Artículo

Estamos trabajando para incorporar este artículo al repositorio
Consulte el artículo en la página del editor
Consulte la política de Acceso Abierto del editor

Abstract:

There is growing interest in the neurobiological mechanisms involved in the extinction of aversive memory. This cognitive process usually occurs after repeated or prolonged presentation of a conditioned stimulus that was previously associated with an unconditioned stimulus. If extinction is considered to be a new memory, the role of the γ-aminobutyric acid system (GABAergic system) during extinction memory consolidation should be similar to that described for the original trace. It is also accepted that negative modulation of the GABAergic system before testing can impair extinction memory expression. However, it seems possible to speculate that inhibitory mechanisms may be required in order to acquire a memory that is inhibitory in nature. Using a combination of behavioral protocols, such as weak and robust extinction training procedures, and pharmacological treatments, such as the systemic administration of GABAA agonist (muscimol) and antagonist (bicuculline), we investigated the role of the GABAergic system in the different phases of the extinction memory in the crab Neohelice granulata. We show that the stimulation of the GABAergic system impairs and its inactivation facilitates the extinction memory consolidation. Moreover, fine variations in the GABAergic tone affect its expression at testing. Finally, an active GABAergic system is necessary for the acquisition of the extinction memory. This detailed description may contribute to the understanding of the role of the GABAergic system in diverse aspects of the extinction memory. © 2013 Federation of European Neuroscience Societies and John Wiley & Sons Ltd.

Registro:

Documento: Artículo
Título:The involvement of the GABAergic system in the formation and expression of the extinction memory in the crab Neohelice granulata
Autor:Tano, M.C.; Molina, V.A.; Pedreira, M.E.
Filiación:Laboratorio de Neurobiología de la Memoria, Departamento de Fisiología y Biología Molecular y Celular, IFIBYNE-CONICET, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Buenos Aires, C1428EHA, Argentina
Departamento de Farmacología, IFEC-CONICET, Facultad de Ciencias Químicas, Universidad Nacional de Córdoba, Córdoba, Argentina
Palabras clave:Associative learning; Extinction memory; GABA; Invertebrate; animal experiment; animal model; anticipation; article; aversive behavior; cognition; conditioning; controlled study; crab; extinction memory; GABAergic system; GABAergic transmission; information retrieval; locomotion; male; memory; memory consolidation; Neohelice granulata; neurobiology; neurotransmission; nonhuman; priority journal; protein analysis; protein expression; protein function; associative learning; extinction memory; GABA; invertebrate; Animals; Bicuculline; Brachyura; Conditioning, Classical; Extinction, Psychological; GABA-A Receptor Agonists; GABA-A Receptor Antagonists; Memory; Muscimol
Año:2013
Volumen:38
Número:9
Página de inicio:3302
Página de fin:3313
DOI: http://dx.doi.org/10.1111/ejn.12328
Título revista:European Journal of Neuroscience
Título revista abreviado:Eur. J. Neurosci.
ISSN:0953816X
CODEN:EJONE
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_0953816X_v38_n9_p3302_Tano

Referencias:

