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Quetiapine improves sensorimotor gating deficit in a sleep deprivation-induced rat model

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Abstract

Background

Sleep deprivation (SD) impairs pre-stimulus inhibition, but the effect of quetiapine (QET) remains largely unknown.

Objective

This study aimed to investigate the behavioral and cognitive effects of QET in both naïve and sleep-deprived rats.

Materials and methods

Seven groups (n = 49) of male Wistar Albino rats were used in this study. SD was performed using the modified multiple platform technique in a water tank for 72 h. Our study consists of two experiments investigating the effect of QET on pre-pulse inhibition (PPI) of the acoustic startle reflex. The first experiment tested the effect of short- and long-term administration of QET on PPI response in non-sleeping (NSD) rats. The second experiment used 72 h REM sleep deprivation as a model for SD-induced impairment of the PPI response. Here, we tested the effect of QET on the % PPI of SD rats by short- and long-term intraperitoneal injection at the last 90 min of sleep SD and immediately subsequently tested for PPI.

Results

72 h SD impaired PPI, reduced startle amplitude, and attenuated the PPI% at + 4 dB, + 8 dB, and + 16 dB prepulse intensities. 10 mg/kg short and long-term QET administration completely improved sensorimotor gating deficit, increased startle amplitude, and restored the impaired PPI% at + 4 dB, + 8 dB, and + 16 dB after 72 h SD in rats.

Conclusion

Our results showed short- and long-term administration of QET improved sensorimotor gating deficit in 72 h SD. Further research is required for the etiology of insomnia and the dose-related behavioral effects of QET.

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References

  1. Sprecher KE, Ferrarelli F, Benca RM. Sleep and plasticity in schizophrenia. Curr Top Behav Neurosci. 2015;25:433–58. https://doi.org/10.1007/7854_2014_366.

    Article  PubMed  PubMed Central  Google Scholar 

  2. Waters F, Chiu V, Atkinson A, Blom JD. Severe sleep deprivation causes hallucinations and a gradual progression toward psychosis with increasing time awake. Front Psychiatry. 2018;10(9):303. https://doi.org/10.3389/fpsyt.2018.00303.

    Article  Google Scholar 

  3. Davies G, Haddock G, Yung AR, Mulligan LD, Kyle SD. A systematic review of the nature and correlates of sleep disturbance in early psychosis. Sleep Med Rev. 2017;31:25–38. https://doi.org/10.1016/j.smrv.2016.01.001.

    Article  PubMed  Google Scholar 

  4. Malik V, Parthasarathy S. Sleep in intensive care units. Curr Respir Care Reports. 2014;3(2):35–41. https://doi.org/10.1007/s13665-014-0077-1.

    Article  Google Scholar 

  5. Owens J, Gruber R, Brown T, Corkum P, Cortese S, O’Brien L, Stein M, Weiss M. Future research directions in sleep and ADHD: report of a consensus working group. J Atten Disord. 2013;17(7):550–64. https://doi.org/10.1177/1087054712457992.

    Article  PubMed  Google Scholar 

  6. Pisani MA, Friese RS, Gehlbach BK, Schwab RJ, Weinhouse GL, Jones SF. Sleep in the intensive care unit. Am J Respir Crit Care Med. 2015;191(7):731–8. https://doi.org/10.1164/rccm.201411-2099CI.

    Article  PubMed  PubMed Central  Google Scholar 

  7. Brisch R, Saniotis A, Wolf R, Bielau H, Bernstein HG, Steiner J, Bogerts B, Braun K, Jankowski Z, Kumaratilake J, Henneberg M, Gos T. The role of dopamine in schizophrenia from a neurobiological and evolutionary perspective: old fashioned, but still in vogue. Front Psychiatry. 2014;19(5):47. https://doi.org/10.3389/fpsyt.2014.00047.

    Article  Google Scholar 

  8. Kim SA. 5-HT1A and 5-HT2A signaling, desensitization, and downregulation: serotonergic dysfunction and abnormal receptor density in schizophrenia and the prodrome. Cureus. 2021;13(6): e15811. https://doi.org/10.7759/cureus.15811.

    Article  PubMed  PubMed Central  Google Scholar 

  9. Elmenhorst D, Kroll T, Matusch A, Bauer A. Sleep deprivation increases cerebral serotonin 2A receptor binding in humans. Sleep. 2012;35(12):1615–23. https://doi.org/10.5665/sleep.2230.

