Animal cells and systems

The Korean Society for Integrative Biology (한국통합생물학회)
권호 표지
DOI QR코드

DOI QR Code

Anxiolytic effects of an acetylcholinesterase inhibitor, physostigmine, in the adult zebrafish

  • Received : 2011.04.29
  • Accepted : 2011.11.15
  • Published : 2012.06.30
Download PDF
⟨ Previous Next ⟩

Abstract

Anxiety in zebrafish can be determined by examining their bottom-dwelling and light-avoidance behavior. This study determines the effects of physostigmine and scopolamine on anxiety in zebrafish by measuring swimming frequency for three horizontal layers and three vertical columns of a water test tank illuminated by a light source located above the central surface of the tank. In the 1 h session, zebrafish in the control group preferred the bottom layer the most and the center column the least. Zebrafish treated with 2-20 ${\mu}M$ physostigmine were more likely to prefer the to layer than controls, and there were significant pairwise differences between physostigmine-treated zebrafish and controls, indicating the anxiolytic effect of physostigmine. Further, 10 and $20{\mu}M$ physostigmine-treated zebrafish no longer avoided the center column. Scopolamine had no anxiolytic effect on bottom-dwelling and light-avoidance behaviors but suppressed the anxiolytic effect of physostigmine. In terms of their preference for various zones formed by layers and columns, zebrafish in the control group preferred the bottom left and right zones the most. Physostigmine had a positive effect on the preference for the top center zone, which was suppressed by scopolamine pretreatment. The results suggest that the level of anxiety in zebrafish can be reduced by activating acetylcholinergic neurotransmitter systems, which is mediated in part by muscarinic receptors.

Keywords

References

  1. Auld DS, Kornecook TJ, Bastianetto S, Quirion R. 2002. Alzheimer's disease and the basal forebrain cholinergic system: Relations to beta-amyloid peptides, cognition, and treatment strategies. Prog Neurobiol. 68:209-245. https://doi.org/10.1016/S0301-0082(02)00079-5
  2. Bencan Z, Levin ED. 2008. The role of alpha7 and alpha4beta2 nicotinic receptors in the nicotine-induced anxiolytic effect in zebrafish. Physiol Behav. 95:408-412. https://doi.org/10.1016/j.physbeh.2008.07.009
  3. Benetti F, Mello PB, Bonini JS, Monteiro S, Cammarota M, Izquierdo I. 2009. Early postnatal maternal deprivation in rats induces memory deficits in adult life that can be reversed by donepezil and galantamine. Int J Dev Neurosci. 27:59-64. https://doi.org/10.1016/j.ijdevneu.2008.09.200
  4. Cachat J, Stewart A, Grossman L, Gaikwad S, Kadri F, Chung KM, Wu N, Wong K, Roy S, Suciu C, et al. 2010. Measuring behavioral and endocrine responses to novelty stress in adult zebrafish. Nat Protoc. 5:1786-1799. https://doi.org/10.1038/nprot.2010.140
  5. Champagne DL, Hoefnagels CC, de Kloet RE, Richardson MK. 2010. Translating rodent behavioral repertoire to zebrafish (Danio rerio): Relevance for stress research. Behav Brain Res. 214:332-342. https://doi.org/10.1016/j.bbr.2010.06.001
  6. Choi YS, Lee CJ, Kim YH. 2011. MK-801-induced learning impairments reversed by physostigmine and nicotine in zebrafish. Anim Cells Syst. doi:10.1080/19768354.2011.555124.
  7. Clemente D, Porteros A, Weruaga E, Alonso JR, Arenzana FJ, Aijon J, Arevalo R. 2004. Cholinergic elements in the zebrafish central nervous system: Histochemical and immunohistochemical analysis. J Comp Neurol. 474: 75-107. https://doi.org/10.1002/cne.20111
  8. Dong H, Csernansky CA, Martin MV, Bertchume A, Vallera D, Csernansky JG. 2005. Acetylcholinesterase inhibitors ameliorate behavioral deficits in the Tg2576 mouse model of Alzheimer's disease. Psychopharmacology (Berl) 181:145-152. https://doi.org/10.1007/s00213-005-2230-6
  9. Gerlai R. 2010. Zebrafish antipredatory responses: A future for translational research? Behav Brain Res. 207:223-231. https://doi.org/10.1016/j.bbr.2009.10.008
  10. Gerlai R, Lahav M, Guo S, Rosenthal A. 2000. Drinks like a fish: Zebra fish (Danio rerio) as a behavior genetic model to study alcohol effects. Pharmacol Biochem Behav. 67:773-782. https://doi.org/10.1016/S0091-3057(00)00422-6
  11. Kim YH, Lee Y, Kim D, Jung MW, Lee CJ. 2010. Scopolamine-induced learning impairment reversed by physostigmine in zebrafish. Neurosci Res. 67:156-161. https://doi.org/10.1016/j.neures.2010.03.003
  12. Levin ED, Bencan Z, Cerutti DT. 2007. Anxiolytic effects of nicotine in zebrafish. Physiol Behav. 90:54-58. https://doi.org/10.1016/j.physbeh.2006.08.026
  13. Lopez-Patino MA, Yu L, Cabral H, Zhdanova IV. 2008. Anxiogenic effects of cocaine withdrawal in zebrafish. Physiol Behav. 93:160-171. https://doi.org/10.1016/j.physbeh.2007.08.013
  14. Maximino C, de Brito TM, Colmanetti R, Pontes AA, de Castro HM, de Lacerda RI, Morato S, Gouveia A. Jr 2010a. Parametric analyses of anxiety in zebrafish scototaxis. Behav Brain Res. 210:1-7. https://doi.org/10.1016/j.bbr.2010.01.031
  15. Maximino C, Marques de Brito T, Dias CA, Gouveia A. Jr, Morato S. 2010b. Scototaxis as anxiety-like behavior in fish. Nat Protoc. 5:209-216. https://doi.org/10.1038/nprot.2009.225
  16. Park E, Lee Y, Kim Y, Lee CJ. 2008. Cholinergic modulation of neural activity in the telencephalon of the zebrafish. Neurosci Lett. 439:79-83. https://doi.org/10.1016/j.neulet.2008.04.064
  17. Pepeu G, Giovannini MG. 2009. Cholinesterase inhibitors and beyond. Curr Alzheimer Res. 6:86-96. https://doi.org/10.2174/156720509787602861
  18. Schliebs R. 2005. Basal forebrain cholinergic dysfunction in Alzheimer's disease - interrelationship with beta-amyloid, inflammation and neurotrophin signaling. Neurochem Res. 30:895-908. https://doi.org/10.1007/s11064-005-6962-9
  19. Sienkiewicz-Jarosz H, Czlonkowska AI, Siemiatkowski M, Maciejak P, Szyndler J, Plaznik A. 2000. The effects of physostigmine and cholinergic receptor ligands on novelty- induced neophobia. J Neural Transm. 107: 1403-1412. https://doi.org/10.1007/s007020070004
  20. Sienkiewicz-Jarosz H, Maciejak P, Krzascik P, Czlonkowska AI, Szyndler J, Bidzinski A, Kostowski W, Plaznik A. 2003. The effects of central administration of physostigmine in two models of anxiety. Pharmacol Biochem Behav. 75:491-496. https://doi.org/10.1016/S0091-3057(03)00141-2
  21. Smythe JW, Murphy D, Bhatnagar S, Timothy C, Costall B. 1996. Muscarinic antagonists are anxiogenic in rats tested in the black-white box. Pharmacol Biochem Behav. 54:57-63. https://doi.org/10.1016/0091-3057(95)02130-2
  22. Wetzels RB, Zuidema SU, de Jonghe JF, Verhey FR, Koopmans RT. 2010. Course of neuropsychiatric symptoms in residents with dementia in nursing homes over 2-year period. Am J Geriatr Psychiatry. 18:1054-1065. https://doi.org/10.1097/JGP.0b013e3181f60fa1
  23. Wong K, Elegante M, Bartels B, Elkhayat S, Tien D, Roy S, Goodspeed J, Suciu C, Tan J, Grimes C, et al. 2010. Analyzing habituation responses to novelty in zebrafish (Danio rerio). Behav Brain Res. 208:450-457. https://doi.org/10.1016/j.bbr.2009.12.023
  24. Zarrindast MR, Sroushi A, Bananej M, Vousooghi N, Hamidkhaniha S. 2011. Involvement of the dopaminergic receptors of the rat basolateral amygdala in anxiolyticlike effects of the cholinergic system. Eur J Pharmacol. doi:10.1016/j.ejphar.2011.09.168.

