Acute stress does not affect the impairing effect of chronic stress on memory retrieval

Document Type : Original Article

Authors

1 School of Biology, Damghan University, Damghan, Iran

2 Laboratory of Learning and Memory, Research Center and Department of Physiology, School of Medicine, Semnan University of Medical Sciences, Semnan, Iran

Abstract

Objective(s): Due to the prevalence and pervasiveness of stress in modern life and exposure to both chronic and acute stresses, it is not clear whether prior exposure to chronic stress can influence the impairing effects of acute stress on memory retrieval. This issue was tested in this study.
Materials and Methods: Adult male Wistar rats were randomly assigned to the following groups: control, acute, chronic, and chronic + acute stress groups. The rats were trained with six trials per day for 6 consecutive days in the water maze. Following training, the rats were either kept in control conditions or exposed to chronic stress in a restrainer 6 hr/day for 21 days. On day 22, a probe test was done to measure memory retention. Time spent in target and opposite areas, platform location latency, and proximity were used as indices of memory retention. To induce acute stress, 30 min before the probe test, animals received a mild footshock.
Results: Stressed animals spent significantly less time in the target quadrant and more time in the opposite quadrant than control animals. Moreover, the stressed animals showed significantly increased platform location latency and proximity as compared with control animals. No significant differences were found in these measures among stress exposure groups. Finally, both chronic and acute stress significantly increased corticosterone levels.
Conclusion: Our results indicate that both chronic and acute stress impair memory retrieval similarly. Additionally, the impairing effects of chronic stress on memory retrieval were not influenced by acute stress.

