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The swimming control group in spatial reference memory task: analysis of its motor cortex activity

S. Cid-Duarte, A. Gutiérrez-Menéndez, C. Zorzo, J. L. Arias, M. Méndez

Abstract


Spatial reference memory in rodents is commonly performed in the Morris Water Maze (MWM). The use of control groups on this task is essential in order to subtract brain activity not related to learning. To study the functional contribution of selected brain areas, we assessed neuronal metabolic activity thorough quantitative cytochrome c oxidase histochemistry. This technique allows the measurement of the oxidative metabolism responsible for ATP production. Our objective is to analyse if the swimming control group is an optimal control for the evaluation of spatial reference memory task. To do so, we explore the behaviour in the MWM and the neuronal metabolic activity of motor cortex and its layers, in addition to hippocampus. For this purpose, three groups of Wistar rats were used: reference memory group, swimming control, and cage control. The behavioural results show significant differences between the experimental group and the swimming control group in time spent in the quadrants and swimming speed. In addition, higher neuronal hippocampal metabolic activity (CA1 subfield) was found in the experimental when compared to both controls. However, there are no differences in the motor cortex neuronal metabolic activity of the groups. Therefore, we can assume that the swimming control group effectively isolates the motor activity during the swim and the behavioural results are due to the hippocampal activity related to learning itself and not the physical activity performed in the labyrinth.


Keywords


Morris water maze; rat; swimming control; motor cortex; cytochrome c oxidase

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Albasser, M.M., Dumont, J.R., Amin, E., Holmes, J.D., Horne, M.R., Pearce, J.M., Aggleton, J.P. Association rules for rat spatial learning: The importance of the hippocampus for binding item identity with item location. Hippocampus, 23: 1162–1178, 2013.

Terry A.V. Spatial Navigation (Water Maze) Tasks. pp. 164–177. In: Buccafusco J.J. (Ed). Methods Behav. Anal. Neurosci., Boca Raton (FL): CRC Press/Taylor & Francis, 2009.

Arias, N., Méndez, M., Arias, J. and Arias, J.L. Brain metabolism and spatial memory are affected by portal hypertension. Metab. Brain Dis., 27: 183–191, 2012.

Arias, N., Méndez, M., Vallejo, G. and Arias, J.L. Finding the place without the whole: Timeline involvement of brain regions. Brain Res., 1625: 18–28, 2015.

Bannerman, D.M., Good, M.A., Butcher, S.P. and Morris, R.G. Distinct components of spatial learning revealed by prior training and NMDA receptor blockade. Nature, 378: 182–186, 1995.

Beery, A.K. and Zucker, I. Sex bias in neuroscience and biomedical research. Neurosci. Biobehav. Rev., 35: 565–572, 2011.

Brandeis, R., Brandys, Y. and Yehuda, S. The use of the Morris water maze in the study of memory and learning. Int. J. Neurosci., 48: 29–69, 1989.

Bures, J., Buresová, O. and Huston, J.P. Techniques and basic experiments for the study of brain and behaviour. pp. 37-45. In: Bures J (Ed). Techniques and Basic Experiments for a Study of Brain and

Behavior, Elsevier Scientific Publishing Company, 1976.

Burgess, N. The 2014 nobel prize in physiology or medicine: A spatial model for cognitive neuroscience. Neuron, 84: 1120–1125, 2014.

Clark, R.E. and Martin, S.J. Interrogating rodents regarding their object and spatial memory. Curr. Opin. Neurobiol., 15: 593–598, 2005.

Conejo, N.M., González-Pardo, H., Gonzalez-Lima, F. and Arias, J.L. Spatial learning of the water maze: Progression of brain circuits mapped with cytochrome oxidase histochemistry. Neurobiol. Learn. Mem., 93: 362–371, 2010.

Conejo, N.M., González-Pardo, H., Vallejo, G. and Arias, J.L. Changes in brain oxidative metabolism induced by water maze training. Neuroscience, 145: 403–412, 2007.

D’Hooge, R. and De Deyn, P.P. Applications of the Morris water maze in the study of learning and memory. Brain Res. Rev., 36: 60-90, 2001.

Davoodi, F.G., Motamedi, F., Naghdi, N. and Akbari, E. Effect of reversible inactivation of the reuniens nucleus on spatial learning and memory in rats using Morris water maze task. Behav. Brain Res., 198: 130–135, 2009.

Ehninger, D. and Kempermann, G. Paradoxical effects of learning the Morris water maze on adult hippocampal neurogenesis in mice may be explained by a combination of stress and physical activity. Genes, Brain Behav., 5: 29–39, 2006.

Epstein, R.A., Patai, E.Z., Julian, J.B. and Spiers, H.J. The cognitive map in humans: Spatial navigation and beyond. Nat. Neurosci., 20: 1504–1513, 2017.

Fouquet, C., Tobin, C. and Rondi-Reig, L. A new approach for modeling episodic memory from rodents to humans: The temporal order memory. Behav. Brain Res., 215: 172–179, 2010.

Gonzalez-Lima, F. and Cada, A. Cytochrome oxidase activity in the auditory system of the mouse: A qualitative and quantitative histochemical study. Neuroscience, 63: 559–578, 1994.

He, J. et al. Neurochemical changes in the hippocampus and prefrontal cortex associated with electroacupuncture for learning and memory impairment. Int. J. Mol. Med., 41: 709–716, 2018.

