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Research ArticleNew Research, Cognition and Behavior

Subthreshold Fear Conditioning Produces a Rapidly Developing Neural Mechanism that Primes Subsequent Learning

Kehinde E. Cole, Jessica Lee, Michael Davis and Ryan G. Parsons
eNeuro 20 June 2019, 6 (3) ENEURO.0113-19.2019; DOI: https://doi.org/10.1523/ENEURO.0113-19.2019
Kehinde E. Cole
1Department of Psychology, Stony Brook University, Stony Brook, NY 11794
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Jessica Lee
1Department of Psychology, Stony Brook University, Stony Brook, NY 11794
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Michael Davis
2Department of Psychiatry and Behavioral Sciences, Emory University, Atlanta, GA 30329
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Ryan G. Parsons
1Department of Psychology, Stony Brook University, Stony Brook, NY 11794
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Abstract

Learning results in various forms of neuronal plasticity that provide a lasting representation of past events, and understanding the mechanisms supporting lasting memories has been a primary pursuit of the neurobiological study of memory. However, learning also alters the capacity for future learning, an observation that likely reflects its adaptive significance. In the laboratory, we can study this essential property of memory by assessing how prior experience alters the capacity for subsequent learning. Previous studies have indicated that while a single weak fear conditioning trial is insufficient to support long-term memory (LTM), it can facilitate future learning such that another trial delivered within a protracted time window results in a robust memory. Here, we sought to determine whether or not manipulating neural activity in the basolateral amygdala (BLA) using designer receptors exclusively activated by designer drugs (DREADDs) during or after the initial learning trial would affect the ability of the initial trial to facilitate subsequent learning. Our results show that inhibiting the BLA in rats prior to the first trial prevented the ability of that trial to facilitate learning when a second trial was presented the next day. Inhibition of the BLA immediately after the first trial using DREADDs was not effective, nor was pharmacological inhibition of protein kinase A (PKA) or the mitogen-activated protein kinase (MAPK). These findings indicate that the neural mechanisms that permit an initial subthreshold fear conditioning trial to alter later learning develop rapidly and do not appear to require a typical post-learning consolidation period.

  • amygdala
  • conditioning
  • fear
  • memory
  • metaplasticity
  • priming

Footnotes

  • The authors declare no competing financial interests.

  • This work was supported by the Stony Brook University and by National Institutes of Health Grants R37 MH047840 (to M.D.) and F32 MH090700 (to R.G.P.).

This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license, which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.

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eneuro: 6 (3)
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Subthreshold Fear Conditioning Produces a Rapidly Developing Neural Mechanism that Primes Subsequent Learning
Kehinde E. Cole, Jessica Lee, Michael Davis, Ryan G. Parsons
eNeuro 20 June 2019, 6 (3) ENEURO.0113-19.2019; DOI: 10.1523/ENEURO.0113-19.2019

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Subthreshold Fear Conditioning Produces a Rapidly Developing Neural Mechanism that Primes Subsequent Learning
Kehinde E. Cole, Jessica Lee, Michael Davis, Ryan G. Parsons
eNeuro 20 June 2019, 6 (3) ENEURO.0113-19.2019; DOI: 10.1523/ENEURO.0113-19.2019
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Keywords

  • amygdala
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