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Microtopography of fear memory consolidation and extinction retrieval within prefrontal cortex and amygdala

  • Angela Jacques
  • Nicholas Chaaya
  • Chiemi Hettiarachchi
  • Marie-Louise Carmody
  • Kate Beecher
  • Arnauld Belmer
  • Fatemeh Chehrehasa
  • Selena Bartlett
  • Andrew R. Battle
  • Luke R. JohnsonEmail author
Original Investigation
  • 141 Downloads

Abstract

Rationale

The precise neural circuitry that encodes fear memory and its extinction within the brain are not yet fully understood. Fearful memories can be persistent, resistant to extinction, and associated with psychiatric disorders, especially post-traumatic stress disorder (PTSD). Here, we investigated the microtopography of neurons activated during the recall of an extinguished fear memory, as well as the influence of time on this microtopography.

Methods

We used the plasticity-related phosphorylated mitogen-activated protein kinase (pMAPK) to identify neurons activated in the recall of consolidated and extinguished auditory Pavlovian fear memories in rats. Quantitatively matched brain regions were used to investigate activity in the amygdala and prefrontal cortex.

Results

Recall of a consolidated, nonextinguished auditory fear memory resulted in a significantly greater number of activated neurons located in the dorsolateral subdivision of the lateral amygdala (LADL) when recalled 24 h after consolidation but not when recalled 7 days later. We found that the recall of an extinction memory was associated with pMAPK activation in the ventrolateral subdivision of the lateral amygdala (LAVL). Next, we showed that the pattern of pMAPK expression in the prelimbic cortex differed spatially following temporal variation in the recall of that memory. The deep and superficial layers of the pre-limbic cortex were engaged in recent recall of a fear memory, but only the superficial layers were recruited if the recall occurred 7 days later.

Conclusions

Collectively, our findings demonstrate a functional microtopography of auditory fear memory during consolidation and extinction at the microanatomical level within the lateral amygdala and medial prefrontal cortex.

Keywords

pMAPK Topography Neuroplasticity Amygdala Medial prefrontal cortex Extinction Fear conditioning 

Notes

Acknowledgements

We gratefully acknowledge scholarship support from QUT Research Training Program [RTP] stipend. The authors wish to thank Dimitrios Vagenas for his helpful discussions and advice on statistical analysis.

Funding information

This work was financially supported by the IHBI, QUT.

Compliance with ethical standards

All procedures were conducted in compliance with the Animal Welfare Unit, The University of Queensland Research, and Innovation Ethics Committee and the Research Ethics Committee of the Queensland University of Technology, Australia. Procedures complied with policies, regulations and ethical standards for animal experimentation, in accordance with the Queensland Government Animal Research Act 2001, associated Animal Care and Protection Regulations (2002 and 2008), and the Australian Code for the Care and Use of Animals for Scientific Purposes, 8th Edition

Conflict of interest

The authors declare that they have no conflict of interest.

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Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Angela Jacques
    • 1
    • 2
  • Nicholas Chaaya
    • 1
    • 2
  • Chiemi Hettiarachchi
    • 2
  • Marie-Louise Carmody
    • 1
    • 2
  • Kate Beecher
    • 2
    • 3
  • Arnauld Belmer
    • 2
    • 3
  • Fatemeh Chehrehasa
    • 2
    • 4
  • Selena Bartlett
    • 2
    • 3
  • Andrew R. Battle
    • 2
    • 4
    • 5
  • Luke R. Johnson
    • 1
    • 2
    • 6
    Email author
  1. 1.School of Psychology and CounsellingQueensland University of TechnologyBrisbaneAustralia
  2. 2.Translational Research Institute, Institute of Health and Biomedical Innovation, Department of Psychology and CounsellingQueensland University of TechnologyBrisbaneAustralia
  3. 3.School of Clinical SciencesQueensland University of TechnologyBrisbaneAustralia
  4. 4.School of Biomedical SciencesQueensland University of TechnologyBrisbaneAustralia
  5. 5.The University of Queensland Diamantina InstituteBrisbaneAustralia
  6. 6.Center for the Study of Traumatic Stress, Department of PsychiatryUSU School of MedicineBethesdaUSA

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