Contributions of associative and non-associative learning to the dynamics of defensive ethograms
- Tulane Brain Institute, Tulane University, United States
- Program in Neuroscience, Tulane University, United States
- Department of Psychology, Tulane University, United States
Figures
Figure 1
Experimental design.
(A) Graphical representation of the three stages of the SCS conditioning paradigm. (B) Five SCS-shock association variants were used during conditioning. SCS, Serial compound stimulus; CD1, Conditioning Day 1; CD2, Conditioning Day 2; Ext1, Extinction Day 1; Ext2, Extinction Day 2; US, Unconditioned stimulus; ISI, Inter-stimulus interval.
Figure 2
Stimulus-evoked freezing and activity during CD2 are affected by serial compound stimulus (SCS)-shock contingency.
(A) Trial-by-trial freezing during the tone period. (B) Trial-by-trial freezing during the white noise (WN) period. (C) Trial-by-trial activity index during the tone period. (D) Trial-by-trial activity index during the WN period. (E) Average freezing during the tone period from all trials of CD2. (F) Average activity index scores during the tone period from all trials of CD2. (G) Average freezing during the WN period from all trials of CD2. (H) Average activity index scores during the WN period from all trials of CD2. (I) Baseline contextual freezing levels during CD2. (J) Differences in freezing between pre-SCS and tone periods from all trials of CD2. (K) Average activity index scores during the WN period for the PA and UN groups from all trials of CD2. (L) Average activity index scores during the WN for the PA and PA-R groups from all trials of CD2. PA: n=32, UN: n=20, PA-R: n=10, UN-R: n=10, SO: n=20. Data from (A–D) are presented as mean ± SEM and were analyzed with two-way ANOVA. Data from (E–J) are presented as box-and-whisker plots from min to max and were analyzed with one-way ANOVA and Tukey’s post-hoc multiple comparisons test. Data from (K and L) are presented as box-and-whisker plots from min to max and were analyzed with Welch’s unpaired t-test. *p<0.05; **p<0.01; ***p<0.001; ****p<0.0001; ^p<0.05, effect of group. For both the standard and reverse SCS groups, (A, C, E and F) detail responses during the tone period, and (B, D, G and H) detail responses during the WN period.
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Figure 2—source data 1
Dataset contains behavioral measurements for Figure 2 from each individual mouse in each group, classified by sex, group, and trial where applicable.
- https://cdn.elifesciences.org/articles/90414/elife-90414-fig2-data1-v1.xlsx
Figure 3
Associative pairings of the serial compound stimulus (SCS) and shock lead to robust escape jumping during white noise (WN).
(A) The percentage of the paired (PA) group that exhibited jumping during WN on CD2. Data are distributed across 1 s bins, each coinciding with one of the ten pips of WN that occurred during each SCS presentation. (B) The cumulative distribution of jumps from 20 randomly selected subjects of the PA group across the duration of the SCS from all five trials of CD2. Empty boxes represent each 0.5 s pip of tone, filled boxes represent each 0.5 s pip of WN, and striped boxes represent the 1 s shock stimulus. The vertical dotted lines depict the onset and termination of the WN period. Total jumps per stimulus are listed above the histogram bars. (C) The percentage of the UN group that exhibited jumping during WN on CD2. Data are distributed across 1 s bins, each coinciding with one of the ten pips of WN that occurred during each SCS presentation. (D) The cumulative distribution of jumps from the UN group across the duration of the SCS from all five trials of CD2. Empty boxes represent each 0.5 s pip of tone, filled boxes represent each 0.5 s pip of WN, and striped boxes represent the 1 s shock stimulus. The vertical dotted lines depict the onset and termination of the WN period. ISI represents the period between SCS and shock. Total jumps per stimulus are listed above the histogram bars. € The distribution of jumps across the duration of the SCS from 20 randomly selected subjects of the PA group for each trial of CD2. Each dot represents a single jump event, and each tick on the x-axis represents the onset of each pip of tone or WN. The vertical dotted line depicts the onset of the WN period. (F) The distribution of jumps across the duration of the SCS from the UN group for each trial of CD2. Each dot represents a single jump event, and each tick on the x-axis represents the onset of each pip of tone or WN. The vertical dotted line depicts the onset of the WN period. (G) The percentage of the PA-R group that exhibited jumping during WN on CD2. Data are distributed across 1 s bins, each coinciding with one of the ten pips of WN that occurred during each SCS presentation. (H) The percentage of the UN-R group that exhibited jumping during WN on CD2. Data are distributed across 1 s bins, each coinciding with one of the ten pips of WN that occurred during each SCS presentation. (I) Total percentage of the cohort that jumped during WN over the whole CD2 session. (J) Total percentage of cohort that jumped to shock over the whole CD2 session.
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Figure 3—source data 1
Dataset contains cumulative behavioral measurements for Figure 3 from each group.
- https://cdn.elifesciences.org/articles/90414/elife-90414-fig3-data1-v1.xlsx
Figure 4
Associative serial compound stimulus (SCS)-shock pairings elicit darting responses to white noise (WN) during CD2.
