Evaluating of the Role of 5HT3 Serotonergic Receptors in Hippocampal CA1 area on Pain, Memory and Motor Activity after 6 hours of REM and Total Sleep Deprivation

Document Type : Original Article

Author

teacher- education

Abstract

Background and Objectives: Sleep is a reversible state in which the capacity for reaction and interaction with the environment is limited and consciousness is lost. 5HT3 receptors are mainly expressed in hippocampus CA1 regions, plays a vital role in sleep regulation and memory consolidation. The present study aims to investigate the effects of activation and inactivation of serotonin 5HT3 receptor by use of 5HT3 agonist and antagonist (MCHL and Y25130) respectively on acquired memory impairment induced by total sleep deprivation and REM sleep deprivation in rat,
Subjects and Methods: Male Wistar rats were randomly assigned to five groups including eight rats: 1- Two groups receiving effective doses of 5HT3 receptor antagonist (MCHL) and agonist (Y25130); 2- TSD control group 3- With TSD sleep deprivation 4- RSD control groups 5- with RSD sleep deprivation. Water box apparatus was used to induce total sleep deprivation, multi-platform apparatus was applied to induce RSD. Passive avoidance memory test was used to evaluate memory consolidation.
Results: Doses of 0.01 and 0.001 mg MCHL and 0.1 mg Y25130 significantly reduced the acquired memory (P <0.01). While MCHL at 0.1 and Y25130 at doses of 0.01 and 0.1 significantly increased motor activities (P <0.01). However, both drugs did not significantly affect the pain at all tested doses. TSD and RSD- induced amnesia was improved significantly (P <0.01) by Y25130 with sub- threshold dose. While both drugs had no significant effect on motor activity in TSD and RSD conditions (P> 0.05). But, MCHL under RSD conditions and Y25130 under TSD conditions significantly (P Conclusion: It seems that CA1 5HT3 receptor plays a critical role in cognitive and non-cognitive behaviors