Keywords


1. Scoville WB, Milner B. Loss of recent memory after bilateral hippocampal lesions. J Neurol Neurosurg Psychiatry 1957; 20:11-21.
2. Squire LR, Zola-Morgan S. The medial temporal lobe memory system. Science. 1991; 253:1380-1386.
3. Eichenbaum H. A cortical-hippocampal system for declarative memory. Nat Rev Neurosci 2000; 1:41-50.
4. Morris RG, Garrud P, Rawlins JN, O'Keefe J. Place navigation impaired in rats with hippocampal lesions. Nature 1982; 297:681-683.
5. Moser EI, Krobert KA, Moser MB, Morris RG. Impaired spatial learning after saturation of long-term potentiation. Science 1998, 281:2038-2042.
6. McEwen BS. Physiology and neurobiology of stress and adaptation: central role of the brain. Physiol Rev 2007; 87:873-904.
7. de Kloet ER, Joels M, Holsboer F. Stress and the brain: from adaptation to disease. Nat Rev Neurosci 2005; 6:463-475.
8. Howland JG, Wang YT. Synaptic plasticity in learning and memory: stress effects in the hippocampus. Prog Brain Res 2008; 169:145-158.
9. Magarinos AM, McEwen BS. Stress-induced atrophy of apical dendrites of hippocampal CA3c neurons: involvement of glucocorticoid secretion and excitatory amino acid receptors. Neuroscience 1995; 69:89-98.
10. Magarinos AM, McEwen BS, Flugge G, Fuchs E. Chronic psychosocial stress causes apical dendritic atrophy of hippocampal CA3 pyramidal neurons in subordinate tree shrews. J Neurosci 1996; 16:3534-3540.
11. Alfarez DN, Karst H, Velzing EH, Joels M, Krugers HJ. Opposite effects of glucocorticoid receptor activation on hippocampal CA1 dendritic complexity in chronically stressed and handled animals. Hippocampus 2008; 18:20-28.
12. Donohue HS, Gabbott PL, Davies HA, Rodriguez JJ, Cordero MI, Sandi C, et al. Chronic restraint stress induces changes in synapse morphology in stratum lacunosum-moleculare CA1 rat hippocampus: a stereological and three-dimensional ultrastructural study. Neuroscience 2006; 140:597-606.
13. Shors TJ, Falduto J, Leuner B. The opposite effects of stress on dendritic spines in male vs. female rats are NMDA receptor-dependent. Eur J Neurosci 2004; 19:145-150.
14. Chen Y, Dube CM, Rice CJ, Baram TZ. Rapid loss of dendritic spines after stress involves derangement of spine dynamics by corticotropin-releasing hormone. J Neurosci 2008; 28:2903-2911.
15. de Kloet ER, Oitzl MS, Joels M. Stress and cognition: are corticosteroids good or bad guys? Trends Neurosci 1999; 22:422-426.
16. Oitzl MS, de Kloet ER. Selective corticosteroid antagonists modulate specific aspects of spatial orientation learning. Behav Neurosci 1992; 106:62-71.
17. Roozendaal B, McGaugh JL. Basolateral amygdala lesions block the memory-enhancing effect of glucocorticoid administration in the dorsal hippocampus of rats. Eur J Neurosci 1997; 9:76-83.
18. Diamond DM, Rose GM. Stress impairs LTP and hippocampal-dependent memory. Ann N Y Acad Sci 1994; 746:411-414.
19. Diamond DM, Fleshner M, Ingersoll N, Rose GM. Psychological stress impairs spatial working memory: relevance to electrophysiological studies of hippocampal function. Behav Neurosci 1996; 110:661-672.
20. de Quervain DJ, Roozendaal B, McGaugh JL. Stress and glucocorticoids impair retrieval of long-term spatial memory. Nature 1998; 394:787-790.
21. Pakdel R, Rashidy-Pour A. Glucocorticoid-induced impairment of long-term memory retrieval in rats: an interaction with dopamine D2 receptors. Neurobiol Learn Mem 2006; 85:300-306.
22. Rashidy-Pour A, Sadeghi H, Taherain AA, Vafaei AA, Fathollahi Y. The effects of acute restraint stress and dexamethasone on retrieval of long-term memory in rats: an interaction with opiate system. Behav Brain Res 2004; 154:193-198.
23. de Quervain DJ, Roozendaal B, Nitsch RM, McGaugh JL, Hock C. Acute cortisone administration impairs retrieval of long-term declarative memory in humans. Nature Neurosci 2000; 3:313-314.
24. Wolf OT, Convit A, McHugh PF, Kandil E, Thorn EL, De Santi S, et al. Cortisol differentially affects memory in young and elderly men. Behav Neurosci 2001; 115:1002-1011.
25. Lupien SJ, Gaudreau S, Tchiteya BM, Maheu F, Sharma S, Nair N P, et al. Stress-induced declarative memory impairment in healthy elderly subjects: relationship to cortisol reactivity. J Clin Endocrinol Metab 1997; 82:2070-2075.
