1. Neuroscience
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'Online' integration of sensory and fear memories in the rat medial temporal lobe

  1. Francesca S Wong
  2. R Fred Westbrook
  3. Nathan M Holmes  Is a corresponding author
  1. University of New South Wales, Australia
Research Article
Cite this article as: eLife 2019;8:e47085 doi: 10.7554/eLife.47085
6 figures and 1 additional file

Figures

Demonstration of sensory preconditioned fear.

(A) Schematic of the behavioral protocol used for the group of interest (Group PP) in Experiment 1, and in all subsequent experiments (Group PP, n = 13; Group PU, n = 16; and Group UP, n = 16). It is important to note that the sound and light were fully counterbalanced across the preconditioned and conditioned stimulus identities in this experiment and all subsequent experiments. For convenience of explanation, the designs are described with reference to one half of the counterbalancing. (B) Percentage freezing to the preconditioned sound (left panel) and to the conditioned light (right panel), averaged across the eight trials of their respective tests. It is also important to note that the level of freezing to the preconditioned sound is never as high as the level of freezing to the directly conditioned light (see Holmes et al., 2013; Holmes et al., 2018; Parkes and Westbrook, 2010). For this reason, we avoid drawing direct comparisons between the preconditioned sound and directly conditioned light, and use y-axis scales that most effectively show the key findings. Data shown are means ± SEM. They were analyzed using sets of planned orthogonal contrasts (Hays, 1963). For test levels of freezing to the sound, the first contrast compared Group PP versus the weighted average of Groups PU and UP; and the second contrast compared Group PU versus Group UP. For test levels of freezing to the light, the first contrast compared Group PU (no light-shock pairings) versus the weighted average of Groups UP and PP (both received light-shock pairings); and the second contrast compared Group UP versus Group PP. Cohen’s d (d) is shown for statistically significant results. For raw data, see the Figure 1—source data 1.

https://doi.org/10.7554/eLife.47085.002
Figure 1—source data 1

Demonstration of sensory preconditioned fear.

https://doi.org/10.7554/eLife.47085.003
Protein synthesis in the PRh is required for consolidation of a sensory sound-light memory.

(A) Schematic of the behavioral procedure for Experiment 2 (Group VEH, n = 8; and Group CHX, n = 10). The red arrow indicates infusions occurred immediately after stage 1 training. (B) Percentage freezing to the preconditioned sound (left panel) and to the conditioned light (right panel), averaged across the eight trials of their respective tests. Data shown are means ± SEM, and Cohen’s d (d) for statistically significant results (contrasts used to compare Group VEH versus Group CHX). For raw data, see the Figure 2—source data 1.

https://doi.org/10.7554/eLife.47085.004
Figure 2—source data 1

Protein synthesis in the PRh is required for consolidation of a sensory sound-light memory.

https://doi.org/10.7554/eLife.47085.005
Illustration of the two possible mechanisms underlying integration of the sound-light memory formed in stage 1 and the light-shock memory formed in stage 2.

(A) The first possibility is that the memories are integrated ‘online’ during training. When the subject is exposed to light-shock pairings in stage 2, presentation of the light triggers retrieval of its past associate, the sound, thereby allowing it to enter into an association with the shock. Test presentations of the sound then retrieve this mediated sound-shock association, and thus, elicit fear. (B) The second possibility is that the memories are integrated at the time of testing (‘memory chaining’). According to this account, the sound-light memory (stage 1) and the light-shock memory (stage 2) are formed independently of each other. It is at the point of testing, when the sound is once again encountered, that the subject retrieves the initial sound-light memory and integrates (or chains) it with the light-shock memory; thus, the sound elicits fear.

https://doi.org/10.7554/eLife.47085.006
The PRh supports online integration of the sound-light and light-shock memories.

(A) Behavioral procedure for Experiment 3 (Group VEH, n = 8; Group PRE-BUP, n = 6; and Group POST-BUP, n = 8). The red arrows indicate that the infusions of bupivacaine (BUP) or vehicle (VEH) occurred either before stage 2 or after stage 2. (B) Percentage freezing to the preconditioned sound (left panel) and to the conditioned light (right panel), averaged across the eight trials of their respective tests. Data shown are means ± SEM. The levels of freezing in both tests were analyzed using a set of planned orthogonal contrasts (Hays, 1963). The first contrast compared Group VEH versus the weighted average of Groups PRE-BUP and POST-BUP; and the second contrast compared Group PRE-BUP versus Group POST-BUP. Cohen’s d (d) is shown for statistically significant results. (C) Schematic of the behavioral procedure for Experiment 4 (Group VEH, n = 6; and Group CHX, n = 6). The red arrow indicates the infusions occurred immediately after stage 2. (D) Percentage freezing to the preconditioned sound (left panel) and to the conditioned light (right panel), averaged across the eight trials during their respective tests. Data shown are means ± SEM, and Cohen’s d (d) for statistically significant results. It is worth noting that the level of freezing to the sound in each of the treatment groups was not significantly different from the baseline (Fs < 1). We take this result to mean that the infusion of bupivacaine or cycloheximide into the PRh before/after stage 2 training completely blocked formation of the mediated sound-shock association. For raw data, see the Figure 4—source data 1.

https://doi.org/10.7554/eLife.47085.007
Figure 4—source data 1

The PRh supports online integration of the sound-light and light-shock memories.

https://doi.org/10.7554/eLife.47085.008
Neuronal activity in the PRh is required for expression of fear to the preconditioned sound, but not the conditioned light.

(A) Schematic of the procedure for Experiment 5 (Group VEH, n = 10; Group CHX, n = 7; and Group BUP, n = 7). The red arrows indicate that infusions occurred before the test for the sensory preconditioned sound and before the test for the conditioned light. (B) Percentage freezing to the preconditioned sound (left panel) and to the conditioned light (right panel), averaged across the eight trials of their respective tests. Data shown are means ± SEM. The levels of freezing in both tests were analyzed using a set of planned orthogonal contrasts (Hays, 1963). The first contrast compared Group BUP versus the weighted average of Groups VEH and CHX (both of which were expected to show fear); and the second contrast compared Group VEH versus Group CHX. Cohen’s d (d) is shown for statistically significant results. For raw data, see the Figure 5—source data 1.

https://doi.org/10.7554/eLife.47085.009
Figure 5—source data 1

Neuronal activity in the PRh is required for expression of fear to the preconditioned sound, but not the conditioned light.

https://doi.org/10.7554/eLife.47085.010
Cannula placements in the PRh taken from rats in Experiments 2–5.

The most ventral portion of the cannulas are marked on coronal sections based on the atlas of Paxinos and Watson (2006).

https://doi.org/10.7554/eLife.47085.011

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