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Long-Term Contextual Memory in Mice: Persistence and Associability with Reinforcement

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Many animal species are able to use context as a conditioned signal for learning. In some cases, the initial memorization of the context and its subsequent association with an unconditioned stimulus can be separated by a long period of time – a phenomenon termed the “context preexposure effect.” This type of associative learning is based on a reminder and is significantly different from the classical version, though its properties have previously been studied only in rats. The present study addressed the formation of this type of conditioned link in mice. The conditioned signal was the context of a chamber, which the animals were allowed to explore for 5 min. After different time intervals, the mice were placed in the same chamber for 2 sec, during which they were given immediate electrocutaneous shocks (ECS). The mice formed a specific aversive memory for the preexplored context; formation of the memory did not occur if the animals received the same ECS in a context which was novel for them. This associative learning occurred in mice on application of the conditioned and unconditioned stimuli with intervals ranging from 30 min to 30 days. The resulting memory was long-term, persisting for at least 30 days. These results open up the potential for using mice of various transgenic strains for studying the cellular and molecular mechanisms of this type of associative learning.

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References

  • Amel’chenko, E. M., Zvorykina, S. V., Bezryadnov, D. V., et al., “Memory repair: a reminder restores conditioned reflex freezing impaired by a protein synthesis inhibitor in mice,” Zh. Vyssh. Nerv. Deyat., 63, No. 2, 227–234 (2013).

    Google Scholar 

  • Bevins, R. A., McPhee, J. E., Rauhut, A. S., and Ayres, J. J., “Converging evidence for one-trial context fear conditioning with an immediate shock: importance of shock potency,” J. Exp. Psychol. Anim. Behav. Process., 23, No. 3, 312–324 (1997).

    Article  CAS  PubMed  Google Scholar 

  • Biedenkapp, J. C. and Rudy, J. W., “Context preexposure prevents forgetting of a contextual fear memory: implication for regional changes in brain activation patterns associated with recent and remote memory tests,” Learn. Mem., 14, No. 3, 200–203 (2007).

    Article  PubMed  PubMed Central  Google Scholar 

  • Bourtchouladze, R., Abel, T., Berman, N., et al., “Different training procedures remit either one or two critical periods for contextual memory consolidation, each of which requires protein synthesis and PKA,” Learn. Mem., 5, No. 4–5, 365–374 (1998).

    CAS  PubMed  PubMed Central  Google Scholar 

  • Brown, K. L., Kennard, J. A., Sherer, D. J., et al., “The context preexposure facilitation effect in mice: a dose-response analysis of pre-training scopolamine administration,” Behav. Brain Res., 225, No. 1, 290–296 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fanselow, M. S., “Conditional and unconditional components of postshock freezing,” Pavlov J. Biol. Sci., 15, No. 4, 177–182 (1980).

    CAS  PubMed  Google Scholar 

  • Fanselow, M. S., “Factors governing one-trial contextual conditioning,” Anim. Learn. Behav., 18, No. 3, 264–270 (1990).

    Article  Google Scholar 

  • Fanselow, M. S., Kim, J. J., Yipp, J., and De Oca, B., “Differential effects of the N-methyl-D-aspartate antagonist DL2-amino-5-phosphonovalerate on acquisition of fear of auditory and contextual cues,” Behav. Neurosci., 108, No. 2, 235–240 (1994).

    Article  CAS  PubMed  Google Scholar 

  • Frankland, P. W., Josselyn, S. A., Anagnostaras, S. G., et al., “Consolidation of CS and US representations in associative fear conditioning,” Hippocampus, 14, No. 5, 557–569 (2004).

    Article  PubMed  Google Scholar 

  • Guenthner, C. J., Miyamichi, K., Yang, H. H., et al., “Permanent genetic access to transiently active neurons via TRAP: Targeted Recombination in Active Populations,” Neuron, 78, No. 5, 773–784 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Matus-Amat, P., Higgins, E. A., Barrientos, R. M., and Rudy, J. W., “The role of the dorsal hippocampus in the acquisition and retrieval of context memory representations,” J. Neurosci., 24, No. 10, 2431–2439 (2004).

