Skip to main content
Download PDF

Comparison of scopolamine-induced cognitive impairment responses in three different ICR stocks

Laboratory Animal Research volume 34, pages 317–328 (2018)Cite this article

Abstract

Cognitive impairment responses are important research topics in the study of degenerative brain diseases as well as in understanding of human mental activities. To compare response to scopolamine (SPL)-induced cognitive impairment, we measured altered parameters for learning and memory ability, inflammatory response, oxidative stress, cholinergic dysfunction and neuronal cell damages, in Korl:ICR stock and two commercial breeder stocks (A:ICR and B:ICR) after relevant SPL exposure. In the water maze test, Korl:ICR showed no significant difference in SPL-induced learning and memory impairment compared to the two different ICRs, although escape latency was increased after SPL exposure. Although behavioral assessment using the manual avoidance test revealed reduced latency in all ICR mice after SPL treatment as compared to Vehicle, no differences were observed between the three ICR stocks. To determine cholinergic dysfunction induction by SPL exposure, activity of acetylcholinesterase (AChE) assessed in the three ICR stocks revealed no difference of acetylcholinesterase activity. Furthermore, low levels of superoxide dismutase (SOD) activity and high levels of inflammatory cytokines in SPL-treated group were maintained in all three ICR stocks, although some variations were observed between the SPLtreated groups. Neuronal cell damages induced by SPL showed similar response in all three ICR stocks, as assessed by terminal deoxynucleotidyl transferase dUTP nick end labeling (TUNEL) assay, Nissl staining analysis and expression analyses of apoptosis-related proteins. Thus, the results of this study provide strong evidence that Korl:ICR is similar to the other two ICR. Stocks in response to learning and memory capacity.

References

  1. Brem AK, Ran K, Pascual-Leone A. Learning and memory. Handb Clin Neurol 2013; 116: 693–737.

    Article  PubMed  PubMed Central  Google Scholar 

  2. Okano H, Hirano T, Balaban E. Learning and memory. Proc Natl Acad Sci U S A 2000; 97(23): 12403–12404.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Jewart RD, Green J, Lu CJ, Cellar J, Tune LE. Cognitive, behavioral, and physiological changes in Alzheimer disease patients as a function of incontinence medications. Am J Geriatr Psychiatry 2005; 13(4): 324–328.

    Article  PubMed  Google Scholar 

  4. Anderson LA, McConnell SR. Cognitive health: an emerging public health issue. Alzheimers Dement 2007; 3(2 Suppl): S70–73.

    PubMed  Google Scholar 

  5. Akaike A, Takada-Takatori Y, Kume T, Izumi Y. Mechanisms of neuroprotective effects of nicotine and acetylcholinesterase inhibitors: role of alpha4 and alpha7 receptors in neuroprotection. J Mol Neurosci 2010; 40(1–2): 211–216.

    Article  CAS  PubMed  Google Scholar 

  6. Xu Z, Li H, Jin P. Epigenetics-based therapeutics for neurodegenerative disorders. Curr Transl Geriatr Exp Gerontol Rep 2012; 1(4): 229–236.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Kim DH, Ryu JH. Differential effects of scopolamine on memory processes in the object recognition test and the morris water maze test in Mice. Biomol Ther 2008; 16(3): 173–178.

    Article  CAS  Google Scholar 

  8. Vannucchi MG, Scali C, Kopf SR, Pepeu G, Casamenti F. Selective muscarinic antagonists differentially affect in vivo acetylcholine release and memory performances of young and aged rats. Neuroscience 1997; 79(3): 837–846.

    Article  CAS  PubMed  Google Scholar 

  9. Kwon SH, Lee HK, Kim JA, Hong SI, Kim HC, Jo TH, Park YI, Lee CK, Kim YB, Lee SY, Jang CG. Neuroprotective effects of chlorogenic acid on scopolamine-induced amnesia via antiacetylcholinesterase and anti-oxidative activities in mice. Eur J Pharmacol 2010; 649(1–3): 210–217.