  • Abbot, J., Absence of blood-brain barrier in a crustacean, Carcimus maenas (1970) Nature, 225, pp. 291-293
  • Akirav, I., Raizel, H., Maroun, M., Enhancement of conditioned fear extinction by infusion of the GABA(A) agonist muscimol into the rat prefrontal cortex and amygdala (2006) Eur. J. Neurosci., 23, pp. 758-764
  • Berlau, D.J., McGaugh, J.L., Enhancement of extinction memory consolidation: the role of the noradrenergic and GABAergic systems within the basolateral amygdala (2006) Neurobiol. Learn. Mem., 86, pp. 123-132
  • Bouton, M.E., Context and behavioral processes in extinction (2004) Learn Mem., 11, pp. 485-494
  • Bouton, M.E., Kenney, F.A., Rosengard, C., State-dependent fear extinction with two benzodiazepine tranquilisers (1990) Behav. Neurosci., 104, pp. 44-55
  • Carbó Tano, M., Molina, V.A., Maldonado, H., Pedreira, M.E., Memory consolidation and reconsolidation in an invertebrate model: the role of the GABAergic system (2009) Neuroscience, 158, pp. 387-401
  • Chhatwal, J.P., Myers, K.M., Ressler, K.J., Davis, M., Regulation of gephyrin and GABAA receptor binding within the amygdala after fear acquisition and extinction (2005) J. Neurosci., 25, pp. 502-506
  • Corcoran, K.A., Maren, S., Hippocampal inactivation disrupts contextual retrieval of fear memory after extinction (2001) J. Neurosci., 21, pp. 1720-1726
  • Davis, M., Myers, K.M., The role of glutamate and gamma-aminobutyric acid in fear extinction: clinical implications for exposure therapy (2002) Biol. Psychiatry, 52, pp. 998-1007
  • Domjan, M., Pavlovian conditioning: a functional perspective (2005) Annu. Rev. Psychol., 56, pp. 179-206
  • Erdö, S.L., Kiss, B., Riesz, M., Szporny, L., Stimulus-evoked efflux of GABA from preloaded slices of the rabbit oviduct (1986) Eur. J. Pharmacol., 130, pp. 295-303
  • Estes, W.K., Memory and conditioning (1973) Contemporary Approaches to Conditioning and Learning, pp. 265-286. , In McGuigan, F.J. & Lumsden, D.B. (Eds), Winston, Washington DC
  • Fustiñana, M.S., Carbó Tano, M., Romano, A., Pedreira, M.E., Contextual Pavlovian conditioning in the crab Chasmagnathus (2013) Anim. Cogn., 16, pp. 255-272
  • Goldman, M.S., Effect of chlordiazepoxide administered early in extinction on subsequent extinction of a conditioned emotional response in rats: implications for human clinical use (1977) Psychol. Rep., 40, pp. 783-786
  • Harris, J.A., Westbrook, R.F., Evidence that GABA transmission mediates context-specific extinction of learned fear (1998) Psychopharmacology, 140, pp. 105-115
  • Hart, G., Harris, J.A., Westbrook, R.F., Systemic or intra-amygdala injection of a benzodiazepine (midazolam) impairs extinction but spares re-extinction of conditioned fear responses (2009) Learn Mem., 16, pp. 53-61
  • Hart, G., Harris, J.A., Westbrook, R.F., Systemic or intra-amygdala infusion of the benzodiazepine, midazolam, impairs learning, but facilitates re-learning to inhibit fear responses in extinction (2010) Learn Mem., 17, pp. 210-220
  • Heldt, S.A., Ressler, K.J., Training-induced changes in the expression of GABAA-associated genes in the amygdala after the acquisition and extinction of Pavlovian fear (2007) Eur. J. Neurosci., 26, pp. 3631-3644
  • Helmstetter, F.J., Bellgowan, P.S., Effects of muscimol applied to the basolateral amygdala on acquisition and expression of contextual fear conditioning in rats (1994) Behav. Neurosci., 108, pp. 1005-1009
  • Hepp, Y., Pérez-Cuesta, L.M., Maldonado, H., Pedreira, M.E., Extinction memory in the crab Chasmagnathus: recovery protocols and effects of multi-trial extinction training (2010) Anim. Cogn., 13, pp. 391-403
  • Herry, C., Ferraguti, F., Singewald, N., Letzkus, J.J., Ehrlich, I., Lüthi, A., Neuronal circuits of fear extinction (2010) Eur. J. Neurosci., 31, pp. 599-612
  • Hoeger, U., Florey, E., Catecholamine degradation in the hemolymph of the Chinese crab, Eriocheir Sinensis (1989) Comp. Biochem. Physiol. C., 92, pp. 323-327
  • Howell, D.C., (2009) Statistical Methods for Psychology, , 7th Edn. Wadsworth Publishing
  • Josselyn, S.A., Shi, C., Carlezon, W.A.J., Neve, R.L., Nestler, E.J., Davis, M., Long-term memory is facilitated by cAMP response element-binding protein over expression in the amygdala (2001) J. Neurosci., 21, pp. 2404-2412
  • Kamano, D.K., Using drugs to modify the effect of response prevention on avoidance extinction (1972) Behav. Res. Ther., 10, pp. 367-370
  • Konorski, J., (1948) Conditioned Reflexes and Neuron Organization, , Univ. Press, New York, NY
  • Lin, C.-H., Yeh, S.-H., Lu, H.-Y., Gean, P.-W., The similarities and diversities of signal pathways leading to consolidation of conditioning and consolidation of extinction of fear memory (2003) J. Neurosci., 23, pp. 8310-8317
