Acquisition of a spatial navigation task in the padding pool induces an increase of GABA level in the hippocampus of Swiss mice

Authors

  • Isabela Cristina Sena Romano Programa de Pós-graduação em Neurociências, Laboratório de Neurociências Comportamental e Molecular, LaNeC, Universidade Federal de Minas Gerais, Belo Horizonte 31270-010, Brasil.
  • Angela Maria Ribeiro Departamento de Bioquímica e Imunologia – Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Belo Horizonte 31270-010, Brasil.

DOI:

https://doi.org/10.30574/gscarr.2021.7.2.0092

Keywords:

Spatial Learning, SWM, Hippocampus, GABA, Glutamate, Swiss mice

Abstract

The balance between excitatory and inhibitory glutamatergic and GABAergic systems, respectively, is crucial for the maintenance of complex cognitive functions such as learning. Using Swiss mice as experimental model, the aims of the present study were to evaluate cognitive performance in a shallow water maze (SWM) and the effects of training in this spatial navigation task on hippocampal GABA and glutamate levels.  In addition, correlations between neurochemical and behavioural data, and between glutamate and GABA levels were assessed. Forty-six three-month-old mice were divided into three groups: Learning, n=18: animals submitted to the SWM task; Active, n=14: animals exposed to the SWM, without the demand of performing a cognitive task and Control, n=14: the animals were kept in the vivarium without contact with the SWM. There was significant training effect indicating that the Learning group animals have learned the task. Regarding neurochemical data, the findings of the present work show for the first time that the task learning process in SWM has a significant effect on GABA levels in the hippocampus. The relationship between the two neurotransmitters, observed in the control animals, was adjusted by a significant increase in hippocampal GABA levels caused by the spatial training performed by the animals from the Learning group. However, the relationship observed in control condition is disrupted by a subsequent exposure to the maze in the absence of a spatial cognitive demand, as was the case of the Active group.  These data open new perspectives to explore the involvement of the inhibitory and excitatory systems in the molecular mechanisms associated with different types and steps of learning processes.

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References

Olton DS, Becker JT, Handelmann GE. Hippocampus, space and memory. Behav Brain Sci. 1979; 2: 313–65.

Kessels RPC, Haan EHF, Kappelle IJ, Postma A. Varieties of human spatial memory: a meta-analysis on the effects of hippocampal lesions. Brain Res Rev. 2001; 35: 295–303.

Hafting T, Fyhn M, Molden S, Moser MB, Moser EI. Microstructure of a spatial map in the entorhinal cortex. Nature. 2005; 436: 801–6.

Liguz-Lecznar M, Lehner M, Kaliszewska A, Zakrzewska R, Sobolewska A, Kossut M. Altered glutamate/GABA equilibrium in aged mice cortex influences cortical plasticity. Brain Struct Funct. 2015; 220: 1681–93.

Marshall P, Garton DR, Taira T, Võikar V, Vilenius C, Kulesskaya N, et al. Elevated expression of endogenous glial cell line-derived neurotrophic factor impairs spatial memory performance and raises inhibitory tone in the hippocampus. Eur J Neurosci. 2021. Advance on.

McGee AW, Bredt DS. Assembly and plasticity of glutamatergic postsynaptic specialization. Curr Opin Neurobiol. 2003; 13: 111–8.

Nacher J, Alonso-Llosa G, Rosell D, McEwen BS. NMDA receptor antagonist treatment increases the production of new neurons in the aged rat hippocampus. Neurobiol Aging. 2002; 5759: 1–12.

Mishra A, Goel RK. Psychoneurochemical investigations to reveal neurobiology of memory deficit in epilepsy. Neurochem Res. 2013; 38[12]: 2503–15.

Foster AC, Kemp JA. Glutamate- and GABA-based CNS therapeutics. Curr Opin Pharmacol. 2006; 6: 7–17.

Gao J, Wang H, Liu Y, Li YY, Chen C, Liu LM, et al. Glutamate and GABA imbalance promotes neuronal apoptosis in hippocampus after stress. Med Sci Monit. 2014; 20: 499–512.

Pires RGW, Pereira SRC, Oliveira-Silva IF, Franco GC, Ribeiro AM. Cholinergic parameters and the retrieval of learned and re-learned spatial information: a study using a model of Wernicke-Korsakoff Syndrome. Behav Brain Res. 2005; 162[1]: 11–21.

Oliveira-Silva IF, Pinto L, Pereira SRC, Ferraz VP, Barbosa AJA, Coelho VAA, et al. Age-related deficit in behavioural extinction is counteracted by long-term ethanol consumption: Correlation between 5-HIAA/5HT ratio in dorsal raphe nucleus and cognitive parameters. Behav Brain Res. 2007; 180: 226–34.