Keywords

References

1-Colavito V, Fabene PF, Grassi-Zucconi G, Pifferi F, Lamberty Y, Bentivoglio M, et al. Experimental sleep deprivation as a tool to test memory deficits in rodents. Frontiers in systems neuroscience. 2013;  7- 106. Dec 13;7:106. PubMed PMID: 24379759.
2-Kim Y, Elmenhorst D, Weisshaupt A, Wedekind F, Kroll T, McCarley RW, et al. Chronic sleep restriction induces long-lasting changes in adenosine and noradrenaline receptor density in the rat brain. Journal of sleep research. 2015 Oct;24(5):549-58. PubMed PMID: 25900125.
3-Graves L, Pack A, Abel T. Sleep and memory: a molecular perspective. Trends in neurosciences. 2001:237-43. PubMed PMID: 11250009.
4-Uschakov A, Grivel J, Cvetkovic-Lopes V, Bayer L, Bernheim L, Jones BE, et al. Sleep-deprivation regulates alpha-2 adrenergic responses of rat hypocretin/orexin neurons. PloS one. 2011;3-4. PubMed PMID: 21347440.
5-Jones DG, Endsley MR. Sources of situation awareness errors in aviation. Aviation, space, and environmental medicine. 1996:507-12. PubMed PMID: 8827130.
6-Westcott KJ. Modafinil, sleep deprivation, and cognitive function in military and medical settings. Military medicine. 2005:333-5. PubMed PMID: 15916305.
7-van Hulzen ZJ, Coenen AM. Paradoxical sleep deprivation and locomotor activity in rats. Physiology & behavior. 1981:741-4. PubMed PMID: 7323178.
8- Albertazzi P. Noradrenergic and serotonergic modulation to treat vasomotor symptoms. The journal of the British Menopause Society. 2006:7-11. PubMed PMID: 16513016.
9-Fink KB, Gothert M. 5-HT receptor regulation of neurotransmitter release. Pharmacological reviews. 2007:360-417. PubMed PMID: 18160701.
10-Chegini HR, Nasehi M, Zarrindast MR. Differential role of the basolateral amygdala 5-HT3 and 5-HT4 serotonin receptors upon ACPA-induced anxiolytic-like behaviors and emotional memory deficit in mice. Behavioural brain research. 2014:114-26. PubMed PMID: 24333573.
11-Raiteri M. Functional pharmacology in human brain. Pharmacological reviews. 2006 Jun;58(2):162-93. PubMed PMID: 16714485.
12-Ariel P, Ryan TA. New insights into molecular players involved in neurotransmitter release. Physiology. 2012:15-24. PubMed PMID: 22311967.
 13-Hampson RE, Deadwyler SA. Cannabinoids reveal the necessity of hippocampal neural encoding for short-term memory in rats. The Journal of neuroscience : the official journal of the Society for Neuroscience. 2000:8932-42. PubMed PMID: 11102504.
14-Meneses A. Stimulation of 5-HT1A, 5-HT1B, 5-HT2A/2C, 5-HT3 and 5-HT4 receptors or 5-HT uptake inhibition: short- and long-term memory. Behavioural brain research. 2007:81-90. PubMed PMID: 17692935.
15-Prince TM, Abel T. The impact of sleep loss on hippocampal function. Learning & memory. 2013:558-69. PubMed PMID: 24045505. Pubmed Central PMCID: 3768199
16-Hakki Onen S, Alloui A, Jourdan D, Eschalier A, Dubray C. Effects of rapid eye movement (REM) sleep deprivation on pain sensitivity in the rat. Brain research. 2001:261-7. PubMed PMID: 11334806.
17-Zarrindast MR, Nasehi M, Pournaghshband M, Yekta BG. Dopaminergic system in CA1 modulates MK-801 induced anxiolytic-like responses. Pharmacology, biochemistry, and behavior. 2012:102-10. PubMed PMID: 22885281.
18-Naseri MH, Hesami-Tackallou S, Torabi-Nami M, Zarrindast MR, Nasehi M. Involvement of the CA1 GABAA receptors in MK-801-induced anxiolytic-like effects: an isobologram analysis. Behavioural pharmacology. 2014 Jun;25(3):197-205. PubMed PMID: 24710315.
19-Pierard C, Liscia P, Chauveau F, Coutan M, Corio M, Krazem A, et al. Differential effects of total sleep deprivation on contextual and spatial memory: modulatory effects of modafinil. 2011:399-405. PubMed PMID: 20883715
20-Pierard C, Liscia P, Philippin JN, Mons N, Lafon T, Chauveau F, et al. Modafinil restores memory performance and neural activity impaired by sleep deprivation in mice. 2007:55-63. PubMed PMID: 17698177.
21-McDermott CM, Hardy MN, Bazan NG, Magee JC. Sleep deprivation-induced alterations in excitatory synaptic transmission in the CA1 region of the rat hippocampus. The Journal of physiology. 2006:553-65. PubMed PMID: 16322058. Pubmed Central PMCID: 1479879.
22-Khakpai F, Nasehi M, Zarrindast MR. The role of NMDA receptors of the medial septum and dorsal hippocampus on memory acquisition. Pharmacology, biochemistry, and behavior. 2016:18-25. PubMed PMID: 26780596.
23-Hosseini N, Nasehi M, Radahmadi M, Zarrindast MR. Effects of CA1 glutamatergic systems upon memory impairments in cholestatic rats. Behavioural brain research. 2013:636-45. PubMed PMID: 24050889.
24-Norozpour Y, Nasehi M, Sabouri-Khanghah V, Torabi-Nami M, Zarrindast MR. The effect of CA1 alpha2 adrenergic receptors on memory retention deficit induced by total sleep deprivation and the reversal of circadian rhythm in a rat model. Neurobiology of learning and memory. 2016:53-60. PubMed PMID: 27291858.
25-Nasehi M, Sahebgharani M, Haeri-Rohani A, Zarrindast MR. Effects of cannabinoids infused into the dorsal hippocampus upon memory formation in 3-days apomorphine-treated rats. Neurobiology of learning and memory. 2009:391-9. PubMed PMID: 19450698.
