The Tapping Assay: A Simple Method to Induce Fear Responses in Zebrafish
Tóm tắt
The zebrafish is increasingly employed in behavioral neuroscience as a translationally relevant model organism for human central nervous system disorders. One of the most prevalent CNS disorders representing an unmet medical need is the disorder cluster defined under the umbrella term anxiety disorders. Zebrafish have been shown to respond to a variety of anxiety and fear inducing stimuli and have been suggested for modeling human anxiety. Here, we describe a simple method with which we intend to induce fear/anxiety responses in this species. The method allows us to deliver a visual and lateral line stimulus (vibration or “tapping”) to the fish with the use of a moving object, a ball colliding with the side glass of the experimental tank. We describe the hardware construction of the apparatus and the procedure of the behavioral paradigm. We also present data on how zebrafish respond to the tapping. Our results demonstrate that the method induces significant fear/anxiety responses. We argue that the simplicity of the method and the efficiency of the paradigm should make it popular among those who plan to use zebrafish as a tool in anxiety research.
Tài liệu tham khảo
Ahmed, O., Seguin, D., Gerlai, R. (2011). An automated predator avoidance task in zebrafish. Behavioural Brain Research, 216(1), 166-171. https://doi.org/10.1016/j.bbr.2010.07.028.
Ahmed TS, Fernandes Y, Gerlai R (2012). Effects of animated images of sympatric predators and abstract shapes on fear responses in zebrafish. Behaviour 149, 1125-1153.
Bass, S. L., Gerlai, R. (2008). Zebrafish (Danio rerio) responds differentially to stimulus fish: the effects of sympatric and allopatric predators and harmless fish. Behavioural Brain Research, 186(1), 107-117. https://doi.org/10.1016/j.bbr.2007.07.037.
Blaser, R. E., Gerlai, R. (2006). Behavioral phenotyping in zebrafish: comparison of three behavioral quantification methods. Behavior Research Methods, 38, 456–469.
Chouinard-Thuly L, Gierszewski S, Rosenthal GG, Reader SM, Rieucau G, Woo KL, Gerlai R, et al. (2017). Technical and conceptual considerations for using animated stimuli in studies of animal behaviour. Current Zoology 63, 5-19
Craske, M. G., Stein, M.B. (2016). Anxiety. The Lancet, 388(10063), 3048-3059. https://doi.org/10.1016/S0140-6736(16)30381-6.
de Abreu MS, Giacomini ACVV, Demin KA, Galstyan DS, Zabegalov KN, Kolesnikova TO, Amstislavskaya TG, Strekalova T, Petersen EV, Kalueff AV. (2021). Unconventional anxiety pharmacology in zebrafish: Drugs beyond traditional anxiogenic and anxiolytic spectra. Pharmacol Biochem Behav. ;207:173205. https://doi.org/10.1016/j.pbb.2021.173205.
Dugatkin, L. A., Godin, J. G. (1992). Predator inspection, shoaling and foraging under predation hazard in the Trinidadian guppy, Poecilia reticulata. Environmental Biology of Fishes, 34, 265–276.
Eddins D, Cerutti D, Williams P, Linney E, Levin ED. (2010). Zebrafish provide a sensitive model of persisting neurobehavioral effects of developmental chlorpyrifos exposure: comparison with nicotine and pilocarpine effects and relationship to dopamine deficits. Neurotoxicology and Teratology; 32(1):99-108.
Engeszer, R. E., Patterson, L. B., Rao, A. A., Parichy, D. M. (2007). Zebrafish in the wild: a review of natural history and new notes from the field. Zebrafish, 4(1), 21-40. https://doi.org/10.1089/zeb.2006.9997.
Facciol, A., Iqbal, M., Eada, A., Tran, S., Gerlai, R. (2019). The light-dark task in zebrafish confuses two distinct factors: Interaction between background shade and illumination level preference. Pharmacology Biochemistry and Behavior, 179, 9-21. https://doi.org/10.1016/j.pbb.2019.01.006.
Gerlai, R (2017). Animated Images in the analysis of zebrafish behaviour. Current Zoology, 63, 35-44.