26. Krugers HJ, Douma BR, Andringa G, Bohus B, Korf J, Luiten PG. Exposure to chronic psychosocial stress and corticosterone in the rat: effects on spatial discrimination learning and hippocampal protein kinase Cgamma immunoreactivity. Hippocampus 1997; 7:427-436.
27. Magarinos AM, McEwen BS. Stress-induced atrophy of apical dendrites of hippocampal CA3c neurons: comparison of stressors. Neuroscience 1995; 69:83-88.
28. De Kloet ER, Vreugdenhil E, Oitzl MS, Joels M. Brain corticosteroid receptor balance in health and disease. Endocr Rev 1998; 19:269-301.
29.  McEwen  BS. Stress and hippocampal plasticity. Annu Rev Neurosci 1999; 22:105-122.
30. Conrad CD, Galea LA, Kuroda Y, McEwen BS. Chronic stress impairs rat spatial memory on the Y maze, and this effect is blocked by tianeptine pretreatment. Behav Neurosci 1996; 110:1321-1334.
31. Fuchs E, Flugge G, Ohl F, Lucassen P, Vollmann-Honsdorf GK, Michaelis T. Psychosocial stress, glucocorticoids, and structural alterations in the tree shrew hippocampus. Physiol Behav 2001; 73:285-291.
32. Sandi C, Merino JJ, Cordero MI, Touyarot K, Venero C. Effects of chronic stress on contextual fear conditioning and the hippocampal expression of the neural cell adhesion molecule, its polysialylation, and L1. Neuroscience 2001; 102:329-339.
33. Sandi C, Davies HA, Cordero MI, Rodriguez JJ, Popov VI, Stewart MG. Rapid reversal of stress induced loss of synapses in CA3 of rat hippocampus following water maze training. Eur J Neurosci 2003; 17:2447-2456.
34. Cordero MI, Kruyt ND, Sandi C. Modulation of contextual fear conditioning by chronic stress in rats is related to individual differences in behavioral reactivity to novelty. Brain Res 2003; 970:242-245.
35. Alkadhi K. Brain Physiology and Pathophysiology i n Mental Stress. ISRN Physiol 2013; 2013:23.
36. Sapolsky RM. Glucocorticoids, stress, and their adverse neurological effects: relevance to aging. Exp Gerontol 1999; 34:721-732.
37. Gilbertson MW, Shenton ME, Ciszewski A, Kasai K, Lasko NB, Orr SP, et al. Smaller hippocampal volume predicts pathologic vulnerability to psychological trauma. Nat Neurosci 2002; 5:1242-1247.
38. Mohammadi HS, Goudarzi I, Lashkarbolouki T, Abrari K, Elahdadi Salmani M. Chronic administration of quercetin prevent spatial learning and memory deficits provoked by chronic stress in rats. Behav Brain Res 2014; 270:196-205.
39. Rashidy-Pour A, Vafaei AA, Taherian AA, Miladi-Gorji H, Sadeghi H, Fathollahi Y, et al. Verapamil enhances acute stress or glucocorticoid-induced deficits in retrieval of long-term memory in rats. Behav Brain Res 2009; 203:76-80.
40. Ghadrdoost B, Vafaei AA, Rashidy-Pour A, Hajisoltani R, Bandegi AR, Motamedi F, et al. Protective effects of saffron extract and its active constituent crocin against oxidative stress and spatial learning and memory deficits induced by chronic stress in rats. Eur J Pharmacol 2011; 667:222-229.
41. Salin PA, Bullier J. Corticocortical connections in the visual system: structure and function. Physiol Rev 1995; 75:107-154.
42. Nelson JI, Frost BJ. Orientation-selective inhibition from beyond the classic visual receptive field. Brain Res 1978; 139:359-365.
43. Vanduffel W, Orban GA, Lomber SG, Payne BR. Functional impact of cerebral projection systems. Mol Psychiatry 1998; 3:215-219.
44. Kirschbaum C, Wolf OT, May M, Wippich W, Hellhammer DH. Stress- and treatment-induced elevations of cortisol levels associated with impaired declarative memory in healthy adults. Life Sci 1996; 58:1475-1483.
45. Kim JJ, Diamond DM. The stressed hippocampus, synaptic plasticity and lost memories. Nat Rev Neurosci  2002; 3:453-462.
46. Diamond DM, Park CR, Heman KL, Rose GM. Exposing rats to a predator impairs spatial working memory in the radial arm water maze. Hippocampus 1999; 9:542-552.
47. de Quervain DJ-F R, Benno; Nitsch, Roger M; McGaugh, James L.; Hock, Christoph???. Acute cortisone administration impairs retrieval of long-term declarative memory in humans. Nat Neurosci 2000; 3:313.
48. McLaughlin KJ, Gomez JL, Baran SE, Conrad CD. The effects of chronic stress on hippocampal morphology and function: an evaluation of chronic restraint paradigms. Brain Res 2007; 1161:56-64.
49. Song L, Che W, Min-Wei W, Murakami Y, Matsumoto K. Impairment of the spatial learning and memory induced by learned help