    Article  CAS  PubMed  Google Scholar 

  • Murav’eva, E. V. and Anokhin, K. V., “Involvement of protein synthesis in memory reconsolidation at different times after training to conditioned reflex freezing in mice,” Zh. Vyssh. Nerv. Deyat., 56, No. 2, 274–282 (2006).

    Google Scholar 

  • Nakayama, D., Baraki, Z., Onoue, K., et al., “Frontal association cortex is engaged in stimulus integration during associative learning,” Curr. Biol., 25, 117–123 (2015).

    Article  CAS  PubMed  Google Scholar 

  • Reijmers, L. G., Perkins, B. L., Matsuo, N., and Mayford, M., “Localization of a stable neural correlate of associative memory,” Science, 317, No. 5842, 1230–1233 (2007).

    Article  CAS  PubMed  Google Scholar 

  • Rudy, J. W. and Morledge, P., “Ontogeny of contextual fear conditioning in rats: implications for consolidation, infantile amnesia, and hippocampal system function,” Behav. Neurosci., 108, No. 2, 227–234 (1994).

    Article  CAS  PubMed  Google Scholar 

  • Rudy, J. W. and O’Reilly, R. C., “Conjunctive representations, the hippocampus, and contextual fear conditioning,” Cogn. Affect. Behav. Neurosci., 1, No. 1, 66–82 (2001).

    Article  CAS  PubMed  Google Scholar 

  • Rudy, J. W. and O’Reilly, R. C., “Contextual fear conditioning, conjunctive representations, pattern completion, and the hippocampus,” Behav. Neurosci., 113, No. 5, 867–880 (1999).

    Article  CAS  PubMed  Google Scholar 

  • Rudy, J. W. and Wright-Hardesty, K., “The temporal dynamics of retention of a context memory: something is missing,” Learn. Mem., 12, 172–177 (2005).

    Article  PubMed  PubMed Central  Google Scholar 

  • Rudy, J. W., “Context representations, context functions, and the parahippocampal-hippocampal system,” Learn. Mem., 16, No. 10, 573–585 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  • Rudy, J. W., Huff, N. C., and Matus-Amat, P., “Understanding contextual fear conditioning: insights from a two-process model,” Neurosci. Biobehav. Rev., 28, 675–685 (2004).

    Article  CAS  PubMed  Google Scholar 

  • Westbrook, R. F., Good, A. J., and Kiernan, M. J., “Effects of the interval between exposure to a novel environment and the occurrence of shock on the freezing responses of rats,” Q. J. Exp. Psychol. B., 47, No. 4, 427–446 (1994).

    CAS  PubMed  Google Scholar 

  • Wheeler, A. L., Teixeira, C. M., Wang, A. H., et al., “Identification of a functional connectome for long-term fear memory in mice,” PLoS Comput. Biol., 9, No. 1, el002853 (2013).

    Article  Google Scholar 

  • Zvorykina, S. V. and Anokhin, K. V., “Studies of the topography of c-fos-expressing neurons in the mouse neocortex on training to conditioned refl ex freezing,” Zh. Vyssh. Nerv. Deyat., 53, No. 4, 518–522 (2003).

    CAS  Google Scholar 

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Correspondence to K. V. Anokhin.

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Translated from Zhurnal Vysshei Nervnoi Deyatel’nosti imeni I. P. Pavlova, Vol. 66, No. 3, pp. 352–360, May–June, 2016.

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Vorob’eva, N.S., Ivashkina, O.I., Toropova, K.A. et al. Long-Term Contextual Memory in Mice: Persistence and Associability with Reinforcement. Neurosci Behav Physi 47, 780–786 (2017). https://doi.org/10.1007/s11055-017-0467-2

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  • DOI: https://doi.org/10.1007/s11055-017-0467-2

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