Possibilities and Prospects of the Behavioral Test “Morris Water Maze”

Journal of Evolutionary Biochemistry and Physiology - Tập 57 - Trang 289-303 - 2021
D. P. Chernyuk1, A. V. Bol’shakova1, O. L. Vlasova1, I. B. Bezprozvanny1,2
1Peter the Great St. Petersburg Polytechnic University, St. Petersburg, Russia
2Department of Physiology, University of Texas Southwestern Medical Center, Dallas, TX, USA

Tóm tắt

The Morris Water Maze (MWM) behavioral test is a universal method for testing cognitive functions in experimental rodents, and it is especially effective in detecting deviations in memory functions and learning, which makes it indispensable in a study of aging, stroke, neurodegenerative diseases, effects of therapeutic drugs, and so on. However, this test can be a far more informative tool for analyzing the behavior of experimental animals than it seems at first glance. The formation and consolidation of memory, as well as learning, are quite complex processes that mainly involve the hippocampus but, in addition, many other brain areas. The numerous MWM protocols are so sensitive to changes in functioning of different, not only hippocampal, brain areas that they can be used as an “indicator” of normal cognitive function. Thus, MWM modifications involve different mechanisms of navigation, learning and memory, and the results of these tests, as well as their correct interpretation, can give a lot more information about the behavior of tested animals. Here, we survey most popular methods for conducting the MWM procedure and discuss those informative parameters that can help analyze the results of this test.

Tài liệu tham khảo

Morris, R.G.M., Spatial localization does not require the presence of local cues, Learning and Motivation, 1981, vol. 1(2), pp. 239–260. Morris, R.G.M., Developments of a water-maze procedure for studying spatial learning in the rat, J. Neurosci. Methods, 1984, vol. 11(1), pp. 47–60. Sutherland, R.J., Whishaw, I.Q., and Kolb, B., Contributions of cingulate cortex to two forms of spatial learning and memory, J. Neurosci., 1988, vol. 8(6), pp. 1863–1872. Brandeis, R., Brandys, Y., and Yehuda, S., The use of the Morris Water Maze in the study of memory and learning, Int. J. Neurosci., 1989, vol. 48(1–2), pp. 29–69. Vorhees, C.V. and Williams, M.T., Morris water maze: procedures for assessing spatial and related forms of learning and memory, Nat. Protoc., 2006, vol. 1(2), pp. 848–858. Buresova, O., Krekule, I., Zahalka, A., and Bures, J., On-demand platform improves accuracy of the Morris water maze procedure. J. Neurosci. Methods, 1985, vol. 15(1), pp. 63–72. Whishaw, I.Q. and Mittleman, G., Visits to starts, routes and places by rats (Rattus norvegicus) in swimming pool navigation tasks, J. Comp. Psychol., 1987, vol. 100, pp. 422–443. Nakazawa, K., Quirk, M.C., Chitwood, R.A., Watanabe, M., Yeckel, M.F., Sun, L.D., Kato, A., Carr, C.A., Johnston, D., Wilson, M.A., and Tonegawa, S., Requirement for hippocampal CA3 NMDA receptors in associative memory recall, Science, 2002, vol. 297(5579), pp. 211–218. Brun, V.H., Otnass, M.K., Molden, S., Steffenach, H.A., Witter, M.P., Moser, M.B. and Moser, E.I., Place cells and place recognition maintained by direct entorhinal-hippocampal circuitry, Science, 2002, vol. 296(5576), pp. 2243–2246. Kallai, J., Makany, T., Karadi, K., and Jacobs, W.J., Spatial orientation strategies in Morris-type virtual water task for humans, Behav. Brain Res., 2005, vol. 159(2), pp. 