26-Najar F, Nasehi M, Haeri-Rohani SA, Zarrindast MR. The involvement of medial septum 5-HT1 and 5-HT2 receptors on ACPA-induced memory consolidation deficit: possible role of TRPC3, TRPC6 and TRPV2. Journal of psychopharmacology. 2015:1200-8. PubMed PMID: 26464456.
27-Nasehi M, Tabatabaie M, Khakpai F, Zarrindast MR. The effects of CA1 5HT4 receptors in MK801-induced amnesia and hyperlocomotion. Neuroscience letters. 2015:73-8. PubMed PMID: 25524640.
28-Nascimento DC, Andersen ML, Hipolide DC, Nobrega JN, Tufik S. Pain hypersensitivity induced by paradoxical sleep deprivation is not due to altered binding to brain mu-opioid receptors. Behavioural brain research. 2007:216-20. PubMed PMID: 17239968.
29-Durmer JS, Dinges DF. Neurocognitive consequences of sleep deprivation. Seminars in neurology. 2005:117-29. PubMed PMID: 15798944.
30-Versace F, Cavallero C, De Min Tona G, Mozzato M, Stegagno L. Effects of sleep reduction on spatial attention. Biological psychology. 2006:248-55. PubMed PMID: 15978717.
31-Alhola P, Polo-Kantola P. Sleep deprivation: Impact on cognitive performance. Neuropsychiatric disease and treatment. 2007;3(5):553-67. PubMed PMID: 19300585. Pubmed Central PMCID: 2656292.
32-Bridoux A, Laloux C, Derambure P, Bordet R, Monaca Charley C. The acute inhibition of rapid eye movement sleep by citalopram may impair spatial learning and passive avoidance in mice. Journal of neural transmission. 2013:383-9. PubMed PMID: 23053350.
33-Alhaider IA, Aleisa AM, Tran TT, Alkadhi KA. Sleep deprivation prevents stimulation-induced increases of levels of P-CREB and BDNF: protection by caffeine. Molecular and cellular neurosciences. 2011:742-51. PubMed PMID: 21338685.
34-Copinschi G. Metabolic and endocrine effects of sleep deprivation. Essential psychopharmacology. 2005;6(6):341-7. PubMed PMID: 16459757.
35-Longordo F, Kopp C, Mishina M, Lujan R, Luthi A. NR2A at CA1 synapses is obligatory for the susceptibility of hippocampal plasticity to sleep loss. The Journal of neuroscience : the official journal of the Society for Neuroscience. 2009:9026-41. PubMed PMID: 19605640. Pubmed Central PMCID: 3849614.
36-Puig MV, Santana N, Celada P, Mengod G, Artigas F. In vivo excitation of GABA interneurons in the medial prefrontal cortex through 5-HT3 receptors. Cerebral cortex. 2004:1365-75. PubMed PMID: 15166106.
37-Turner TJ, Mokler DJ, Luebke JI. Calcium influx through presynaptic 5-HT3 receptors facilitates GABA release in the hippocampus: in vitro slice and synaptosome studies. Neuroscience. 2004;129(3):703-18. PubMed PMID: 15541891.
38-Amargos-Bosch M, Bortolozzi A, Puig MV, Serrats J, Adell A, Celada P, et al. Co-expression and in vivo interaction of serotonin1A and serotonin2A receptors in pyramidal neurons of prefrontal cortex. Cerebral cortex. 2004:281-99. PubMed PMID: 14754868.
39-Quinlan MG, Almey A, Caissie M, LaChappelle I, Radiotis G, Brake WG. Estradiol and striatal dopamine receptor antagonism influence memory system bias in the female rat. Neurobiology of learning and memory. 2013:221-9. PubMed PMID: 24036396.
40-Penalva RG, Lancel M, Flachskamm C, Reul JM, Holsboer F, Linthorst AC. Effect of sleep and sleep deprivation on serotonergic neurotransmission in the hippocampus: a combined in vivo microdialysis/EEG study in rats. The European journal of neuroscience. 2003:1896-906. PubMed PMID: 12752789.
41-Bjorvatn B, Gronli J, Hamre F, Sorensen E, Fiske E, Bjorkum AA, et al. Effects of sleep deprivation on extracellular serotonin in hippocampus and frontal cortex of the rat. Neuroscience. 2002;113(2):323-30. PubMed PMID: 12127089.
42-Kim EY, Mahmoud GS, Grover LM. REM sleep deprivation inhibits LTP in vivo in area CA1 of rat hippocampus. Neuroscience letters. 2005:163-7. PubMed PMID: 16039776.
43-Lopez-Rodriguez F, Wilson CL, Maidment NT, Poland RE, Engel J. Total sleep deprivation increases extracellular serotonin in the rat hippocampus. Neuroscience. 2003;121(2):523-30. PubMed PMID: 14522011.
44-Pehrson AL, Sanchez C. Serotonergic modulation of glutamate neurotransmission as a strategy for treating depression and cognitive dysfunction. CNS spectrums. 2014:121-33. PubMed PMID: 23903233. Pubmed Central PMCID: 3968911.
45-Gottlieb JP, Keller A. Intrinsic circuitry and physiological properties of pyramidal neurons in rat barrel cortex. Experimental brain research. 1997 Jun;115(1):47-60. PubMed PMID: 9224833.
46-Celada P, Puig MV, Artigas F. Serotonin modulation of cortical neurons and networks. Frontiers in integrative neuroscience. 2013;7-25. PubMed PMID: 23626526. Pubmed Central PMCID: 3630391.
47-Paxinos G., Watson,C., The  rat  brain in stereotaxic coordinates. ( 6th ed )2007, London, UK: Academic Press.
 
 
 
Jundishapur Scientific Medical Journal
Volume 17, Issue 1 - Serial Number 112
March and April 2018
Pages 21-36

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History

  • Receive Date: 18 October 2017
  • Revise Date: 13 December 2017
  • Accept Date: 23 January 2018

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