Top

Published in:

Open Access 01-12-2016 | Research

Effect of context exposure after fear learning on memory generalization in mice

Authors: Ayano Fujinaka, Ruoshi Li, Masanobu Hayashi, Deependra Kumar, Gopakumar Changarathil, Keisuke Naito, Kousuke Miki, Taihei Nishiyama, Michael Lazarus, Takeshi Sakurai, Nohjin Kee, Satomi Nakajima, Szu-Han Wang, Masanori Sakaguchi

Published in: Molecular Brain | Issue 1/2016

Abstract

Background

The conditions under which memory generalization occurs are not well understood. Although it is believed that fear memory generalization is gradually established after learning, it is not clear whether experiences soon after learning affect generalization.

Results

Using a contextual fear conditioning paradigm in mice, we found that fear memory generalization occurred when mice were exposed to a familiar, unconditioned context soon after fear learning.

Conclusions

Our results suggest that the familiarity of contexts and the timing of their exposure influences memory generalization, which increases our understanding of the mechanisms of generalization.

Available only for authorised users

Dudai Y. Memory from A to Z. Oxford: Oxford University Press; 2002.

Kostek JA, Beck KD, Gilbertson MW, Orr SP, Pang KC, Servatius RJ, et al. Acquired equivalence in U.S. veterans with symptoms of posttraumatic stress: reexperiencing symptoms are associated with greater generalization. J Trauma Stress. 2014;27(6):717–20.PubMedPubMedCentralCrossRef

Lissek S, Biggs AL, Rabin SJ, Cornwell BR, Alvarez RP, Pine DS, et al. Generalization of conditioned fear-potentiated startle in humans: experimental validation and clinical relevance. Behav Res Ther. 2008;46(5):678–87.PubMedPubMedCentralCrossRef

Bowers ME, Ressler KJ. An Overview of Translationally Informed Treatments for Posttraumatic Stress Disorder: Animal Models of Pavlovian Fear Conditioning to Human Clinical Trials. Biol Psychiatry. 2015;78(5):E15–27.PubMedCrossRef

McHugh TJ, Jones MW, Quinn JJ, Balthasar N, Coppari R, Elmquist JK, et al. Dentate gyrus NMDA receptors mediate rapid pattern separation in the hippocampal network. Science. 2007;317(5834):94–9.PubMedCrossRef

Arruda-Carvalho M, Sakaguchi M, Akers KG, Josselyn SA, Frankland PW. Posttraining ablation of adult-generated neurons degrades previously acquired memories. J Neurosci. 2011;31(42):15113–27.PubMedCrossRef

Nakashiba T, Cushman JD, Pelkey KA, Renaudineau S, Buhl DL, McHugh TJ, et al. Young dentate granule cells mediate pattern separation, whereas old granule cells facilitate pattern completion. Cell. 2012;149(1):188–201.PubMedPubMedCentralCrossRef

Wang SH, Teixeira CM, Wheeler AL, Frankland PW. The precision of remote context memories does not require the hippocampus. Nat Neurosci. 2009;12(3):253–5.PubMedCrossRef

Winocur G, Moscovitch M, Sekeres M. Memory consolidation or transformation: context manipulation and hippocampal representations of memory. Nat Neurosci. 2007;10(5):555–7.PubMedCrossRef

10.

Biedenkapp JC, Rudy JW. 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. 2007;14(3):200–3.PubMedPubMedCentralCrossRef

11.

Houston FP, Stevenson GD, McNaughton BL, Barnes CA. Effects of age on the generalization and incubation of memory in the F344 rat. Learn Mem. 1999;6(2):111–9.PubMedPubMedCentral

12.

Lissek S, Bradford DE, Alvarez RP, Burton P, Espensen-Sturges T, Reynolds RC, et al. Neural substrates of classically conditioned fear-generalization in humans: a parametric fMRI study. Soc Cogn Affect Neurosci. 2014;9(8):1134–42.PubMedPubMedCentralCrossRef

13.

Xu W, Sudhof TC. A neural circuit for memory specificity and generalization. Science. 2013;339(6125):1290–5.PubMedPubMedCentralCrossRef

14.

Wiltgen BJ, Zhou M, Cai Y, Balaji J, Karlsson MG, Parivash SN, et al. The hippocampus plays a selective role in the retrieval of detailed contextual memories. Curr Biol. 2010;20(15):1336–44.PubMedPubMedCentralCrossRef

15.

Bakker A, Kirwan CB, Miller M, Stark CE. Pattern separation in the human hippocampal CA3 and dentate gyrus. Science. 2008;319(5870):1640–2.PubMedPubMedCentralCrossRef

16.

Leutgeb JK, Leutgeb S, Moser MB, Moser EI. Pattern separation in the dentate gyrus and CA3 of the hippocampus. Science. 2007;315(5814):961–6.PubMedCrossRef

17.

Wiltgen BJ, Silva AJ. Memory for context becomes less specific with time. Learn Mem. 2007;14(4):313–7.PubMedCrossRef

18.