187–196. Morris, R.G.M., An attempt to dissociate ‘spatial-mapping’ and ‘working-memory’ theories of hippocampal function, Neurobiology of the Hippocampus, New York, 1993. Lindner, M.D., Balch, A.H., and VanderMaelen, C.P., Short forms of the “reference-” and “working-memory” Morris water maze for assessing age-related deficits, Behav. Neural. Biol., 1992, vol. 58(2), pp. 94–102. Smolensky, I.V., Zubareva, O.E., Kalemenev, S.V., Lavrentyeva, V.V., Dyomina, A.V., Karepanov, A.A., and Zaitsev, A.V., Impairments in cognitive functions and emotional and social behaviors in a rat lithium-pilocarpine model of temporal lobe epilepsy, 2019, Behav. Brain Res., 2019, vol. 372, p. 112044. Crawley, J.N., Behavioral phenotyping strategies for mutant mice, Neuron, 2008, vol. 57(6), pp. 809–818. Nunn, J.A., LePeillet, E., Netto, C.A., Hodges, H., Gray, J.A., and Meldrum, B.S., Global ischaemia: hippocampal pathology and spatial deficits in the water maze, Behav. Brain Res., 1994, vol. 62(1), pp. 41–54. Gallagher, M. and Rapp, P.R., The use of animal models to study the effects of aging on cognition, Annu. Rev. Psychol., 1997, vol. 48, pp. 339–370. Hsiao, K., Chapman, P., Nilsen, S., Eckman, C., Harigaya, Y., Younkin, S., Yang, F., and Cole, G., Correlative memory deficits, Abeta elevation, and amyloid plaques in transgenic mice, Science, 1996, vol. 274(5284), pp. 99–102. Bromley-Brits, K., Deng, Y., and Song, W., Morris water maze test for learning and memory deficits in Alzheimer's disease model mice, J. Vis. Exp., 2011, vol. (53), e2920. https://doi.org/10.3791/2920 (2011) Edwards, S.R., Hamlin, A.S., Marks, N., Coulson, E.J., and Smith, M.T., Comparative studies using the Morris water maze to assess spatial memory deficits in two transgenic mouse models of Alzheimer's disease, Clin. Exp. Pharmacol. Physiol., 2014, vol. 41(10), pp. 798–806. Shariatpanahi, M., Khodagholi, F., Ashabi, G., Bonakdar Yazdi, B., Hassani, S., Azami, K., Abdollahi, M., Noorbakhsh, F., Taghizadeh, G., and Sharifzadeh, M., The involvement of protein kinase G inhibitor in regulation of apoptosis and autophagy markers in spatial memory deficit induced by Abeta, Fundam. Clin. Pharmacol., 2016, vol. 30(4), pp. 364–375. Wu, M.N., Zhou, L.W., Wang, Z.J., Han, W.N., Zhang, J., Liu, X.J., Tong, J.Q., and Qi, J.S., Colivelin ameliorates amyloid beta peptide-induced impairments in spatial memory, synaptic plasticity, and calcium homeostasis in rats, Hippocampus, 2015, vol. 25(3), pp. 363–372. Ge, M., Zhan, Y., Hao, Q., Zhao, Y., and Dong, B., Effects of mesenchymal stem cells transplantation on cognitive deficits in animal models of Alzheimer’s disease: A systematic review and meta-analysis, Brain Behav., 2018, vol. 8(7), e00982. https://doi.org/10.1002/brb3.982 D’Hooge, R. and De Deyn, P.P., Applications of the Morris water maze in the study of learning and memory, Brain Res. Brain Res. Rev., 2001, vol. 36(1), pp. 60–90. Noldus, L.P., Spink, A.J., and Tegelenbosch, R.A., EthoVision: a versatile video tracking system for automation of behavioral experiments, Behav. Res. Methods Instrum. Comput., 2001, vol. 33(3), pp. 398–414. Spink, A.J., Tegelenbosch, R.A., Buma, M.O., Fursenko, D.V., and Kulikov, A.V., Conducting and automating Morris water maze test under SPF conditions, Russ. J. Genet. Appl. Res., 2016, vol. 6, pp. 394–399. Khotskin, N.V., Kulikov, V.A., Zavyalov, E.L., Fursenko, D.V., and Kulikov, A.V., Conducting and automating Morris water maze test under