Freitas-Silva DM, Resende L, Pereira SR, Franco GC, Ribeiro AM. Maternal thiamine restriction during lactation induces cognitive impairments and changes in glutamate and GABA concentrations in brain of rat offspring. Behav Brain Res. 2010; 211: 33–40.

Nunes PT, Gómez-Mendoza DPR, Resende CP, Figueiredo HCP, Ribeiro AM. Thalamic proteome changes and behavioral impairments in thiamine-deficient rats. Neuroscience. 2018; 385: 181–97.

O’Keefe J, Dostrovsky J. The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. Behavioral Research, 1971; 34:171-175.

Deacon RMJ, Nicholas J, Rawlins JNP. Learning Impairments of Hippocampal-Lesioned Mice in a Paddling Pool. Behav Neurosci. 2002; 116[3]: 472–8.

Puig-Lagunes Á, Rocha L, Morgado-Valle C, BeltrÁn-Parrazal L, LÓpez-Meraz M. Brain and plasma amino acid concentration in infant rats prenatally exposed to valproic acid. An Acad Bras Cienc. 2021; 93[2].

Hoshi E, Tremblay L, Féger J, Carras PL, Strick PL. The cerebellum communicates with the basal ganglia. Nat Neurosci. 2005; 8: 1491–3.

McEntee W, Crook T. Glutamate: its role in learning, memory, and the aging brain. Psychopharmacology [Berl]. 1993; 111: 391–401.

Mengerink Y, Kutlán D, Tóth F, Csámpai A, Molnár-Perl I. Advances in the evaluation of the stability and characteristics of the amino acid and amine derivatives obtained with the o-phthaldialdehyde/3-mercaptopropionic acid and o-phthaldialdehyde/N-acetyl-L-cysteine reagents. High-performance liquid chromatography-mass spectrometry study. J Chromatogr A. 2002; 949(1-2): 99-124.

Sankowski R, Huerta TS, Kalra R., Klein TJ, Strohl JJ, Al-Abed, Yousef RS, Huerta PT. Large-Scale Validation of the Paddling Pool Task in the Clockmaze for Studying Hippocampus-Based Spatial Cognition in Mice. Frontiers in Behavioral Neuroscience. 7 Jun 2019; 13: 121.

Chang, SD, Liang, Kc. Roles of hippocampal GABA (A) and muscarinic receptors in consolidation of context memory and context-shock association in contextual fear conditioning: A double dissociation study. Neurobiology of Learning And Memory. 2012; 98(1): 17-24.

Takács VT, Cserép C, Schlingloff D, Pósfai B, Szőnyi A, Sos KE, Környei Z, Dénes Á, Gulyás AI, Freund TF, Nyiri G. Co-transmission of acetylcholine and GABA regulates hippocampal states. Nat Commun. 20 Jul 2018; 9(1): 28-48.

Durazzo TC, Meyerhoff DJ. GABA concentrations in the anterior cingulate and dorsolateral prefrontal cortices: Associations with chronic cigarette smoking, neurocognition, and decision making. Addict Biol. May 2021; 26(3): e12948.

Geiller T, Vancura B, Terada S, Troullinou E, Chavlis S, Tsagkatakis G, Tsakalides P, Ócsai K, Poirazi P, Rózsa BJ, Losonczy A. Large-Scale 3D Two-Photon Imaging of Molecularly Identified CA1 Interneuron Dynamics in Behaving Mice. Neuron. 9 Dec 2020; 108(5): 968-983.e9.

McNally GP, Augustyn KA, Richardson R. GABA [A] receptors determine the temporal dynamics of memory retention. Learn Mem. 2008; 15[3]: 106–11.

Toso L, Johnson A, Bissell S, Roberson R, Abebe D, Spong CY. Understanding the mechanism of learning enhancement: NMDA and GABA receptor expression. Am J Obs Gynecol. 2007; 197[3]: 267.

Sanderson DJ, Sprengel R, Seeburg PH, Bannerman DM. Deletion of the GluA1 AMPA receptor subunit alters the expression of short-term memory. Learn Mem. 2011; 18(3): 128-131.

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Published

2021-05-30

How to Cite

Sena Romano, I. C., & Ribeiro, A. M. (2021). Acquisition of a spatial navigation task in the padding pool induces an increase of GABA level in the hippocampus of Swiss mice. GSC Advanced Research and Reviews, 7(2), 016–024. https://doi.org/10.30574/gscarr.2021.7.2.0092

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Original Article