  • Makkar, S.R., Zhang, S.Q., Cranney, J., Behavioral and neural analysis of GABA in the acquisition, consolidation, reconsolidation, and extinction of fear memory (2010) Neuropsychopharmacology, 35, pp. 1625-1652
  • Maldonado, H., Crustacean as model to investigate memory illustrated by extensive behavioral and physiological studies in Chasmagnathus (2002) The Crustacean Nervous System, pp. 314-332. , In Wiese, K. (Ed.), Springer, Berlin
  • Maren, S., Quirk, G.J., Neuronal signalling of fear memory (2004) Nat. Rev. Neurosci., 5, pp. 844-852
  • McGaugh, J.L., Castellano, C., Brioni, J., Picrotoxin enhances latent extinction of conditioned fear (1990) Behav. Neurosci., 104, pp. 264-267
  • Monfils, M.H., Cowansage, K.K., Klann, E., LeDoux, J.E., Extinction-reconsolidation boundaries: key to persistent attenuation of fear memories (2009) Science, 324, pp. 951-955
  • Myers, K.M., Davis, M., Mechanisms of fear extinction (2007) Mol. Psychiatry, 12, pp. 120-150
  • Pan, W.-X., Brown, J., Dudman, J.T., Neural signals of extinction in the inhibitory microcircuit of the ventral midbrain (2013) Nat. Neurosci., 16, pp. 71-78
  • Pávlov, I.P., (1927) Conditioned Reflexes, , 1960th Edn. Dover Publications, Inc., New York
  • Pedreira, M.E., Maldonado, H., Protein synthesis subserves reconsolidation or extinction depending on reminder duration (2003) Neuron, 38, pp. 863-869
  • Pedreira, M.E., Pérez-Cuesta, L.M., Maldonado, H., Mismatch between what is expected and what actually occurs triggers memory reconsolidation or extinction (2004) Learn Mem., 11, pp. 579-585
  • Pereyra, P., Saraco, M., Maldonado, H., Decreased response or alternative defensive strategy in escape: two different types of long-term memory in the crab Chasmagnathus (1999) J. Comp. Physiol. A., 184, pp. 301-310
  • Pérez-Cuesta, L.M., Maldonado, H., Memory reconsolidation and extinction in the crab: mutual exclusion or coexistence? (2009) Learn Mem., 16, pp. 714-721
  • Pérez-Cuesta, L.M., Hepp, Y., Pedreira, M.E., Maldonado, H., Memory is not extinguished along with CS presentation but within a few seconds after CS-offset (2007) Learn Mem., 14, pp. 101-108
  • (2012) R: A Language and Environment for Statistical Computing, , http://www.R-project.org, R Core Team. R Foundation for Statistical Computing, Vienna, Austria. Available. ISBN: 3-900051-07-0
  • Radulovic, J., Tronson, N.C., Molecular specificity of multiple hippocampal processes governing fear extinction (2010) Rev. Neurosci., 21, pp. 1-17
  • Rescorla, R.A., Spontaneous recovery (2004) Learn Mem., 11, pp. 501-509
  • Romano, A., Lozada, M., Maldonado, H., Nonhabituation processes affect stimulus specificity of response habituation in the crab Chasmagnathus granulatus (1991) Behav. Neurosci., 105, pp. 542-552
  • Rosenthal, R., Rosnow, R.L., (1985) Contrast Analysis: Focused Comparisons in the Analysis of Variance, , Cambridge University Press
  • (2012), http://www.rstudio.org/, Rstudio. RStudio: Integrated development environment for R (Version 0.96.122) [Computer software]. Boston, MA. Retrieved May 20, 2012. Available; Salinas, J.A., McGaugh, J.L., The amygdala modulates memory for changes in reward magnitude: involvement of the amygdaloid GABAergic system (1996) Behav. Brain Res., 80, pp. 87-98
  • Schafe, G.E., Nadel, N.V., Sullivan, G.M., Harris, A., LeDoux, J.E., Memory consolidation for contextual and auditory fear conditioning is dependent on protein synthesis, PKA, and MAP kinase (1999) Learn Mem., 6, pp. 97-110
  • Schiller, D., Raio, C.M., Phelps, E.A., Extinction training during the reconsolidation window prevents recovery of fear (2012) J. Vis. Exp., 6, pp. e3893
  • Spear, N.E., Retrieval of memory in animals (1973) Psychol. Rev., 80, pp. 163-194
  • Spear, N.E., Gordon, W.C., Sleep, dreaming, and the retrieval of memories (1981) Sleep, Dreams, and Memory, pp. 183-203. , In Fishbein, W. (Ed.), Spectrum Publications, New York, NY
  • Suárez, L.D., Smal, L., Delorenzi, A., Updating contextual information during consolidation as result of a new memory trace (2010) Neurobiol. Learn. Mem., 93, pp. 561-571
  • Tomsic, D., Massoni, V., Maldonado, H., Habituation to a danger estimulus in two semiterrestrial crabs: ontogenic, ecological and opioid modulation correlates (1993) J. Comp. Physiol. [A]., 173, pp. 621-633
  • Tomsic, D., Romano, A., Maldonado, H., Behavioral and mechanistic bases of long-term habituation in the crab Chasmagnathus (1998) Adv. Exp. Med. Biol., 446, pp. 17-35
  • Tronson, N.C., Corcoran, K.A., Jovasevic, V., Radulovic, J., Fear conditioning and extinction: emotional states encoded by distinct signaling pathways (2012) Trends Neurosci., 35, pp. 145-155
  • Wilensky, A.E., Schafe, G.E., LeDoux, J.E., The amygdala modulates memory consolidation of fear-motivated inhibitory avoidance learning but not classical fear conditioning (2000) J. Neurosci., 20, pp. 7059-7066

