Role of the amygdala opioid system in the effects of stress on the post-learning sleep patterns of male Wistar rats

Articles in Press

Document Type : Original Article

Authors

1 Neuroscience Research Center, Baqiyatallah University of Medical Sciences, Tehran, Tehran, Iran

2 Department of Physiology and Medical Physics, School of Medicine, Baqiyatallah University of Medical Sciences, Tehran, Iran

3 Students’ Research Committee, Baqiyatallah University of Medical Sciences, Tehran, Iran

10.22038/ijbms.2024.79291.17266

Abstract

Objective(s): Three physiological processes interact: sleep, learning, and stress. It is essential to understand how stress affects and interacts with the link between sleep, learning, and memory since it has long been recognized that sleep plays a crucial role in memory consolidation and learning. Through naloxone injection in the Baso Lateral Amygdala (BLA), this study intends to shed light on the interactions between stress, learning, and sleep, as well as the function of the opioid system and its impact on Brain-Derived Neurotrophic Factor (BDNF) production in the hippocampus.
Materials and Methods: Male Wistar rats (n=77) in eleven groups were implanted with electroencephalogram (EEG) and electromyography (EMG) recording electrodes, and the BLA area was bilaterally cannulated. Recordings of Rapid Eye Movement (REM) and Non-Rapid Eye Movement (NREM) sleep and wakefulness steps were made for the three hours prior to and three hours following the implementation of the immobility stress protocol and learning with the Barnes maze for three consecutive days. Also, the animals’ memory was tasted 48 hr later. Before the stress and learning procedure, naloxone was injected into each BLA three times in a row at a dosage of 0.05 μg or 0.1 μg in a volume of 0.5 μl. A molecular biomarker of learning and stress, BDNF, was also examined.
Results: The study demonstrated that the immobility stress model lowers REM and NREM sleep. On the other hand, putting the learning technique into practice results in more REM and NREM sleep, and stress situations do not stop this rise after learning. Naloxone injections in the BLA region also enhance learning and memory, preventing stress-related REM and NREM sleep loss. Additionally, stress lowers BDNF expression in the hippocampal region. BDNF expression rises in the hippocampus throughout the learning process, and naloxone administration in the BLA area also raises BDNF expression in the hippocampus.
Conclusion: Stress generally reduces REM, NREM, and BDNF expression in the hippocampal region. Under stress, using the learning protocol increases REM, NREM sleep, and BDNF. Naloxone injection in BLA improves memory and learning, reducing stress-induced memory loss.