Gerlai, R. (2020a). Evolutionary conservation, translational relevance and cognitive function: The future of zebrafish in behavioral neuroscience. Neuroscience & Biobehavioral Reviews, 116, 426-435. https://doi.org/10.1016/j.neubiorev.2020.07.009.
Gerlai R (2020b). Fear responses and antipredatory behavior of zebrafish: A translational perspective. In: Gerlai R (Ed). Behavioral and Neural Genetics of Zebrafish, Elsevier, Academic Press, Amsterdam, The Netherlands ISBN: 9780128175286 pp155-173.
Gerlai R (2013). Antipredatory behavior of zebrafish: Adaptive function and a tool for translational research. Evolutionary Psychology 11: 1-15
Gerlai, R. (2012). Using zebrafish to unravel the genetics of complex brain disorders. Current Topics in Behavioral Neurosciences, 12, 3-24. https://doi.org/10.1007/7854_2011_180.
Gerlai, R. (2010a). High-throughput behavioral screens: the first step towards finding genes involved in vertebrate brain function using zebrafish. Molecules, 15(4), 2609-2622. https://doi.org/10.3390/molecules15042609.
Gerlai, R. (2010b). Zebrafish antipredatory responses: a future for translational research? Behavioural Brain Research, 207(2), 223-231. https://doi.org/10.1016/j.bbr.2009.10.008.
Gerlai, R., Fernandes, Y., Pereira, T. (2009). Zebrafish (Danio rerio) responds to the animated image of a predator: towards the development of an automated aversive task. Behavioural Brain Research, 201(2), 318-324. https://doi.org/10.1016/j.bbr.2009.03.003.
Gerlai, R. (1993). Can paradise fish (Macropodus opercularis) recognize its natural predator? An ethological analysis. Ethology, 94, 127-136.
Jesuthasan, S. (2012). Fear, anxiety, and control in the zebrafish. Developmental Neurobiology, 72(3), 395-403. https://doi.org/10.1002/dneu.20873.
Kalueff, A. V., Stewart, A. M., Gerlai, R. (2014). Zebrafish as an emerging model for studying complex brain disorders. Trends in Pharmacological Sciences, 35(2), 63-75. https://doi.org/10.1016/j.tips.2013.12.002.
Kalueff AV, Gebhardt M, Stewart AM, Cachat JM, Brimmer M, Chawla JS, Craddock C, Kyzar EJ, Roth A, Landsman S, Gaikwad S, Robinson K, Baatrup E, Tierney K, Shamchuk A, Norton W, Miller N, Nicolson T, Braubach O, Gilman CP, Pittman J, Rosemberg DB, Gerlai R, Echevarria D, Lamb E, Neuhauss SCF, Weng W, Bally-Cuif L, Schneider H, and the Zebrafish Neuroscience Research Consortium (2013). Towards a comprehensive catalog of zebrafish behavior 1.0, and beyond. Zebrafish. 10: 70-86.
Levin ED. (2011). Zebrafish assessment of cognitive improvement and anxiolysis: filling the gap between in vitro and rodent models for drug development. Reviews in the Neurosciences; 22(1):75-84.
Levin, E. D., Bencan, Z., Cerutti, D. T. (2007). Anxiolytic effects of nicotine in zebrafish. Physiology & Behavior, 90(1), 54-58. https://doi.org/10.1016/j.physbeh.2006.08.026.
Luca, R. M., Gerlai, R. (2012a). In search of optimal fear inducing stimuli: Differential behavioral responses to computer animated images in zebrafish. Behavioural Brain Research, 226(1), 66-76. https://doi.org/10.1016/j.bbr.2011.09.001.
Luca R, Gerlai R (2012b) Animated bird silhouette above the tank: Acute alcohol diminishes fear responses in zebrafish. Behav. Brain Res. 229: 194-201.
Lush, M. E., Piotrowski, T. (2014). Sensory hair cell regeneration in the zebrafish lateral line. Developmental Dynamics, 243(10), 1187-202. https://doi.org/10.1002/dvdy.24167.
Maximino, C., de Brito, T. M., da Silva Batista, A. W., Herculano, A. M., Morato, S., Gouveia, A Jr. (2010). Measuring anxiety in zebrafish: a critical review. Behavioural Brain Research, 214(2), 157-171. https://doi.org/10.1016/j.bbr.2010.05.031.
