Skip to main content

Advertisement

Log in

Context and the renewal of conditioned taste aversion: the role of rat dorsal hippocampus examined by electrolytic lesion

  • Research Article
  • Published:
Cognitive Neurodynamics Aims and scope Submit manuscript

Abstract

An extinguished conditioned response can sometimes be restored. Previous research has shown that this renewal effect depends on the context in which conditioning versus extinction takes place. Here we provide evidence that the dorsal hippocampus is critically involved in the representation of context that underscores the renewal effect. We performed electrolytic lesions in dorsal hippocampus, before or after extinction, in a conditioned taste aversion paradigm with rats. Rats that underwent all conditioning, extinction and testing procedures in the same experimental context showed no renewal during testing in the original context. In contrast, rats that underwent extinction procedures in a different experimental context than the one in which they had acquired the conditioned response, showed a reliable renewal effect during testing in the original context. When electrolytic lesion was performed prior to extinction, the context-dependent renewal effect was disrupted. When electrolytic lesion was undertaken after extinction, we observed a complex pattern of data including the blockage of the conventional renewal effect, and the appearance of an unconventional renewal effect. The implications of these results are discussed with respect to current views on the role of the dorsal hippocampus in processing context information.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Bouton ME (1993) Context, time, and memory retrieval in the interference paradigms of Pavlovian learning. Psychol Bull 114(1):80–99

    Article  PubMed  CAS  Google Scholar 

  • Bouton ME (1994) Context, ambiguity, and classical conditioning. Psychol Sci 3(2):49–53

    Google Scholar 

  • Bouton ME, Bolles RC (1985) Context, event-memories, and extinction. In Balsam PD, Tomie A (eds) Cotext and learning, Hillsdale, NJ, Erlbaum, pp 133–166

  • Bouton ME, Westbrook RF, Corcoran KA, Maren S (2006) Contextual and temporal modulation of extinction: behavioral and biological mechanisms. Biol Psychiatry 60(4):352–360

    Article  PubMed  Google Scholar 

  • Bruchey AK, Gonzalez-Lima F (2006) Brain activity associated with fear renewal. Eur J Neurosci 24(12):3567–3577

    Article  PubMed  CAS  Google Scholar 

  • Bruchey AK, Shumake J, Gonzalez-Lima F (2007) Network model of fear extinction and renewal functional pathways. Neuroscience 145(2):423–437

    Article  PubMed  CAS  Google Scholar 

  • Buenoa JLO, Holland PC (2008) Occasion setting in Pavlovian ambiguous target discriminations. Behav Process 79(3):132–147

    Article  Google Scholar 

  • Bures J, Bermúdez-Rattoni F, Yamamoto T (1998) Conditioned taste aversion: memory of a special kind. Oxford University Press, New York

    Book  Google Scholar 

  • Corcoran KA, Maren S (2001) Hippocampal inactivation disrupts contextual retrieval of fear memory after extinction. J Neurosci 21(5):1720–1726

    PubMed  CAS  Google Scholar 

  • Corcoran KA, Maren S (2004) Factors regulating the effects of hippocampal inactivation on renewal of conditional fear after extinction. Learn Mem 11(5):598–603

    Article  PubMed  Google Scholar 

  • Frohardt RJ, Guarraci FA, Bouton ME (2000) The effects of neurotoxic hippocampal lesions on two effects of context after fear extinction. Behav Neurosci 114(2):227–240

    Article  PubMed  CAS  Google Scholar 

  • Gallo M, Roldan G, Bures J (1992) Differential involvement of gustatory insular cortex and amygdala in the acquisition and retrieval of conditioned taste aversion in rats. Behav Brain Res 52(1):91–97

    Article  PubMed  CAS  Google Scholar 

  • Herry C, Ciocchi S, Senn V, Demmou L, Müller C, Lüthi A (2008) Switching on and off fear by distinct neuronal circuits. Nature 454(7204):600–606

    Article  PubMed  CAS  Google Scholar 

  • Holland PC (1984) Differential effects of reinforcement of an inhibitory feature after serial and simultaneous feature negative discrimination training. J Exp Psychol Anim Behav Process 10(4):461–475

    Article  PubMed  CAS  Google Scholar 

  • Holland PC, Lamoureux JA, Han JS, Gallagher M (1999) Hippocampal lesions interfere with Pavlovian negative occasion setting. Hippocampus 9(2):143–157

    Article  PubMed  CAS  Google Scholar 

  • Holt W, Maren S (1999) Muscimol inactivation of the dorsal hippocampus impairs contextual retrieval of fear memory. J Neurosci 19(20):9054–9062

    PubMed  CAS  Google Scholar 

  • Jeffery KJ, Anderson MI, Hayman R, Chakraborty S (2004) A proposed architecture for the neural representation of spatial context. Neurosci Biobehav Rev 28(2):201–218

