampus of rats. J Neurosci 1990;10:3707-3713.
35. O'Mara S. Spatially selective firing properties of hippocampal formation neurons in rodents and primates. Prog Neurobiol 1995;45:253-274.
36. Pavlides C, Watanabe Y, McEwen BS. Effects of glucocorticoids on hippocampal long-term potentiation. Hippocampus 1993;3:183-192.
37. Pavlides C, Kimura A, Magarinos AM, McEwen BS. Hippocampal homosynaptic long-term depression/aepotentiation induced by adrenal steroids Neuroscience 1995a;68:379-385.
38. Pavlides C, Watanabe Y, Magarinos AM, McEwen BS. Opposing roles of type I and type II adrenal steroid receptors in hippocampal long-term potentiation. Neuroscience 1995b;68:387-294.
39. Paxinos G, Watson C. The rat brain in stereotaxic coordinates. New York Academic Press, 1982.
40. Paylor R, Rudy JW, Wehner JM. Acute phorbol ester treatment improves spatial learning performance in rats. Behav Brain Res 1991;45:189-193.
41. Saito N, Kikkawa U, Nishizuka Y, Tanaka C. Distribution of protein kinase C-like immunoreactive neurons in rat brain. J Neurosci 1988;8:369-382.
42. Sandi C, Rose SPR. Corticosteroid receptor antagonists are amnestic for passive avoidance learning in day-old chicks. Eur J Neurosci 1994a;6: 1292-1297
43. Sandi C, Rose SPR. Corticosterone enhances long-term retention in one-day-old chicks trained in a weak passive avoidance paradigm. Brain Res 1994b;647:106-112.
44. Scharenberg AM, Olds JL, Schreurs BG, Craig AM, Alkon DL. Protein kinase C redistribution within CA3 stratum oriens during acquisition of nictitating membrane conditioning in the rabbit. Proc Natl Acad Sci USA 1991;88:6637-6641.
45. Schmajuk NA. Role of the hippocampus in temporal and spatial navigation: An adaptive neural network. Behav Brain Res 1990;39: 205-229.
46. Shimizu K, Amagaya S, Ogihara Y. Analysis of corticosterone in the serum of mice and rats using high-performance liquid chromatography. J Chromatogr 1983;272:170-175.
47. Shors TJ, Servatius RJ. Stress-induced sensitisation and facilitated learning require NMDA receptor activation. NeuroReport 1995;6: 677-680.
48. ShorsTJ, Seib TB, Levine S, Thompson RF. Inescapable versus escapable shock modulates long-term potentiation in the rat hippocampus. Science 1989;244:224-226.
49. Shors TJ, Weiss C, Thompson RF. Stress-induced facilitation of classical conditioning. Science 1992;257:537-539.
50. Steffens AB. A method for frequent sampling of blood and continuous infusion of fluids in the rat without disturbing the animal. Physiol Behav 1969;4:833-836.
51. Sunayashiki-Kusuzaki H, Lester DS, Schreurs B, Alkon DL. Associative learning potentiates protein kinase C activation in synaptosomes of the rabbit hippocampus. Proc Natl Acad Sci USA 1993;90:4286-4289.
52. Tsuyama S, Bramblett GT, Huang K-P, Flavin, M. Calcium-phospholipid-dependent kinases recognizes sites in microtubule-associated protein 2 which are phosphorylated in living brain and are not accessible to other kinases. J Biol Chem 1986;261:4110-4116.
53. Van der Zee EA, Compaan JC, De Boer M, Luiten PGM. Changes in PKCγ immunoreactivity in mouse hippocampus induced by spatial discrimination learning. J Neurosci 1992;12:4808-4815.
54. Van der Zee EA, Compaan JC, Bohus B, Luiten PGM. Alterations in the immunoreactivity for muscarinic acetylcholine receptors and colocalized PKCγ in mouse hippocampus induced by spatial discrimination learning. Hippocampus 1995a;5:349-362.
55. Van der Zee EA, Palm IF, Kronforst MA, Maizels M, Shanmugam M, Hunzicker-Dunn M, Disterhoft JF. Trace and delay eyeblink conditioning induce alterations in the immunoreactivity for PKCγ in the rabbit hippocampus. Soc Neurosci Abstr 1995b;478.6.
56. Van der Zee EA, Luiten PGM, Disterhoft JF. Learning-induced alterations in hippocampal PKC-immunoreactivity: A review and hypothesis of its functional significance. Prog Neuropsychopharmacol Biol Psychiatr, in press.
57. Watanabe Y, Gould E, McEwen BS. Stress induces atrophy of apical dendrites of hippocampal CA3 pyramidal neurons. Brain Res 1992; 588:341-345.
58. Wehner JM, Sleight S, Upchurch M. Hippocampal protein kinase C activity is reduced in poor spatial learners. Brain Res 1990;523:181-187.
59. Woolley CS, Gould E, McEwen BS. Exposure to excess glucocorticoids alters dendritic morphology of adult hippocampal pyramidal neurons. Brain Res 1990;531:225-331.
60. Zhao W-Q, Sedman GL, Gibbs ME, Ng KT. Effect of PKC inhibitors and activators on memory. Behav Brain Res 1994;60:151-160.
61. Zola-Morgan SM, Squire LR. The primate hippocampal formation: Evidence for a time-limited role in memory storage. Science 1990;250: 288-290.