Hunsaker, M.R. and Kesner, R.P. Unfolding the cognitive map: The role of hippocampal and extra-hippocampal substrates based on a systems analysis of spatial processing. Neurobiol. Learn. Mem., 147: 90–119, 2018.

Kus, K., Ratajczak, P., Czaja, N., Zaprutko, T. and Nowakowska, E. Effect of combined administration of aripiprazole and fluoxetine on cognitive functions in female rats exposed to ethyl alcohol. Acta Neurobiol. Exp. (Wars)., 77: 86–93, 2017.

McCloskey, D.P., Adamo, D.S. and Anderson, B.J. Exercise increases metabolic capacity in the motor cortex and striatum, but not in the hippocampus. Brain Res., 891: 168–175, 2001.

Méndez, M., Méndez-López, M., López, L., Aller, M.A., Arias, J., Cimadevilla J.M. and Arias, J.L. Spatial memory alterations in three models of hepatic encephalopathy. Behav. Brain Res., 188: 32–40, 2008.

Méndez-López, M., Méndez, M., López, L. and Arias, J.L. Sexually dimorphic c-Fos expression following spatial working memory in young and adult rats. Physiol. Behav., 98: 307–317, 2009a.

Méndez-López, M., Méndez, M., López, L. and Arias, J.L. Spatial working memory learning in young male and female rats: Involvement of different limbic system regions revealed by cytochrome oxidase activity. Neurosci. Res., 65: 28–34, 2009a.

Méndez-López, M., Méndez, M., López, L., Cimadevilla, J. M. and Arias, J.L. Hippocampal heterogeneity in spatial memory revealed by cytochrome oxidase. Neurosci. Lett., 452: 162–166, 2009c.

Méndez-López, M., Méndez, M., Sampedro-Piquero, P. and Arias, J.L. Spatial learning-related changes in metabolic activity of limbic structures at different posttask delays. J. Neurosci. Res., 91: 151–159, 2013.

Morris, R.G. Developments of a water-maze procedure for studying spatial learning in the rat. J. Neurosci. Methods, 11: 47–60, 1984.

Morris, R.G. Spatial localization does not require the presence of local cues. Learn. Motiv., 12: 239–260, 1981.

Moscovitch, M., Cabeza, R., Winocur, G. and Nadel, L. Episodic Memory and Beyond: The Hippocampus and Neocortex in Transformation. Annu. Rev. Psychol., 67: 105–34, 2016.

Moser, E.I., Krobert, K.A., Moser, M.B. and Morris, R.G. Impaired spatial learning after saturation of long-term potentiation. Science, 281: 2038–2042, 1998.

O’Keefe, J. and Nadel, L. The hippocampus as a cognitive map. pp. 141-230. Hippocampus Physiology, Oxford: Oxford University Press, 1978.

Papez, J.W. A proposed mechanism for emotion. Arch. Nerology

Psyquiatry, 38: 725–743, 1937.

Paxinos, G. and Watson, C. The rat brain in stereotaxic coordinates. Elsevier Academic Press, 2005.

Pooters, T., Gantois, I., Vermaercke, B. and D’Hooge, R. Inability to acquire spatial information and deploy spatial search strategies in mice with lesions in dorsomedial striatum. Behav. Brain Res., 298: 134–141, 2016.

Riedel, W.J. and Blokland, A. Declarative Memory. Handb. Exp. Pharmacol., 228: 215–236, 2015.

Rubio, S., Begega, A., Méndez, M., Méndez-López, M. and Arias, J.L. Similarities and differences between the brain networks underlying allocentric and egocentric spatial learning in rat revealed by cytochrome oxidase histochemistry. Neuroscience, 223: 174–182, 2012.

Shinohara, K. and Hata, T. Post-acquisition hippocampal NMDA receptor blockade sustains retention of spatial reference memory in Morris water maze. Behav. Brain Res., 1: 261–267, 2014.

Sneddon, L.U., Halsey, L.G. and Bury, N.R. Considering aspects of the 3Rs principles within experimental animal biology. J. Exp. Biol., 220: 3007-3016, 2017.

Squire, L.R., Stark, C.E.L. and Clark, R.E. The medial temporal lobe. Annu. Rev. Neurosci., 27: 279–306, 2004.

Tolman, E.C. Cognitive maps in rats and men. Psychol. Rev., 55: 189–208, 1948.

Vorhees, C.V. and Williams, M.T. Morris water maze: procedures for assessing spatial and related forms of learning and memory. Nat Protoc., 1: 848–858, 2006.

Wei, P.H., Mao, Z.Q., Cong, F., Yeh, F.C., Wang, B., Ling, Z.P., Liang, S.L., Chen, L., Yu, X.G., In vivo visualization of connections among revised Papez circuit hubs using full q-space diffusion spectrum imaging tractography. Neuroscience, 357: 400–410, 2017.

Wong-Riley, M.T. Cytochrome oxidase: an endogenous metabolic marker for neuronal activity. Trends Neurosci., 12: 94–101, 1989.

Xie, M. et al. Short-term sleep deprivation disrupts the molecular composition of ionotropic glutamate receptors in entorhinal cortex and impairs the rat spatial reference memory. Behav. Brain Res., 300: 70–76, 2016.




DOI: https://doi.org/10.12871/aib.v158i2.4719

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