    Article  CAS  PubMed  Google Scholar 

  10. Lee YK, Yuk DY, Kim TI, Kim YH, Kim KT, Kim KH, Lee BJ, Nam SY, Hong JT. Protective effect of the ethanol extract of Magnolia officinalis and 4-O-methylhonokiol on scopolamineinduced memory impairment and the inhibition of acetylcholinesterase activity. J Nat Med 2009; 63(3): 274–282.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Pachauri SD, Tota S, Khandelwal K, Verma PR, Nath C, Hanif K, Shukla R, Saxena JK, Dwivedi AK. Protective effect of fruits of Morinda citrifolia L. on scopolamine induced memory impairment in mice: a behavioral, biochemical and cerebral blood flow study. J Ethnopharmacol 2012; 139(1): 34–41.

    Article  PubMed  Google Scholar 

  12. Tota S, Nath C, Najmi AK, Shukla R, Hanif K. Inhibition of central angiotensin converting enzyme ameliorates scopolamine induced memory impairment in mice: role of cholinergic neurotransmission, cerebral blood flow and brain energy metabolism. Behav Brain Res 2012; 232(1): 66–76.

    Article  CAS  PubMed  Google Scholar 

  13. Tanabe F, Miyasaka N, Kubota T, Aso T. Estrogen and progesterone improve scopolamine-induced impairment of spatial memory. J Med Dent Sci 2004; 51(1): 89–98.

    PubMed  Google Scholar 

  14. Adams B, Fitch T, Chaney S, Gerlai R. Altered performance characteristics in cognitive tasks: comparison of the albino ICR and CD1 mouse strains. Behav Brain Res 2002; 133(2): 351–361.

    Article  PubMed  Google Scholar 

  15. Bouwknecht JA, Paylor R. Behavioral and physiological mouse assays for anxiety: a survey in nine mouse strains. Behav Brain Res 2002; 136(2): 489–501.

    Article  PubMed  Google Scholar 

  16. Brown RE, Wong AA. The influence of visual ability on learning and memory performance in 13 strains of mice. Learn Mem 2007; 14(3):134–144.

    Article  PubMed  PubMed Central  Google Scholar 

  17. Nguyen PV, Abel T, Kandel ER, Bourtchouladze R. Straindependent differences in LTP and hippocampus-dependent memory in inbred mice. Learn Mem 2000; 7(3): 170–179.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Buæan M, Abel T. The mouse: genetics meets behaviour. Nat Rev Genet 2002; 3(2): 114–123.

    Google Scholar 

  19. Song SH, Choi SM, Kim JE, Sung JE, Lee HA, Choi YH, Bae CJ, Choi YW, Hwang DY. α-Isocubebenol alleviates scopolamineinduced cognitive impairment by repressing acetylcholinesterase activity. Neurosci Lett 2017; 638: 121–128.

    Article  CAS  PubMed  Google Scholar 

  20. Morris R. Developments of a water-maze procedure for studying spatial learning in the rat. J Neurosci Methods 1984; 11(1): 47–60.

    Article  CAS  PubMed  Google Scholar 

  21. Kim MJ, Choi SJ, Lim ST, Kim HK, Kim YJ, Yoon HG, Shin DH. Zeatin supplement improves scopolamine-induced memory impairment in mice. Biosci Biotechnol Biochem 2008; 72(2): 577–581.

    Article  CAS  PubMed  Google Scholar 

  22. LeDoux JE. Emotional memory: in search of systems and synapses. Ann N Y Acad Sci 1993; 702: 149–157.

    Article  CAS  PubMed  Google Scholar 

  23. Prajapati KD, Sharma SS, Roy N. Upregulation of albumin expression in focal ischemic rat brain. Brain Res 2010; 1327:118–124.

    Article  CAS  PubMed  Google Scholar 

  24. Ooigawa H, Nawashiro H, Fukui S, Otani N, Osumi A, Toyooka T, Shima K. The fate of Nissl-stained dark neurons following traumatic brain injury in rats: difference between neocortex and hippocampus regarding survival rate. Acta Neuropathol 2006; 112(4): 471–481.

    Article  CAS  PubMed  Google Scholar 

  25. Balaban H, Nazýroðlu M, Demirci K, Övey ÝS. The protective role of selenium on scopolamine-induced memory impairment, oxidative stress, and apoptosis in aged rats: the involvement of TRPM2 and TRPV1 channels. Mol Neurobiol 2017; 54(4): 2852–2868.