Keywords

Main Subjects

References

1. Rotenberg VS. Sleep and memory. I: The influence of different sleep stages on memory. Neurosci Biobehav Rev 1992;16:497-502.
2. Han KS, Kim L, Shim I. Stress and sleep disorder. Exp Neurobiol 2012;21:141-150.
3. Patterson TA, Schulteis G, Alvarado MC, Martinez JL, Jr., Bennett EL, Rosenzweig MR, et al. Influence of opioid peptides on learning and memory processes in the chick. Behav Neurosci 1989;103:429-437.
4. Baidoo N, Wolter M, Leri F. Opioid withdrawal and memory consolidation. Neurosci Biobehav Rev 2020;114:16-24.
5. Yang Y, Wang JZ. From structure to behavior in basolateral amygdala-hippocampus circuits. Front Neural Circuits 2017;11:86-93.
6. Wellman LL, Fitzpatrick ME, Machida M, Sanford LD. The basolateral amygdala determines the effects of fear memory on sleep in an animal model of PTSD. Exp Brain Res 2014;232:1555-1565.
7. Lu Y, Christian K, Lu B. BDNF: A key regulator for protein synthesis-dependent LTP and long-term memory? Neurobiol Learn Mem 2008;89:312-323.
8. Genzel L, Spoormaker VI, Konrad BN, Dresler M. The role of rapid eye movement sleep for amygdala-related memory processing. Neurobiol Learn Mem 2015;122:110-121.
9. Babaei P, Vahdati S, Soltani-Tehrani B. BDNF Pretreatment Attenuates Morphine-Induced Learning and Memory Impairment in Rats. Caspian J Neurologi Sci 2015;1:12-18.
10. Eacret D, Veasey S, Blendy J. Bidirectional relationship between opioids and disrupted sleep: Putative mechanisms. Molecul Pharmacol 2020;98:445-453.
11. Meilandt WJ, Barea-Rodriguez E, Harvey SA, Martinez JL. Role of hippocampal CA3 μ-opioid receptors in spatial learning and memory. J Neurosci 2004;24:2953-2962.
12. Introini-Collison IB, Nagahara AH, McGaugh JL. Memory enhancement with intra-amygdala post-training naloxone is blocked by concurrent administration of propranolol. Brain Res 1989;476:94-101.
13. Paxinos G, Watson C. The Rat Brain in Stereotaxic Coordinates: Hard cover Edition: Elsevier; 2006.
14. Erfani Sharifian F, Bahrami F, Yeganegi H, Geraily Afra M. Alteration in REM sleep and sleep spindles’ characteristics by a model of immobilization stress in rat. Sleep Biol Rhythm 2020;18:233-241.
15. Gilmour TP, Fang J, Guan Z, Subramanian T. Manual rat sleep classification in principal component space. Neurosci Lett 2010;469:97-101.
16. Mileva-Seitz VR, Louis RP, Stephenson R. A visual aid for computer-based analysis of sleep-wake state in rats. J Neurosci Methods 2005;148:43-48.
17. Kohtoh S, Taguchi Y, Matsumoto N, Wada M, Huang Z-L, Urade Y. Algorithm for sleep scoring in experimental animals based on fast Fourier transform power spectrum analysis of the electroencephalogram. Sleep Biol Rhythm 2008;6:163-171.
18. Zhong P, Zhang Z, Barger Z, Ma C, Liu D, Ding X, et al. Control of non-REM sleep by midbrain neurotensinergic neurons. Neuron. 2019;104:795-809 e6.
19. Bahrami F, Zekri S, Sahraei H. Cinnamaldehyde antagonizes REM sleep reduction induced by immobilization stress in rats. J Mazandaran Univ Med Sci 2019;29:14-24.
20. Afra MG, Bahrami F, Sahraei H, Bahari Z, Gharib A, Ghoshooni H. Enhancement of slow wave sleep after learning procedure even in immobilization stress condition. Focus Med Sci J 2019;5.
21. Hoheisel U, Vogt M, Palme R, Gass P, Mense S. Immobilization stress sensitizes rat dorsal horn neurons having input from the low back. Europ J Pain 2015;19:861-870.
22. Carrasco G, Van de Kar L. Neuroendocrine pharmacology of stress. Europ  J Pharmacol 2003;463:235-272.
23. Kim E-J, Dimsdale JE. The effect of psychosocial stress on sleep: A review of polysomnographic evidence. Behav Sleep Med 2007;5:256-278.
24. Cui R, Li B, Suemaru K, Araki H. Differential effects of psychological and physical stress on the sleep pattern in rats. Acta Med Okayama 2007;61:319-327.
25. Bonnet C, Marinesco S, Debilly G, Kovalzon V, Cespuglio R. Influence of a 1-h immobilization stress on sleep and CLIP (ACTH(18-39)) brain contents in adrenalectomized rats. Brain Res 2000;853:323-329.
26. Sharifian FE, Bahrami F, Yeganegi H, Afra MG. Alteration in REM sleep and sleep spindles’ characteristics by a model of immobilization stress in rat. Sleep Biol Rhythm 2020;18:1-9.
27. Herman JP, McKlveen JM, Ghosal S, Kopp B, Wulsin A, Makinson R, et al. Regulation of the hypothalamic-pituitary-adrenocortical stress response. Compr Physiol 2016;6:603-621.
28. Pawlyk AC, Morrison AR, Ross RJ, Brennan FX. Stress-induced changes in sleep in rodents: Models and mechanisms. Neurosci Biobehav Rev 2008;32:99-117.
29. Palma BD, Suchecki D, Tufik S. Differential effects of acute cold and footshock on the sleep of rats. Brain Res 2000;861:97-104.