    Article  PubMed  PubMed Central  Google Scholar 

  10. Herrero JL, Roberts MJ, Delicato LS, Gieselmann MA, Dayan P, Thiele A. Acetylcholine contributes through muscarinic receptors to attentional modulation in V1. Nature. 2008;454(7208):1110–4. https://doi.org/10.1038/nature07141.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Zant JC, Leenaars CHC, Kostin A, Van Someren EJW, Porkka-Heiskanen T. Increases in extracellular serotonin and dopamine metabolite levels in the basal forebrain during sleep deprivation. Brain Res. 2011;1399:40–8. https://doi.org/10.1016/j.brainres.2011.05.008.

    Article  CAS  PubMed  Google Scholar 

  12. Wang X, Wang Z, Cao J, Dong Y, Chen Y. Melatonin alleviates acute sleep deprivation-induced memory loss in mice by suppressing hippocampal ferroptosis. Front Pharmacol. 2021;16(12): 708645. https://doi.org/10.3389/fphar.2021.708645.

    Article  CAS  Google Scholar 

  13. Benedict C, Brooks SJ, O’Daly OG, Almèn MS, Morell A, Åberg K, Gingnell M, Schultes B, Hallschmid M, Broman JE, Larsson EM, Schiöth HB. Acute sleep deprivation enhances the brain’s response to hedonic food stimuli: an fMRI study. J Clin Endocrinol Metab. 2012;97(3):E443–7. https://doi.org/10.1210/jc.2011-2759.

    Article  CAS  PubMed  Google Scholar 

  14. Eggers AE. A serotonin hypothesis of schizophrenia. Med Hypotheses. 2013;80(6):791–4. https://doi.org/10.1016/j.mehy.2013.03.013.

    Article  CAS  PubMed  Google Scholar 

  15. Sumiyoshi T, Kunugi H, Nakagome K. Serotonin and dopamine receptors in motivational and cognitive disturbances of schizophrenia. Front Neurosci. 2014;4(8):395. https://doi.org/10.3389/fnins.2014.00395.

    Article  Google Scholar 

  16. World Health Organization. International classification of diseases 10th revision (ICD-10). Geneva: World Health Organization; 1994.

    Google Scholar 

  17. American Psychiatric Association (APA). Diagnostic and statistical manual of mental disorder. 5th ed. Arlington, VA: American Psychiatric Publishing; 2013.

    Book  Google Scholar 

  18. Iqbal Y, Connell C, Worthington M, Elrafei H, Mulvaney CA, Kaewchaluay C. Quetiapine dose for people with schizophrenia. Cochrane Database Syst Rev. 2019;2019(7):CD013372. https://doi.org/10.1002/14651858.CD013372.

    Article  PubMed Central  Google Scholar 

  19. KivircikAkdede BB, Alptekin K, Kitiş A, Arkar H, Akvardar Y. Effects of quetiapine on cognitive functions in schizophrenia. Prog Neuropsychopharmacol Biol Psychiatry. 2005;29(2):233–8. https://doi.org/10.1016/j.pnpbp.2004.11.005.

    Article  CAS  Google Scholar 

  20. Li P, Snyder GL, Vanover KE. Dopamine targeting drugs for the treatment of schizophrenia: past, present and future. Curr Top Med Chem. 2016;16(29):3385–403. https://doi.org/10.2174/1568026616666160608084834.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Björkholm C, Jardemark K, Marcus MM, Malmerfelt A, Nyberg S, Schilström B, Svensson TH. Role of concomitant inhibition of the norepinephrine transporter for the antipsychotic effect of quetiapine. Eur Neuropsychopharmacol. 2013;23(7):709–20. https://doi.org/10.1016/j.euroneuro.2012.05.012.

    Article  CAS  PubMed  Google Scholar 

  22. López-Muñoz F, Alamo C. Active metabolites as antidepressant drugs: the role of norquetiapine in the mechanism of action of quetiapine in the treatment of mood disorders. Front Psychiatry. 2013;12(4):102. https://doi.org/10.3389/fpsyt.2013.00102.