(A) The percentage of the paired (PA) group that exhibited darting responses to WN. Data are distributed across 1 s bins, each coinciding with one of the ten pips of WN that occurred during each SCS presentation. (B) The cumulative distribution of darts from 20 randomly selected subjects of the PA group across the duration of the SCS. Empty boxes represent each 0.5 s pip of tone, filled boxes represent each 0.5 s pip of WN, and striped boxes represent the 1 s shock stimulus. The vertical dotted lines depict the onset and termination of the WN period. Total darts per stimulus are listed above the histogram. (C) The percentage of the unpaired (UN) group that exhibited darting responses during WN. Data are distributed across 1 s bins, each coinciding with one of the ten pips of WN that occurred during each SCS presentation. (D) The cumulative distribution of darts from the UN group across the duration of SCS. Empty boxes represent each 0.5 s pip of tone, filled boxes represent each 0.5 s pip of WN, and striped boxes represent the 1 s shock stimulus. The vertical dotted lines depict the onset and termination of the WN period. ISI represents the period between SCS and shock. Total darts per stimulus are listed above the histogram. (E) The distribution of darts across the duration of SCS from 20 randomly selected subjects of the PA group. Each dot represents a single dart event, and each tick on the x-axis represents the onset of each pip of tone or WN. The vertical dotted lines depict the onset of the WN period. (F) The distribution of darts across the duration of SCS from the UN group. Each dot represents a single dart event, and each tick on the x-axis represents the onset of each pip of tone or WN. The vertical dotted lines depict the onset of the WN period. (G) The total percentage of each group that jumped during WN over the whole session. (H) Average distance traveled during the preSCS period. (I) Average distance traveled during the tone period. (J), Average distance traveled during the WN period. (K) The total percentage of each group that jumped to shock over the whole session. PA: n=32, UN: n=20, PA-R: n=10, UN-R: n=10, SO: n=20. Data from (H-J) are presented as box-and-whisker plots from min to max and were analyzed with one-way ANOVA and Tukey’s post-hoc multiple comparisons test. *p<0.05; **p<0.01; ****p<0.0001.
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Figure 4—source data 1
Dataset contains cumulative behavioral measurements for Figure 4 from each group.
- https://cdn.elifesciences.org/articles/90414/elife-90414-fig4-data1-v1.xlsx
Figure 5
Tone-evoked freezing in the paired (PA) group is reduced by extinction learning.
(A) Percent freezing during the tone period for the PA, unpaired (UN), and shock-only (SO) groups. (B) Percent freezing during the tone period for the paired reverse (PA-R) and unpaired reverse (UN-R). (C) The difference in average freezing during the tone period between the first and last four-trial bins of Ext1. (D) The difference in average freezing during the tone period between the first and last 4-trial bins of Ext2. (E) The difference in average freezing between pre-serial compound stimulus (SCS) and tone periods during Ext1. (F) The difference in average freezing between pre-SCS and tone periods during Ext2. PA: n=32, UN: n=20, PA-R: n=10, UN-R: n=10, SO: n=20. Data from (A and B) are presented as Mean ± SEM and were analyzed with two-way ANOVA and Tukey’s post-hoc multiple comparisons test. Data from (C–F) are presented as box-and-whisker plots from min to max and were analyzed with one-way ANOVA and Tukey’s post-hoc multiple comparisons test. *p<0.05, **p<0.01, ***p<0.001, ****p<0.0001.
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Figure 5—source data 1
Dataset contains behavioral measurements for Figure 5 from each individual mouse in each group, classified by sex, group, and trial where applicable.
- https://cdn.elifesciences.org/articles/90414/elife-90414-fig5-data1-v1.xlsx
Figure 6
Stimulus-induced flight is associative and is partially replaced by freezing during extinction.
(A) Trial-by-trial activity during the white noise (WN) period for the paired (PA), unpaired (UN), and shock-only (SO) groups during Ext1 and Ext2. (B) Trial-by-trial activity during the WN period for the paired reverse (PA-R) and unpaired reverse (UN-R) groups during Ext1 and Ext2. (C) Difference in average speed during the WN period from the first and last four-trial bins of Ext1. (D) Difference in average speed during the WN period from the first and last four-trial bins of Ext2. (E) Trial-by-trial freezing during the WN period for all groups during Ext1 and Ext2. (F) Difference in freezing during the WN period from the first and last four-trial bins of Ext1. (G) Difference in freezing during the WN period from early and late four-trial bins of Ext2. PA: n=32, UN: n=20, PA-R: n=10, UN-R: n=10, SO: n=20. Data from (A, B and E) are presented as Mean ± SEM and were analyzed with two-way ANOVA and Tukey’s post-hoc multiple comparisons test. Data from (C, D, F and G) are presented as box-and-whisker plots from min to max and were analyzed with one-way ANOVA and Tukey’s post-hoc multiple comparisons test. #p=0.054, *p<0.05, **p<0.01, ***p<0.001.
