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Research ArticleNew Research, Cognition and Behavior

Danger Changes the Way the Mammalian Brain Stores Information About Innocuous Events: A Study of Sensory Preconditioning in Rats

Nathan M. Holmes, Mukesh Raipuria, Omar A. Qureshi, Simon Killcross and Fred Westbrook
eNeuro 2 January 2018, 5 (1) ENEURO.0381-17.2017; https://doi.org/10.1523/ENEURO.0381-17.2017
Nathan M. Holmes
School of Psychology, University of New South Wales, Sydney, New South Wales 2052, Australia
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Mukesh Raipuria
School of Psychology, University of New South Wales, Sydney, New South Wales 2052, Australia
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Omar A. Qureshi
School of Psychology, University of New South Wales, Sydney, New South Wales 2052, Australia
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Simon Killcross
School of Psychology, University of New South Wales, Sydney, New South Wales 2052, Australia
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Fred Westbrook
School of Psychology, University of New South Wales, Sydney, New South Wales 2052, Australia
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  • Figure 1.
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    Figure 1.

    Experiment 1. The neural substrates involved in consolidation of a sensory preconditioned association depend on the context. The mean (±SEM) levels of freezing in groups control (n = 7), safe-BLA-bupi (n = 8), safe-PRh-bupi (n = 8), danger-BLA-bupi (n = 8), and danger-PRh-bupi (n = 8) during test presentations of S2 (left panel) and S1 (right panel) in experiment 1, relative to the baseline. When sensory preconditioning occurred in a safe context, consolidation of the S2-S1 memory required neuronal activity in the PRh but not the BLA; but when it occurred in a dangerous context, consolidation of the same memory required neuronal activity in the BLA but not the PRh. There was no evidence in any protocol that an infusion of bupivacaine impaired the encoding and/or storage of the S1-shock association. Horizontal arrows in the design schematic (top of figure) indicate transitions between experimental stages, and the vertical arrow indicates an infusion of bupivacaine or vehicle into the PRh or BLA.

  • Figure 2.
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    Figure 2.

    Experiment 2. The role of AMPA receptors and MAPK signaling in consolidation of an S2-S1 memory. The mean (±SEM) levels of freezing during test presentations of S2 (left panel) and S1 (right panel) in experiments 2A (top row) and 2B (bottom row), relative to the baseline. Experiment 2A: when sensory preconditioning occurred in a safe context, consolidation of the S2-S1 memory required activation of AMPA receptors and MAPK signaling in the PRh [groups vehicle (n = 12), NBQX (n = 8), and U0126 (n = 8)]. Experiment 2B: when sensory preconditioning occurred in a dangerous context, consolidation of the S2-S1 memory required activation of AMPA receptors and MAPK signaling in the BLA [groups vehicle (n = 15), NBQX (n = 8), and U0126 (n = 7)]. Horizontal arrows in the design schematics indicate transitions between experimental stages, and the vertical arrows indicate an infusion of NBQX, U0126 or vehicle into the PRh or BLA.

  • Figure 3.
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    Figure 3.

    Experiment 3. Experience of danger shortly after a learning event changes how the brain stores information about that event. The mean (±SEM) levels of freezing during test presentations of S2 (left panel) and S1 (right panel) in experiments 3A (top row) and 3B (bottom row), relative to the baseline. Experiment 3A: a shocked exposure to the context after sensory preconditioning renders consolidation of the S2-S1 memory independent of neuronal activity in the PRh [groups vehicle (n = 8), danger-Bupi (n = 10), and safe-Bupi (n = 10)]. Experiment 3B: a shocked exposure to the context after sensory preconditioning renders consolidation of the S2-S1 memory dependent on neuronal activity in the BLA. This engagement of the BLA requires that the shocked context exposure occurs immediately after sensory preconditioning. Under these circumstances, the effect of the shocked context exposure is blocked when the BLA is inactivated before the shock [groups vehicle (n = 19), Bupi-shock-10 (n = 7) and shock-Bupi-10 (n = 7), and shock-Bupi-24 (n = 11)]. Horizontal arrows in the design schematics indicate transitions between experimental stages, and the vertical arrows indicate an infusion of bupivacaine or vehicle into the PRh or BLA.

  • Figure 4.
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    Figure 4.

    Experiment 4. The role of AMPA receptors and MAPK signaling in consolidation of an S2-S1 memory. The mean (±SEM) levels of freezing during test presentations of S2 (left panel) and S1 (right panel) in experiment 4, relative to the baseline. When danger is experienced shortly after sensory preconditioning, consolidation of the S2-S1 memory requires activation of AMPA receptors and MAPK signaling in the BLA. Groups vehicle (n = 15), NBQX (n = 8), and U0126 (n = 8). Horizontal arrows in the design schematic indicate transitions between experimental stages, and the vertical arrow indicates an infusion of NBQX, U0126 or vehicle into the BLA.

  • Figure 5.
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    Figure 5.

    Approximate placements of microinfusion cannulas in the BLA for 124 rats (left) and PRh (right) for 76 rats. The cannula locations were verified on Nissl-stained coronal sections with reference to the atlas of Paxinos and Watson (1997; p 145).

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Danger Changes the Way the Mammalian Brain Stores Information About Innocuous Events: A Study of Sensory Preconditioning in Rats
Nathan M. Holmes, Mukesh Raipuria, Omar A. Qureshi, Simon Killcross, Fred Westbrook
eNeuro 2 January 2018, 5 (1) ENEURO.0381-17.2017; DOI: 10.1523/ENEURO.0381-17.2017

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Danger Changes the Way the Mammalian Brain Stores Information About Innocuous Events: A Study of Sensory Preconditioning in Rats
Nathan M. Holmes, Mukesh Raipuria, Omar A. Qureshi, Simon Killcross, Fred Westbrook
eNeuro 2 January 2018, 5 (1) ENEURO.0381-17.2017; DOI: 10.1523/ENEURO.0381-17.2017
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Keywords

  • amygdala
  • associative learning
  • consolidation
  • danger
  • memory
  • sensory preconditioning

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