    Article  CAS  PubMed  Google Scholar 

  26. Wong-Guerra M, Jiménez-Martin J, Pardo-Andreu GL, Fonseca-Fonseca LA, Souza DO, de Assis AM, Ramirez-Sanchez J, Del Valle RM, Nuñez-Figueredo Y. Mitochondrial involvement in memory impairment induced by scopolamine in rats. Neurol Res 2017; 39(7): 649–659.

    Article  CAS  PubMed  Google Scholar 

  27. Gella A, Durany N. Oxidative stress in Alzheimer disease. Cell Adh Migr 2009; 3(1): 88–93.

    Article  PubMed  PubMed Central  Google Scholar 

  28. Marcus DL, Thomas C, Rodriguez C, Simberkoff K, Tsai JS, Strafaci JA, Freedman ML. Increased peroxidation and reduced antioxidant enzyme activity in Alzheimer’s disease. Exp Neurol 1998; 150(1): 40–44.

    Article  CAS  PubMed  Google Scholar 

  29. Perry G, Cash AD, Smith MA. Alzheimer disease and oxidative stress. J Biomed Biotechnol 2002; 2(3): 120–123.

    Article  PubMed  PubMed Central  Google Scholar 

  30. Smith MA, Rottkamp CA, Nunomura A, Raina AK, Perry G. Oxidative stress in Alzheimer’s disease. Biochim Biophys Acta 2000; 1502(1): 139–144.

    Article  CAS  PubMed  Google Scholar 

  31. Balu M, Sangeetha P, Haripriya D, Panneerselvam C. Rejuvenation of antioxidant system in central nervous system of aged rats by grape seed extract. Neurosci Lett 2005; 383(3): 295–300.

    Article  CAS  PubMed  Google Scholar 

  32. Mann H, McCoy MT, Subramaniam J, Van Remmen H, Cadet JL. Overexpression of superoxide dismutase and catalase in immortalized neural cells: toxic effects of hydrogen peroxide. Brain Res 1997; 770(1–2): 163–168.

    Article  CAS  PubMed  Google Scholar 

  33. Jain NK, Patil CS, Kulkarni SK, Singh A. Modulatory role of cyclooxygenase inhibitors in aging- and scopolamine or lipopolysaccharide-induced cognitive dysfunction in mice. Behav Brain Res 2002; 133(2): 369–376.

    Article  CAS  PubMed  Google Scholar 

  34. Lee B, Shim I, Lee H, Hahm DH. Rehmannia glutinosa ameliorates scopolamine-induced learning and memory impairment in rats. J Microbiol Biotechnol 2011; 21(8): 874–883.

    Article  PubMed  Google Scholar 

  35. Choi DY, Lee YJ, Lee SY, Lee YM, Lee HH, Choi IS, Oh KW, Han SB, Nam SY, Hong JT. Attenuation of scopolamine-induced cognitive dysfunction by obovatol. Arch Pharm Res 2012; 35(7): 1279–1286.

    Article  CAS  PubMed  Google Scholar 

  36. Liskowsky W, Schliebs R. Muscarinic acetylcholine receptor inhibition in transgenic Alzheimer-like Tg2576 mice by scopolamine favours the amyloidogenic route of processing of amyloid precursor protein. Int J Dev Neurosci 2006; 24(2–3): 149–156.

    Article  CAS  PubMed  Google Scholar 

  37. Gattu M, Boss KL, Terry AV Jr, Buccafusco JJ. Reversal of scopolamine-induced deficits in navigational memory performance by the seed oil of Celastrus paniculatus. Pharmacol Biochem Behav 1997; 57(4): 793–799.

    Article  CAS  PubMed  Google Scholar 

  38. Crawley JN, Belknap JK, Collins A, Crabbe JC, Frankel W, Henderson N, Hitzemann RJ, Maxson SC, Miner LL, Silva AJ, Wehner JM, Wynshaw-Boris A, Paylor R. Behavioral phenotypes of inbred mouse strains: implications and recommendations for molecular studies. Psychopharmacology (Berl) 1997; 132(2): 107–124.

    Article  CAS  Google Scholar 

  39. Yoneoka Y, Satoh M, Akiyama K, Sano K, Fujii Y, Tanaka R. An experimental study of radiation-induced cognitive dysfunction in an adult rat model. Br J Radiol 1999; 72(864): 1196–1201.