    Article  Google Scholar 

  23. Pergola G, Selvaggi P, Trizio S, Bertolino A, Blasi G. The role of the thalamus in schizophrenia from a neuroimaging perspective. Neurosci Biobehav Rev. 2015;54:57–75. https://doi.org/10.1016/j.neubiorev.2015.01.013.

    Article  PubMed  Google Scholar 

  24. Khan MA, Al-Jahdali H. The consequences of sleep deprivation on cognitive performance. Neurosciences (Riyadh). 2023;28(2):91–9. https://doi.org/10.17712/nsj.2023.2.20220108.

    Article  PubMed  Google Scholar 

  25. Sherman SM, Guillery RW. Distinct functions for direct and transthalamic corticocortical connections. J Neurophysiol. 2011;106(3):1068–77. https://doi.org/10.1152/jn.00429.2011.

    Article  PubMed  Google Scholar 

  26. Swerdlow NR, Weber M, Qu Y, Light GA, Braff DL. Realistic expectations of prepulse inhibition in translational models for schizophrenia research. Psychopharmacology. 2008;199(3):331–88. https://doi.org/10.1007/s00213-008-1072-4.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Mena A, Ruiz-Salas JC, Puentes A, Dorado I, Ruiz-Veguilla M, De la Casa LG. Reduced prepulse inhibition as a biomarker of schizophrenia. Front Behav Neurosci. 2016;18(10):202. https://doi.org/10.3389/fnbeh.2016.00202.

    Article  Google Scholar 

  28. Carli M, Invernizzi RW. Serotoninergic and dopaminergic modulation of cortico-striatal circuit in executive and attention deficits induced by NMDA receptor hypofunction in the 5-choice serial reaction time task. Front Neural Circuits. 2014;11(8):58. https://doi.org/10.3389/fncir.2014.00058.

    Article  CAS  Google Scholar 

  29. Liu YP, Tung CS, Chuang CH, Lo SM, Ku YC. Tail-pinch stress and REM sleep deprivation differentially affect sensorimotor gating function in modafinil-treated rats. Behav Brain Res. 2011;219:98–104. https://doi.org/10.1016/j.bbr.2010.12.012.

    Article  PubMed  Google Scholar 

  30. Frau R, Orrù M, Puligheddu M, Gessa GL, Mereu G, Marrosu F, Bortolato M. Sleep deprivation disrupts prepulse inhibition of the startle reflex: reversal by antipsychotic drugs. Int J Neuropsychopharmacol. 2008;11(7):947–55. https://doi.org/10.1017/S1461145708008900.

    Article  CAS  PubMed  Google Scholar 

  31. Machado RB, Hipólide DC, Benedito-Silva AA, Tufik S. Sleep deprivation induced by the modified multiple platform technique: quantification of sleep loss and recovery. Brain Res. 2004;1004(1–2):45–51. https://doi.org/10.1016/j.brainres.2004.01.019.

    Article  CAS  PubMed  Google Scholar 

  32. Uzbay T, Kayir H, Goktalay G, Yildirim M. Agmatine disrupts prepulse inhibition of acoustic startle reflex in rats. J Psychopharmacol. 2010;24(6):923–9. https://doi.org/10.1177/0269881109102533.

    Article  CAS  PubMed  Google Scholar 

  33. Öz P, Gökalp HK, Göver T, Uzbay T. Dose-dependent and opposite effects of orexin A on prepulse inhibition response in sleep-deprived and non-sleep-deprived rats. Behav Brain Res. 2018;2(346):73–9. https://doi.org/10.1016/j.bbr.2017.12.002.

    Article  CAS  Google Scholar 

  34. Kaya-Yertutanol FD, Uzbay İT, Çevreli B, et al. Effect of gabapentin on sleep-deprivation-induced disruption of prepulse inhibition. Psychopharmacology. 2020;237:2993–3006. https://doi.org/10.1007/s00213-020-05587-9.

    Article  CAS  PubMed  Google Scholar 

  35. Tekin M, Kaya-Yertutanol FD, Çevreli B, Özdoğru AA, Kulaksız H, Uzbay İT. Sodium valproate improves sensorimotor gating deficit induced by sleep deprivation at low doses. Turk J Med Sci. 2021;51(3):1521–30. https://doi.org/10.3906/sag-2011-229.