30. Wells AM, Ridener E, Bourbonais CA, Kim W, Pantazopoulos H, Carroll FI, et al. Effects of chronic social defeat stress on sleep and circadian rhythms are mitigated by kappa-opioid receptor antagonism. J Neurosci 2017;37:7656-7668.
31. Wassing R, Lakbila-Kamal O, Ramautar JR, Stoffers D, Schalkwijk F, Van Someren EJW. Restless REM sleep impedes overnight amygdala adaptation. Curr Biol 2019;29:2351-8 e4.
32. McEwen BS, Bowles NP, Gray JD, Hill MN, Hunter RG, Karatsoreos IN, et al. Mechanisms of stress in the brain. Nat Neurosci 2015;18:1353-1363.
33. Jegou A, Schabus M, Gosseries O, Dahmen B, Albouy G, Desseilles M, et al. Cortical reactivations during sleep spindles following declarative learning. Neuroimage. 2019;195:104-112.
34. Newbury CR, Crowley R, Rastle K, Tamminen J. Sleep deprivation and memory: Meta-analytic reviews of studies on sleep deprivation before and after learning. Psychol Bull 2021;147:1215-1240.
35. Cousins JN, Sasmita K, Chee MWL. Memory encoding is impaired after multiple nights of partial sleep restriction. J Sleep Res 2018;27:138-145.
36. Navarro-Lobato I, Genzel L. The up and down of sleep: From molecules to electrophysiology. Neurobiol Learn Mem 2019;160:3-10.
37. Jiao H, Yan Z, Ma Q, Li X, Jiang Y, Liu Y, et al. Influence of Xiaoyaosan on depressive-like behaviors in chronic stress-depressed rats through regulating tryptophan metabolism in hippocampus. Neuropsychia Dis Treat 2019;15:21-31.
38. Abel T, Havekes R, Saletin JM, Walker MP. Sleep, plasticity and memory from molecules to whole-brain networks. Curr Biol 2013;23:R774-R788.
39. Joels M, Fernandez G, Roozendaal B. Stress and emotional memory: A matter of timing. Trends Cogn Sci 2011;15:280-288.
40. Yaribeygi H, Panahi Y, Sahraei H, Johnston TP, Sahebkar A. The impact of stress on body function: A review. EXCLI J 2017;16:1057-1072.
41. Liu Y, Wu YW, Qian ZQ, Yan CF, Fan KM, Xu JH, et al. Effect of opioid receptors on acute stress-induced changes in recognition memory. Sheng Li Xue Bao 2016;68:757-766.
42. Cronin A, Keifer J, Baghdoyan H, Lydic R. Opioid inhibition of rapid eye movement sleep by a specific mu receptor agonist. British J Anaesth 1995;74:188-192.
43. Wang Q, Yue X-F, Qu W-M, Tan R, Zheng P, Urade Y, et al. Morphine inhibits sleep-promoting neurons in the ventrolateral preoptic area via mu receptors and induces wakefulness in rats. Neuropsychopharmacology 2013;38:791-801.
44. Cordner Z, Tamashiro K. Effects of chronic variable stress on cognition and Bace1 expression among wild-type mice. Translation Psychia 2016;6:e854-e.
45. Pandey SC, Zhang H, Roy A, Misra K. Central and medial amygdaloid brain-derived neurotrophic factor signaling plays a critical role in alcohol-drinking and anxiety-like behaviors. J Neurosci 2006;26:8320-8331.
46. Schulte-Herbrüggen O, Chourbaji S, Ridder S, Brandwein C, Gass P, Hörtnagl H, et al. Stress-resistant mice overexpressing glucocorticoid receptors display enhanced BDNF in the amygdala and hippocampus with unchanged NGF and serotonergic function. Psychoneuroendocrinology 2006;31:1266-1277.
47. Boersma GJ, Lee RS, Cordner ZA, Ewald ER, Purcell RH, Moghadam AA, et al. Prenatal stress decreases Bdnf expression and increases methylation of BDNF exon IV in rats. Epigenetics. 2014;9:437-447.
48. Miranda M, Morici JF, Zanoni MB, Bekinschtein P. Brain-derived neurotrophic factor: A key molecule for memory in the healthy and the pathological brain. Frontier Cell Neurosci 2019:363-387.
49. Anastasia A, Hempstead BL. BDNF function in health and disease. Nat Rev Neurosci 2014;15.
50. Bachmann V, Klein C, Bodenmann S, Schafer N, Berger W, Brugger P, et al. The BDNF Val66Met polymorphism modulates sleep intensity: EEG frequency- and state-specificity. Sleep 2012;35:335-344.
51. Giese M, Unternahrer E, Huttig H, Beck J, Brand S, Calabrese P, et al. BDNF: An indicator of insomnia? Mol Psychiatry 2014;19:151-152.
52. Rahmani M, Rahmani F, Rezaei N. The brain-derived neurotrophic factor: missing link between sleep deprivation, insomnia, and depression. Neurochem Res 2020;45:221-231.
53. HB G. Akil H. Opioid Analgesics. Brunton LL, Lazo JS, Editors Goodman & Gilman’s The Pharmacological Basis of Therapeutics. 2001;11:547-590.
54. Conte F, Carobbi G, Errico BM, Ficca G. The effects of pre-sleep learning on sleep continuity, stability, and organization in elderly individuals. Front Neurol 2012;3:109-117.
Iranian Journal of Basic Medical Sciences

Articles in Press, Accepted Manuscript
Available Online from 18 September 2024

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