SPF conditions, Russ. J. Genet. Appl. Res., 2016, vol. 6, pp. 394–399. Glaser, O.C., The formation of habits at high speed, J. Comp. Neurol. Psychol., 1910, vol. 20(3), pp. 165–184. Wever, E.G., Water temperature as an incentive to swimming activity in the rat, J. Compar. Psychol., 1932, vol. 14(2), pp. 219–224. Waller, M.B., Waller, P.F., and Brewster, L.A., A Water Maze for use in studies of drive and learning, Psychol. Rep., 1960, vol. 7(1), pp. 99–102. Woods, P.J., Davidson, E.H., and Peters, R.J. Jr., Instrumental escape conditioning in a water tank: effects of variations in drive stimulus intensity and reinforcement magnitude, J. Comp. Physiol. Psychol., 1964, vol. 57, pp. 466–470. Woods, P.J. and Holland, C.H., Performance on a black-white discrimination problem in water-maze as influenced by water temperature and swimming ability, Psychol. Rep., 1961, vol. 9, pp. 433–439. Morgan, D., Water Maze tasks in mice: special reference to Alzheimer's transgenic mice, Methods of Behavioral Analysis in Neuroscience, vol. 2, p. 14, Boca Raton (FL), 2009. Bryan, K.J., Lee, H., Perry, G., Smith, M.A. and Casadesus, G. Transgenic mouse models of Alzheimer’s disease: behavioral testing and considerations, Methods of Behavioral Analysis in Neuroscience, 2, 1, Boca Raton (FL), 2009. Morris, R.G.M., Morris water maze, Scholarpedia, 6315, 2008. Kim, J.J., Lee, H.J., Han, J.S., and Packard, M.G., Amygdala is critical for stress-induced modulation of hippocampal long-term potentiation and learning, J. Neurosci., 2001, vol. 21(14), pp. 5222–5228. Tomas Pereira, I. and Burwell, R.D., Using the spatial learning index to evaluate performance on the water maze, Behav. Neurosci., 2015, vol. 129(4), pp. 533–539. Gallagher, M., Burwell, R., and Burchinal, M., Severity of spatial learning impairment in aging: development of a learning index for performance in the Morris water maze, Behav. Neurosci., 1993, vol. 107(4), pp. 618–626. Westerman, M.A., Cooper-Blacketer, D., Mariash, A., Kotilinek, L., Kawarabayashi, T., Younkin, L.H., Carlson, G.A., Younkin, S.G., and Ashe, K.H., The relationship between Abeta and memory in the Tg2576 mouse model of Alzheimer’s disease, J. Neurosci., 2002, vol. 22(5), pp. 1858–1867. Steele, R.J. and Morris, R.G., Delay-dependent impairment of a matching-to-place task with chronic and intrahippocampal infusion of the NMDA-antagonist D-AP5, Hippocampus, 1999, vol. 9(2), pp. 118–136. Spooner, R.I., Thoson, A., Hall, J., Morris, R.G., and Salter, S.H., The Atlantis platform: a new design and further developments of Buresova’s on-demand platform for the water maze, Learn. Mem., 1994, vol. 1(3), pp. 203–211. Lipp, H.P. and Wolfer, D.P., Genetically modified mice and cognition, Curr. Opin. Neurobiol., 1998, vol. 8(2), pp. 272–280. Morris, R.G., Hagan, J.J., and Rawlins, J.N., Allocentric spatial learning by hippocampectomised rats: a further test of the “spatial mapping” and “working memory” theories of hippocampal function, Q. J. Exp. Psychol. B, 1986, vol. 38(4), pp. 365–395. Sutherland, R.J. and Dyck, R.H., Place navigation by rats in a swimming pool, Canad. J. Psychol., 1984, vol. 38, pp. 322–347. Vouros, A., Gehring, T.V., Szydlowska, K., Janusz, A., Tu, Z., Croucher, M., Lukasiuk, K., Konopka, W., Sandi, C., and Vasilaki, E., A generalised framework for detailed classification of swimming paths inside the Morris Water Maze, Sci. Rep., 2018, vol. 8(1), 