McHenry M.J., Feitl K.E., Strother J.A. and Van Trump W.J. (2009). Larval zebrafish rapidly sense the water flow of a predator's strike. Biology Letters 5(4), 477–479. https://doi.org/10.1098/rsbl.2009.0048
Mogdans, J. (2019). Sensory ecology of the fish lateral-line system: Morphological and physiological adaptations for the perception of hydrodynamic stimuli. Journal of Fish Biology, 95(1), 53-72. https://doi.org/10.1111/jfb.13966.
Murrough, J. W., Yaqubi, S., Sayed, S., Charney, D. S. (2015). Emerging drugs for the treatment of anxiety. Expert Opinion on Emerging Drugs, 20(3), 393-406. https://doi.org/10.1517/14728214.2015.1049996
Olszewski J, Haehnel M, Taguchi M, Liao JC (2012) Zebrafish Larvae Exhibit Rheotaxis and Can Escape a Continuous Suction Source Using Their Lateral Line. PLoS ONE 7(5): e36661. https://doi.org/10.1371/journal.pone.0036661
Parichy, D. M., Postlethwait, J. H. (2020). The biotic and abiotic environment of zebrafish, in: R.T. Gerlai (Ed.), Behavioral and Neural Genetics of Zebrafish (pp. 17-32). Elsevier.
Parra, K. V., Adrian, J. C. Jr, Gerlai, R. (2009). The synthetic substance hypoxanthine 3-N-oxide elicits alarm reactions in zebrafish (Danio rerio). Behavioural Brain Research, 205(2), 336-41. https://doi.org/10.1016/j.bbr.2009.06.037.
Pelkowski, S. D., Kapoor, M., Richendrfer, H. A., Wang, X., Colwill, R. M., Creton, R. (2011). A novel high-throughput imaging system for automated analyses of avoidance behavior in zebrafish larvae. Behavioural Brain Research, 223(1), 135-144. https://doi.org/10.1016/j.bbr.2011.04.033.
Perusini, J. N., Fanselow, M. S. (2015). Neurobehavioral perspectives on the distinction between fear and anxiety. Learning & Memory, 22(9), 417-425. https://doi.org/10.1101/lm.039180.115.
Pitcher, T. J. (1992). Who dares wins: the function and evolution of predator inspection behaviour in shoaling fish. Netherlands Journal of Zoology, 42, 371–391.
Pittman, J. T., Lott, C. S. (2014). Startle response memory and hippocampal changes in adult zebrafish pharmacologically-induced to exhibit anxiety/depression-like behaviors. Physiology & Behavior, 123, 174-179. https://doi.org/10.1016/j.physbeh.2013.10.023.
Eaton RC, Didomenico R (1986). Role of the Teleost Escape Response during Development. Transactions of the American Fisheries Society, 115(1), 128-142.
Seguin D, Shams S, Gerlai R (2016). Behavioural responses to novelty or to a predator stimulus are not altered in adult zebrafish by early embryonic alcohol exposure. Alcoholism: Clin Exp Res 40: 2667-2675
Speedie, N., Gerlai, R. (2008). Alarm substance induced behavioral responses in zebrafish (Danio rerio). Behavioural Brain Research, 188(1), 168-177. https://doi.org/10.1016/j.bbr.2007.10.031.
Spence, R., Gerlach, G., Lawrence, C., Smith, C. (2008). The behaviour and ecology of the zebrafish, Danio rerio. Biological Reviews of the Cambridge Philosophical Society, 83(1), 13-34. https://doi.org/10.1111/j.1469-185X.2007.00030.x.
Stewart, A., Gaikwad, S., Kyzar, E., Green, J., Roth, A., Kalueff, A. V. (2012). Modeling anxiety using adult zebrafish: a conceptual review. Neuropharmacology, 62(1), 135-143. https://doi.org/10.1016/j.neuropharm.2011.07.037.
Suli, A., Watson, G. M., Rubel, E. W., & Raible, D. W. (2012). Rheotaxis in larval zebrafish is mediated by lateral line mechanosensory hair cells. PloS one, 7(2), e29727. https://doi.org/10.1371/journal.pone.0029727