    Article  CAS  PubMed  Google Scholar 

  36. Zubedat S, Freed Y, Eshed Y, Cymerblit-Sabba A, Ritter A, Nachmani M, Harush R, Aga-Mizrachi S, Avital A. Plant-derived nanoparticle treatment with cocc 30c ameliorates attention and motor abilities in sleep-deprived rats. Neuroscience. 2013;3(253):1–8. https://doi.org/10.1016/j.neuroscience.2013.08.021.

    Article  CAS  Google Scholar 

  37. Gründer G, Heinze M, Cordes J, Mühlbauer B, Juckel G, Schulz C, Rüther E, Timm J, NeSSy Study Group. Effects of first-generation antipsychotics versus second-generation antipsychotics on quality of life in schizophrenia: a double-blind, randomised study. Lancet Psychiatry. 2016;3(8):717–29. https://doi.org/10.1016/S2215-0366(16)00085-7.

    Article  PubMed  Google Scholar 

  38. Powell SB, Young JW, Ong JC, Caron MG, Geyer MA. Atypical antipsychotics clozapine and quetiapine attenuate prepulse inhibition deficits in dopamine transporter knockout mice. Behav Pharmacol. 2008;19(5–6):562–5. https://doi.org/10.1097/FBP.0b013e32830dc110.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. He J, Zu Q, Wen C, Liu Q, You P, Li X, Wang W. Quetiapine attenuates schizophrenia-like behaviors and demyelination in a MK-801-induced mouse model of schizophrenia. Front Psychiatry. 2020;19(11):843. https://doi.org/10.3389/fpsyt.2020.00843.

    Article  Google Scholar 

  40. Chamera K, Curzytek K, Kamińska K, Trojan E, Basta-Kaim A. Quetiapine ameliorates MIA-induced impairment of sensorimotor gating: focus on neuron-microglia communication and the inflammatory response in the frontal cortex of adult offspring of Wistar rats. Cells. 2022;11(18):2788. https://doi.org/10.3390/cells11182788.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Tanibuchi Y, Fujita Y, Horio M, Iyo M, Hashimoto K. Effects of quetiapine on dizocilpine-induced prepulse inhibition deficits in mice possible role of the aα1 adrenergic receptor. Clin Psychopharmacol Neurosci. 2010;8(3):133–6.

    CAS  Google Scholar 

  42. Duncan GE, Moy SS, Lieberman JA, Koller BH. Effects of haloperidol, clozapine, and quetiapine on sensorimotor gating in a genetic model of reduced NMDA receptor function. Psychopharmacology. 2006;184(2):190–200. https://doi.org/10.1007/s00213-005-0214-1.

    Article  CAS  PubMed  Google Scholar 

  43. Li M, He E, Volf N. Time course of the attenuation effect of repeated antipsychotic treatment on prepulse inhibition disruption induced by repeated phencyclidine treatment. Pharmacol Biochem Behav. 2011;98(4):559–69. https://doi.org/10.1016/j.pbb.2011.03.007.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Shoemaker JM, Pitcher L, Noh HR, Swerdlow NR. Quetiapine produces a prolonged reversal of the sensorimotor gating-disruptive effects of basolateral amygdala lesions in rats. Behav Neurosci. 2003;117(1):136–43. https://doi.org/10.1037//0735-7044.117.1.136.

    Article  CAS  PubMed  Google Scholar 

  45. Auclair AL, Galinier A, Besnard J, Newman-Tancredi A, Depoortère R. Putative antipsychotics with pronounced agonism at serotonin 5-HT1A and partial agonist activity at dopamine D2 receptors disrupt basal PPI of the startle reflex in rats. Psychopharmacology. 2007;193(1):45–54. https://doi.org/10.1007/s00213-007-0762-7.

    Article  CAS  PubMed  Google Scholar 

  46. Molina V, López DE, Villa R, Pérez J, Martín C, Ballesteros A, Cardoso A, Sancho C. Prepulse inhibition of the startle reflex in schizophrenia remains stable with short-term quetiapine. Eur Psychiatry. 2011;26(5):271–5. https://doi.org/10.1016/j.eurpsy.2010.03.002.