    Article  PubMed  Google Scholar 

  • Ji J, Maren S (2005) Electrolytic lesions of the dorsal hippocampus disrupt renewal of conditional fear after extinction. Learn Mem 12(3):270–276

    Article  PubMed  Google Scholar 

  • Ji J, Maren S (2007) Hippocampal involvement in contextual modulation of fear extinction. Hippocampus 17(9):749–758

    Article  PubMed  Google Scholar 

  • Kim JJ, Fanselow MS (1992) Modality-specific retrograde amnesia of fear. Science 256(5057):675–677

    Article  PubMed  CAS  Google Scholar 

  • Lamprecht R, Hazvi S, Dudai Y (1997) cAMP response element-binding protein in the amygdala is required for long- but not short-term conditioned taste aversion memory. J Neurosci 17(21):8443–8450

    PubMed  CAS  Google Scholar 

  • Neumann DL, Longbottom PL (2008) The renewal of extinguished conditioned fear with fear-relevant and fear-irrelevant stimuli by a context change after extinction. Behav Res Ther 46(2):188–206

    Article  PubMed  Google Scholar 

  • Orsini CA, Kim JH, Knapska E, Maren S (2011) Hippocampal and prefrontal projections to the basal amygdala mediate contextual regulation of fear after extinction. J Neurosci 31(47):17269–17277

    Article  PubMed  CAS  Google Scholar 

  • Paxinos G, Watson C (2005) The rat brain in stereotaxic coordinates 5th edition. Elsevier Academic Press, London, UK

  • Phillips RG, LeDoux JE (1992) Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning. Behav Neurosci 106(2):274–285

    Article  PubMed  CAS  Google Scholar 

  • Quinteroa E, Díaza E, Vargasa JP, Schmajukb N, Lópeza JC, Dela-Casaa LG (2011) Effects of context novelty vs. familiarity on latent inhibition with a conditioned taste aversion procedure. Behav Process 86(2):242–249

    Article  Google Scholar 

  • Ross RT, Holland PC (1981) Conditioning of simultaneous and serial feature-positive discriminations. Anim Learn Behav 9(3):293–303

    Article  Google Scholar 

  • Rudy JW, O’Reilly RC (2001) Conjunctive representations, the hippocampus, and contextual fear conditioning. Cogn Affect Behav Neurosci 1(1):66–82

    Article  PubMed  CAS  Google Scholar 

  • Schafe GE, Bernstein IL (1998) Forebrain contribution to the induction of a brainstem correlate of conditioned taste aversion. II. Insular (gustatory) cortex. Brain Res 800(1):40–47

    Article  PubMed  CAS  Google Scholar 

  • Selden NR, Everitt BJ, Jarrard LE, Robbins TW (1991) Complementary roles for the amygdala and hippocampus in aversive conditioning to explicit and contextual cues. Neuroscience 42(2):335–350

    Article  PubMed  CAS  Google Scholar 

  • Spector AC (1995) Gustatory function in the parabrachial nuclei: implications from lesion studies in rats. Rev Neurosci 6(2):143–175

    Article  PubMed  CAS  Google Scholar 

  • Wilson A, Brooks DC, Bouton ME (1995) The role of the rat hippocampal system in several effects of context in extinction. Behav Neurosci 109(5):828–836

    Article  PubMed  CAS  Google Scholar 

  • Yamamoto T, Fujimoto Y, Shimura T, Sakai N (1995) Conditioned taste aversion in rats with excitotoxic brain lesions. Neurosci Res 22(1):31–49

    Article  PubMed  CAS  Google Scholar 

  • Yasoshima Y, Yamamoto T (1997) Rat gustatory memory requires protein kinase C activity in the amygdala and cortical gustatory area. Neuro Report 8(6):1363–1367

    CAS  Google Scholar 

  • Zelikowsky M, Pham DL, Fanselow MS. (2011) Temporal factors control hippocampal contributions to fear renewal after extinction. Hippocampus. doi:10.1002/hipo.20954 (on line)

Download references

Acknowledgments

We thank Dr. Satoshi Fujii in Yamagata University School of Medicine for valuable discussions and advice on physiological experiments. This work was supported by MEXT: Tamagawa University GCOE program, Supported Program for the Strategic Research Foundation at Private Universities (2009–2013), and Grant-in-Aid for Scientific Research on Innovative Areas (No. 4103–21120006).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Hiroki Fujiwara.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Fujiwara, H., Sawa, K., Takahashi, M. et al. Context and the renewal of conditioned taste aversion: the role of rat dorsal hippocampus examined by electrolytic lesion. Cogn Neurodyn 6, 399–407 (2012). https://doi.org/10.1007/s11571-012-9208-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11571-012-9208-y

Keywords

Navigation