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Figure 6—source data 1
Dataset contains behavioral measurements for Figure 6 from each individual mouse in each group, classified by sex, group, and trial where applicable.
- https://cdn.elifesciences.org/articles/90414/elife-90414-fig6-data1-v1.xlsx
Figure 7
Stimulus-evoked escape jumping and darting during extinction.
(A) The cumulative distribution of jumps from the first four trials of Ext1 for 20 randomly selected subjects from the paired (PA) group (top), the unpaired (UN) group (middle), and the shock-only (SO) group (bottom). Empty boxes represent each 0.5 s pip of tone, filled boxes represent each 0.5 s pip of white noise (WN), and the vertical dotted lines represent the onset and termination of the WN period. Total jumps per stimulus are listed above the histogram. (B) The cumulative distribution of darts from the first four trials of Ext1 for 20 randomly selected subjects from the PA group (top), the UN group (middle), and the SO group (bottom). Empty boxes represent each 0.5 s pip of tone, filled boxes represent each 0.5 s pip of WN, and the vertical dotted lines represent the onset and termination of the WN period. Total darts per stimulus are listed above the histogram. (C) The percentage of each group that exhibited jumping responses during the WN period of serial compound stimulus (SCS) per trial on Ext1. (D) The percentage of each group that exhibited darting responses to the WN period of SCS per trial on Ext1. (E) Total percentage of each cohort that jumped to WN over the whole Ext1 session. (F) Total percentage of each cohort that darted to WN over the whole Ext1 session.
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Figure 7—source data 1
Dataset contains cumulative behavioral measurements for Figure 7 from each group.
- https://cdn.elifesciences.org/articles/90414/elife-90414-fig7-data1-v1.xlsx
Figure 8
Tail rattling is a non-associative behavioral response during extinction.
(A) The percentage of each group that exhibited tail rattling to the tone. (B) The percentage of each group that exhibited tail rattling to the white noise (WN). (C) Cumulative tail rattling during tone across early and late periods of Ext1 and Ext2. (D) Cumulative tail rattling during WN across early and late periods of Ext1 and Ext2. (E) Total percentage of each cohort that tail rattled to tone during Ext1. (F) Total percentage of each cohort that tail rattled to WN during Ext1.
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Figure 8—source data 1
Dataset contains cumulative behavioral measurements for Figure 8 from each group.
- https://cdn.elifesciences.org/articles/90414/elife-90414-fig8-data1-v1.xlsx
Author response image 1
Baseline Freezing levels for all groups during the first extinction session.
Baseline period is defined as the first 180 seconds of the session, before any auditory stimulus was presented. PA, Paired; UN, Unpaired; SO, Shock Only; PA-R, Paired Reverse; UN-R, Unpaired Reverse. *p<0.05, **p<0.01, ****p<0.0001.
Author response image 2
Trial-by-trial plot of activity index during the tone period of SCS across both extinction sessions for the PA group.
SCS, Serial compound stimulus; Ext, extinction; PA, Paired.
Author response image 3
Trial-by-trial plot of activity index during the tone period of SCS across both extinction sessions for the SO group.
SCS, Serial compound stimulus; Ext, extinction; SO, Shock Only.
Videos
Video 1
Representative comparison of paired (PA) and unpaired (UN) groups’ response to serial compound stimulus (SCS) during conditioning.
The video features audio of the SCS, which consists of 10 pips of tone followed by 10 pips of white noise (WN).
Video 2
Representative comparison of paired reverse (PA-R) and unpaired reverse (UN-R) groups’ response to reverse serial compound stimulus (SCS) during conditioning.
The video features audio of the reverse SCS, which consists of 10 pips of white noise (WN) followed by 10 pips of tone.
Video 3
Representative comparison of paired (PA), unpaired (UN), and shock-only (SO) groups’ responses to the serial compound stimulus (SCS) during an early and late extinction trial of the first extinction session.
The video features audio of the SCS, which consists of 10 pips of tone followed by 10 pips of white noise (WN).
Video 4
Representative comparison of paired (PA)-R and unpaired (UN)-R groups’ responses to the reverse serial compound stimulus (SCS) during an early and late extinction trial of the first extinction session.
The video features audio of the reverse SCS, which consists of 10 pips of white noise (WN) followed by 10 pips of tone.
Tables
Table 1
Statistical analysis of sex differences in defensive behavior.
| Figure | Group | Behavioral Comparison | Statistical Test | p-value | Result |
|---|---|---|---|---|---|
| 2E | UN | Average tone-evoked % freezing | Welch’s unpaired t-test | p=0.0053 | Males froze more to tone than females in CD2 |
| 2F | UN | Average tone-evoked activity index score | Welch’s unpaired t-test | p=0.0178 | Males had higher activity to tone compared to females in CD2 |
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Contributions of associative and non-associative learning to the dynamics of defensive ethograms
eLife 12:RP90414.
https://doi.org/10.7554/eLife.90414.3