Pole N, Neylan TC, Otte C, Henn-Hasse C, Metzler TJ, Marmar CR. Prospective prediction of posttraumatic stress disorder symptoms using fear potentiated auditory startle responses. Biol Psychiatry. 2009;65(3):235–40.PubMedPubMedCentralCrossRef

19.

Suendermann O, Ehlers A, Boellinghaus I, Gamer M, Glucksman E. Early heart rate responses to standardized trauma-related pictures predict posttraumatic stress disorder: a prospective study. Psychosom Med. 2010;72(3):301–8.PubMedPubMedCentralCrossRef

20.

Nader K, Schafe GE, Le Doux JE. Fear memories require protein synthesis in the amygdala for reconsolidation after retrieval. Nature. 2000;406(6797):722–6.PubMedCrossRef

21.

Lee JL. Memory reconsolidation mediates the strengthening of memories by additional learning. Nat Neurosci. 2008;11(11):1264–6.PubMedCrossRef

22.

Nader K, Hardt O. A single standard for memory: the case for reconsolidation. Nat Rev Neurosci. 2009;10(3):224–34.PubMedCrossRef

23.

Wang SH, Morris RG. Hippocampal-neocortical interactions in memory formation, consolidation, and reconsolidation. Annu Rev Psychol. 2010;61:49–79. C1-4.PubMedCrossRef

24.

Miserendino MJ, Sananes CB, Melia KR, Davis M. Blocking of acquisition but not expression of conditioned fear-potentiated startle by NMDA antagonists in the amygdala. Nature. 1990;345(6277):716–8.PubMedCrossRef

25.

Rodrigues SM, Schafe GE, LeDoux JE. Intra-amygdala blockade of the NR2B subunit of the NMDA receptor disrupts the acquisition but not the expression of fear conditioning. J Neurosci. 2001;21(17):6889–96.PubMed

26.

Sanders MJ, Fanselow MS. Pre-training prevents context fear conditioning deficits produced by hippocampal NMDA receptor blockade. Neurobiol Learn Mem. 2003;80(2):123–9.PubMedCrossRef

27.

Tayler KK, Lowry E, Tanaka K, Levy B, Reijmers L, Mayford M, et al. Characterization of NMDAR-Independent Learning in the Hippocampus. Front Behav Neurosci. 2011;5:28.PubMedPubMedCentralCrossRef

28.

Wang SH, Finnie PS, Hardt O, Nader K. Dorsal hippocampus is necessary for novel learning but sufficient for subsequent similar learning. Hippocampus. 2012;22(11):2157–70.PubMedCrossRef

29.

Squire LR, Davis HP. The pharmacology of memory: a neurobiological perspective. Annu Rev Pharmacol Toxicol. 1981;21:323–56.PubMedCrossRef

30.

McGaugh JL. Memory--a century of consolidation. Science. 2000;287(5451):248–51.PubMedCrossRef

31.

Moncada D, Viola H. Induction of long-term memory by exposure to novelty requires protein synthesis: evidence for a behavioral tagging. J Neurosci. 2007;27(28):7476–81.PubMedCrossRef

32.

Ballarini F, Moncada D, Martinez MC, Alen N, Viola H. Behavioral tagging is a general mechanism of long-term memory formation. Proc Natl Acad Sci U S A. 2009;106(34):14599–604.PubMedPubMedCentralCrossRef

33.

Wang SH, Redondo RL, Morris RG. Relevance of synaptic tagging and capture to the persistence of long-term potentiation and everyday spatial memory. Proc Natl Acad Sci U S A. 2010;107(45):19537–42.PubMedPubMedCentralCrossRef

34.

Blanchard RJ, Blanchard DC. Crouching as an index of fear. J Comp Physiol Psychol. 1969;67(3):370–5.PubMedCrossRef

Title: Effect of context exposure after fear learning on memory generalization in mice
Authors: Ayano Fujinaka
Ruoshi Li
Masanobu Hayashi
Deependra Kumar
Gopakumar Changarathil
Keisuke Naito
Kousuke Miki
Taihei Nishiyama
Michael Lazarus
Takeshi Sakurai
Nohjin Kee
Satomi Nakajima
Szu-Han Wang
Masanori Sakaguchi
Publication date: 01-12-2016
Publisher: BioMed Central
Published in: Molecular Brain / Issue 1/2016
Electronic ISSN: 1756-6606
DOI: https://doi.org/10.1186/s13041-015-0184-0

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Effect of context exposure after fear learning on memory generalization in mice

Abstract

Background

Results

Conclusions

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Background

Results

Conclusions

Please log in to get access to this content

Other articles of this Issue 1/2016

Regulation of LRRK2 promoter activity and gene expression by Sp1

Amyloid Precursor-Like Protein 2 deletion-induced retinal synaptopathy related to congenital stationary night blindness: structural, functional and molecular characteristics

Endothelial nitric oxide synthase: a potential therapeutic target for cerebrovascular diseases

PERK regulates Gq protein-coupled intracellular Ca2+ dynamics in primary cortical neurons

Potentiation of synaptic transmission in Rat anterior cingulate cortex by chronic itch

Magnetic nanotherapeutics for dysregulated synaptic plasticity during neuroAIDS and drug abuse