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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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    Figure 1.

    LTM priming requires paired presentation of light and shock. A, Timeline of the experiment. Rats were with either a single paired trial (N = 10), two paired trials separated by 60 min (N = 13), or an unpaired trial followed by a paired trial (N = 11). B, Shock reactivity did not differ between the groups. C, Rats given two paired trials showed higher levels of fear-potentiated startle compared to both the unpaired-one trial and one trial groups; **p < 0.01 (Tukey HSD). Error bars, SEM.

  • Figure 2.
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    Figure 2.

    The ability of an initial fear conditioning trial to prime future learning depends on neural activity in the BLA. A, Timeline of the experiment. Rats were infected with AAV8-CaMKIIa-hM4Di-mCherry or AAV8-CaMKIIa-EGFP targeting the BLA. Animals were given a single fear conditioning trial, 60 min before which they received an intraperitoneal injection of CNO or vehicle. A second trial was given the following day, and memory was tested 48 h later. B, Activity during the baseline period of training did not differ between groups, nor did reactivity to the shock. C, Rats expressing the hM4Di-DREADD receptor and given CNO (N = 7) before trial 1 showed significantly less fear potentiated startle compared to hM4Di rats given vehicle (N = 8) and compared to EGFP rats given CNO (N = 6). D, **p < 0.01, *p < 0.05 (Tukey HSD). Error bars, SEM.

  • Figure 3.
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    Figure 3.

    Neural activity in the BLA after the initial trial is not required for priming of future learning. A, Timeline of the experiment. Rats were infected with AAV8-CaMKIIa-hM4Di-mCherry (N = 8) or AAV8-CaMKIIa-EGFP (N = 7) targeting the BLA. Rats were given a single fear conditioning immediately after which they received an intraperitoneal injection of CNO. A second trial was given the following day and memory was tested 48 h later. B, Activity during the baseline period of training did not differ between groups, nor did reactivity to the shock (C) during the test session, and (D) levels of fear-potentiated startle did not differ in hM4Di and EGFP rats given CNO. Error bars, SEM.

  • Figure 4.
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    Figure 4.

    Photomicrographs depicting fluorescent labeling in the BLA in rats infected with AAV8-CaMKIIa-hM4Di-mCherry (A) or AAV8-CaMKIIa-EGFP (B), for the rats included in Figures 1, 2. Lighter shade of red and green indicate the maximal extent of viral expression for hM4di (C) and EGFP (D), respectively. Darker color shapes indicate the smallest spread extent of spread for the same viruses. Rat brain atlas images are from Swanson (2004).

  • Figure 5.
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    Figure 5.

    Pharmacological inhibition of PKA or MAPK immediately after trial 1 had no effect on the priming of future learning. A, Timeline for the experiments. Rats were given infusions of the PKA inhibitor Rp-cAMPS (N = 8) or its vehicle (saline, N = 10), or the MAPK blocker U0126 (N = 8) or its vehicle (50% DMSO, N = 8), into the BLA immediately after the initial training trial. Activity during the baseline period of training did not differ between groups in either experiment (B, C), nor did reactivity to the shock (D, E). There were no differences in levels of fear-potentiated startle during the test session for either experiment (F, G). Dots indicate cannula placements for the rats included in this experiment (H). Rat brain atlas images are from Swanson (2004). Error bars, SEM.

  • Figure 6.
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    Figure 6.

    Pre-training inhibition of MAPK disrupted LTM formation. A, Timeline for the experiment. Rats were given infusions of the MAPK inhibitor U0126 (N = 9) or its vehicle (N = 13) into the BLA 30 min before training. Reactivity to the shock on either the first or second trial did not differ between groups. B, Rats given U0126 before training showed less fear-potentiated startle during the testing session. C, *p < 0.05 (t test). Error bars, SEM.

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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
  • conditioning
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