Citas:

---------- APA ----------
Tano, M.C., Molina, V.A. & Pedreira, M.E. (2013) . The involvement of the GABAergic system in the formation and expression of the extinction memory in the crab Neohelice granulata. European Journal of Neuroscience, 38(9), 3302-3313.
http://dx.doi.org/10.1111/ejn.12328
---------- CHICAGO ----------
Tano, M.C., Molina, V.A., Pedreira, M.E. "The involvement of the GABAergic system in the formation and expression of the extinction memory in the crab Neohelice granulata" . European Journal of Neuroscience 38, no. 9 (2013) : 3302-3313.
http://dx.doi.org/10.1111/ejn.12328
---------- MLA ----------
Tano, M.C., Molina, V.A., Pedreira, M.E. "The involvement of the GABAergic system in the formation and expression of the extinction memory in the crab Neohelice granulata" . European Journal of Neuroscience, vol. 38, no. 9, 2013, pp. 3302-3313.
http://dx.doi.org/10.1111/ejn.12328
---------- VANCOUVER ----------
Tano, M.C., Molina, V.A., Pedreira, M.E. The involvement of the GABAergic system in the formation and expression of the extinction memory in the crab Neohelice granulata. Eur. J. Neurosci. 2013;38(9):3302-3313.
http://dx.doi.org/10.1111/ejn.12328