    Article  CAS  PubMed  Google Scholar 

  40. Beninger RJ, Jhamandas K, Boegman RJ, el-Defrawy SR. Effects of scopolamine and unilateral lesions of the basal forebrain on Tmaze spatial discrimination and alternation in rats. Pharmacol Biochem Behav 1986; 24(5): 1353–1360.

    Article  CAS  PubMed  Google Scholar 

  41. Carballo-Márquez A, Vale-Martínez A, Guillazo-Blanch G, Torras-Garcia M, Boix-Trelis N, Martí-Nicolovius M. Differential effects of muscarinic receptor blockade in prelimbic cortex on acquisition and memory formation of an odor-reward task. Learn Mem 2007; 14(9): 616–624.

    Article  PubMed  PubMed Central  Google Scholar 

  42. Halder S, Mehta AK, Kar R, Mustafa M, Mediratta PK, Sharma KK. Clove oil reverses learning and memory deficits in scopolamine-treated mice. Planta Med 2011; 77(8): 830–834.

    Article  CAS  PubMed  Google Scholar 

  43. Chen KC, Baxter MG, Rodefer JS. Central blockade of muscarinic cholinergic receptors disrupts affective and attentional set-shifting. Eur J Neurosci 2004; 20(4): 1081–1088.

    Article  PubMed  Google Scholar 

  44. Liem-Moolenaar M, de Boer P, Timmers M, Schoemaker RC, van Hasselt JG, Schmidt S, van Gerven JM. Pharmacokineticpharmacodynamic relationships of central nervous system effects of scopolamine in healthy subjects. Br J Clin Pharmacol 2011; 71(6): 886–898.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Hosseini-Sharifabad A, Mohammadi-Eraghi S, Tabrizian K, Soodi M, Khorshidahmad T, Naghdi N, Abdollahi M, Beyer C, Roghani A, Sharifzadeh M. Effects of training in the Morris water maze on the spatial learning acquisition and VAChT expression in male rats. Daru 2011; 19(2): 166–172.

    CAS  PubMed  PubMed Central  Google Scholar 

  46. Lamberty Y, Gower AJ. Cholinergic modulation of spatial learning in mice in a Morris-type water maze. Arch Int Pharmacodyn Ther 1991; 309: 5–19.

    CAS  PubMed  Google Scholar 

  47. Kim JS, Yang MY, Son YH, Kim SH, Kim JC, Kim SJ, Lee YD, Shin TK, Moon CJ. Strain-dependent differences of locomotor activity and hippocampus-dependent learning and memory in mice. Toxicol Res 2008; 24(3): 183–188.

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Author notes

  1. These authors contributed equally to this work

Authors and Affiliations

  1. Department of Biomaterials Science, College of Natural Resources & Life Science, Pusan National University, 1268-50 Cheonghakro, Samnangjin-eup, Miryang, Gyeongnam, 50463, Korea

    Woo Bin Yoon, Hyeon Jun Choi, Ji Eun Kim, Ji Won Park, Mi Ju Kang, Su Ji Bae, Young Ju Lee, You Sang Choi & Dae Youn Hwang

  2. College of Veterinary Medicine, Kyungpook National University, Daegu, Korea

    Kil Soo Kim

  3. College of Pharmacy, Pusan National University, Busan, Korea

    Young-Suk Jung

  4. Exercise Biochemistry Laboratory, Korea National Sport University, Seoul, Korea

    Joon-Yong Cho

  5. Biomedical Science Institute, Changwon National University, 20 Changwondaero, Uichanggu, Changwon, Gyeongnam, 51140, Korea

    Hyun Keun Song

Authors
  1. Woo Bin Yoon
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Hyeon Jun Choi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ji Eun Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ji Won Park
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Mi Ju Kang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Su Ji Bae
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Young Ju Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. You Sang Choi
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Kil Soo Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Young-Suk Jung
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Joon-Yong Cho
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Dae Youn Hwang
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Hyun Keun Song
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Dae Youn Hwang or Hyun Keun Song.

Rights and permissions

This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (https://doi.org/creativecommons.org/licenses/by-nc/3.0) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yoon, W.B., Choi, H.J., Kim, J.E. et al. Comparison of scopolamine-induced cognitive impairment responses in three different ICR stocks. Lab Anim Res 34, 317–328 (2018). https://doi.org/10.5625/lar.2018.34.4.317

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.5625/lar.2018.34.4.317

Keywords

Laboratory Animal Research

ISSN: 2233-7660