    Article  CAS  PubMed  Google Scholar 

  47. Aggernaes B, Glenthoj BY, Ebdrup BH, Rasmussen H, Lublin H, Oranje B. Sensorimotor gating and habituation in antipsychotic-naive, first-episode schizophrenia patients before and after 6 months’ treatment with quetiapine. Int J Neuropsychopharmacol. 2010;13(10):1383–95. https://doi.org/10.1017/S1461145710000787.

    Article  CAS  PubMed  Google Scholar 

  48. Geyer MA, Krebs-Thomson K, Braff DL, Swerdlow NR. Pharmacological studies of prepulse inhibition models of sensorimotor gating deficits in schizophrenia: a decade in review. Psychopharmacology. 2001;156(2–3):117–54. https://doi.org/10.1007/s002130100811.

    Article  CAS  PubMed  Google Scholar 

  49. Nair AB, Jacob S. A simple practice guide for dose conversion between animals and human. J Basic Clin Pharm. 2016;7(2):27–31. https://doi.org/10.4103/0976-0105.177703.

    Article  PubMed  PubMed Central  Google Scholar 

  50. Christie MA, McKenna JT, Connolly NP, McCarley RW, Strecker RE. 24 hours of sleep deprivation in the rat increases sleepiness and decreases vigilance: introduction of the rat-psychomotor vigilance task. J Sleep Res. 2008;17(4):376–84. https://doi.org/10.1111/j.1365-2869.2008.00698.x.

    Article  PubMed  PubMed Central  Google Scholar 

  51. Libourel PA, Corneyllie A, Luppi PH, Chouvet G, Gervasoni D. Unsupervised online classifier in sleep scoring for sleep deprivation studies. Sleep. 2015;38(5):815–28. https://doi.org/10.5665/sleep.4682.

    Article  PubMed  PubMed Central  Google Scholar 

  52. Bhopal N, Khatwa U. Sleep deprivation and human development. In: Bianchi MT, editor. Sleep deprivation and disease: effects on the body, brain and behavior. New York: Springer Science Business Media; 2014. p. 91–9.

    Chapter  Google Scholar 

  53. Claverie D, Becker C, Ghestem A, Coutan M, Camus F, Bernard C, Benoliel JJ, Canini F. Low β2 main peak frequency in the electroencephalogram signs vulnerability to depression. Front Neurosci. 2016;2(10):495. https://doi.org/10.3389/fnins.2016.00495.

    Article  Google Scholar 

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Acknowledgements

The authors dedicated this publication to the 100th anniversary of the Republic of Türkiye. As scientists raised by Türkiye, we are proud of to be citizen of this country.

Funding

Funded by Üsküdar University Scientific Research Projects Unit.

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Authors and Affiliations

  1. Electroneurophysiology, Vocational School of Health Sciences, Üsküdar University, Istanbul, Turkey

    Öznur Özge Özcan

  2. Neuropsychopharmacology Practice and Research Center, Üsküdar University, Istanbul, Turkey

    Burcu Çevreli

  3. Department of Physiology, Faculty of Medicine, Altınbaş University, Istanbul, Turkey

    Arzu Temizyürek

  4. Medical Laboratory Techniques, Vocational School of Health Sciences, Üsküdar University, Mimar Sinan, Selmani Pak, Üsküdar, 34672, Istanbul, Turkey

    Mesut Karahan

  5. Department of Molecular Biology and Genetics, Faculty of Engineering and Natural Sciences, Üsküdar University, Istanbul, Turkey

    Muhsin Konuk

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Corresponding author

Correspondence to Mesut Karahan.

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All authors declare that they have no conflicts of interest.

Ethical approval

All experiments were conducted according to the ethical guidelines in the Guidelines for the Care and Use of Laboratory Animals adopted by the US National Institutes of Health and published in 1996 and OECD guidelines no. 423. All animal experiments were performed with prior permission from the Animal Research Ethics Committee of Üsküdar University, İstanbul, Turkey. This study was approved by the Local Ethic Committee of Uskudar University on February 20.01.2023 the decision number of Ü.Ü-HADYEK 2023–03.

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Özcan, Ö.Ö., Çevreli, B., Temizyürek, A. et al. Quetiapine improves sensorimotor gating deficit in a sleep deprivation-induced rat model. Sleep Biol. Rhythms 22, 269–278 (2024). https://doi.org/10.1007/s41105-023-00504-x

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