15089. Morgan, D., Diamond, D.M., Gottschall, P.E., Ugen, K.E., Dickey, C., Hardy, J., Duff, K., Jantzen, P., DiCarlo, G., Wilcock, D., Connor, K., Hatcher, J., Hope, C., Gordon, M., and Arendash, G.W., A beta peptide vaccination prevents memory loss in an animal model of Alzheimer’s disease, Nature, 2000, vol. 408(6815), pp. 982–985. Maei, H.R., Zaslavsky, K., Teixeira, C.M., and Frankland, P.W., What is the most sensitive measure of water maze probe test performance? Front. Integr. Neurosci., 2009, vol. 3, p. 4. Whiting, M.D. and Kokiko-Cochran, O.N., Assessment of cognitive function in the water mMaze task: maximizing data collection and analysis in animal models of brain injury, Methods Mol. Biol., 2016, vol. 1462, pp. 553–571. Kokiko-Cochran, O., Ransohoff, L., Veenstra, M., Lee, S., Saber, M., Sikora, M., Teknipp, R., Xu, G., Bemiller, S., Wilson, G., Crish, S., Bhaskar, K., Lee, Y.S., Ransohoff, R.M., and Lamb, B.T., Altered neuroinflammation and behavior after traumatic brain injury in a mouse model of Alzheimer’s disease, J. Neurotrauma, 2016, vol. 33(7), pp. 625–640. Whishaw, I.Q., Cholinergic receptor blockade in the rat impairs locale but not taxon strategies for place navigation in a swimming pool, Behav. Neurosci., 1985, vol. 99(5), pp. 979–1005. Harker, K.T. and Whishaw, I.Q., Impaired spatial performance in rats with retrosplenial lesions: importance of the spatial problem and the rat strain in identifying lesion effects in a swimming pool, J. Neurosci., 2002, vol. 22(3), pp. 1155–1164. Bye, C.M., Hong, N.S., Moore, K., Deibel, S.H., and McDonald, R.J., The effects of pool shape manipulations on rat spatial memory acquired in the Morris water maze, Learn. Behav., 2019, vol. 47(1), pp. 29–37. Chernyuk, D.P., Zorin, A.G., Derevtsova, K.Z., Efimova, E.V., Prikhodko, V.A., Sysoev, Y.I., Vlasova, O.L., Bolsunovskaia, M.V., Bezprozvanny, I.B., Automatic analysis of the "Morris Water Maze" behavioral test data, I.P. Pavlov J. Higher Nerv. Activity, 2021, vol. 71(1), pp. 121–130. Rogers, J., Churilov, L., Hannan, A.J., and Renoir, T., Search strategy selection in the Morris water maze indicates allocentric map formation during learning that underpins spatial memory formation, Neurobiol. Learn. Mem., 2017, vol. 139, pp. 37–49. Morris, R., Neurobiology of Learning and Memory, Neuroscience in the 21st Century, 2013, pp. 2173–2211. Maurer, R. and Derivaz, V., Rats in a transparent Morris water maze use elemental and configural geometry of landmarks as well as distance to the pool wall, Spatial Cognit. Comput., 2000, vol. 2, pp. 135–156. Nunez, J., Morris water maze experiment, J. Vis. Exp., 2008, vol. (19), 897. Hodges, H., Maze procedures: the radial-arm and water maze compared, Brain Res. Cogn. Brain Res., 1996, vol. 3(3–4), pp. 167–181. Bello-Arroyo, E., Roque, H., Marcos, A., Orihuel, J., Higuera-Matas, A., Desco, M., Caiolfa, V.R., Ambrosio, E., Lara-Pezzi, E., and Gomez-Gaviro, M.V., MouBeAT: a new and open toolbox for guided analysis of behavioral tests in mice, Front. Behav. Neurosci., 2018, vol. 12, p. 201. Rodriguez, A., Zhang, H., Klaminder, J., Brodin, T., Andersson, P.L., and Andersson, M., ToxTrac: a fast and robust software for tracking organisms, Methods Ecol. Evolut., 2018, vol. 9(3), pp. 460–464. Aragao Rda, S., Rodrigues, M.A., de Barros, K.M., Silva, S.R., Toscano, A.E., de Souza, R.E., and Manhaes-de-Castro, R., Automatic system for analysis of locomotor activity in rodents—a reproducibility study, J. Neurosci. Methods, 2011, vol. 195(2), pp. 216–221.