Cited by

  1. Non-mammalian models in behavioral neuroscience: consequences for biological psychiatry vol.9, pp.None, 2012, https://doi.org/10.3389/fnbeh.2015.00233
  2. Establishing zebrafish as a model to study the anxiolytic effects of scopolamine vol.7, pp.None, 2012, https://doi.org/10.1038/s41598-017-15374-w
  3. Commentary: Establishing zebrafish as a model to study the anxiolytic effects of scopolamine vol.9, pp.None, 2018, https://doi.org/10.3389/fphar.2018.00293
  4. Emotional behavior in aquatic organisms? Lessons from crayfish and zebrafish vol.98, pp.5, 2012, https://doi.org/10.1002/jnr.24550
  5. An acetylcholinesterase inhibitor, donepezil, increases anxiety and cortisol levels in adult zebrafish vol.34, pp.12, 2020, https://doi.org/10.1177/0269881120944155
  6. Anxiolytic, Promnesic, Anti-Acetylcholinesterase and Antioxidant Effects of Cotinine and 6-Hydroxy-L-Nicotine in Scopolamine-Induced Zebrafish (Danio rerio) Model of Alzheimer’s Disease vol.10, pp.2, 2012, https://doi.org/10.3390/antiox10020212
  7. Baicalein 5,6-Dimethyl Ether Prevents Memory Deficits in the Scopolamine Zebrafish Model by Regulating Cholinergic and Antioxidant Systems vol.10, pp.6, 2012, https://doi.org/10.3390/plants10061245
  8. Clitorienolactones and Isoflavonoids of Clitorea ternatea Roots Alleviate Stress-Like Symptoms in a Reserpine-Induced Zebrafish Model vol.26, pp.14, 2012, https://doi.org/10.3390/molecules26144137