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Vicarious reward unblocks associative learning about novel cues in male rats

  1. Sander van Gurp  Is a corresponding author
  2. Jochen Hoog
  3. Tobias Kalenscher
  4. Marijn van Wingerden
  1. Social Rodent Lab, Institute of Experimental Psychology, Germany
  2. Comparative Psychology, Institute of Experimental Psychology, Heinrich-Heine-University, Germany
  3. Department of Cognitive Science and Artificial Intelligence, Tilburg School of Humanities and Digital Sciences, Tilburg University, Netherlands
Research Article
Cite this article as: eLife 2020;9:e60755 doi: 10.7554/eLife.60755
6 figures, 5 videos, 1 data set and 1 additional file

Figures

Figure 1 with 2 supplements
Behavioral apparatus, experimental timeline, and trial timeline.

(a) The PhenoTyper consisting of lower and upper compartment in which behavioral training took place is displayed in the middle. On the left, the custom made separation wall is shown with interaction windows, camera, and microphone. On the right, the right side of the PhenoTyper is displayed with the used operant devices and in both sides of the box the food cup. (b) An example experimental time line is displayed. Actor rats learn to discriminate two visual cues in the upper compartment while at a different time partner rats learned to discriminate two auditory cues in the lower compartment. In the compound phase actor and partner rat are either both rewarded (BR, aCS+/pCS+), actor rat is rewarded while the partner is not rewarded (OR, aCS+/pCS-) or both actor and partner rat are not rewarded (NR, aCS/pCS-). In the probe trials, all learned cues are presented to the actor and at a different time to the partner rat without reward. (c) Here a timeline is shown with the different components that make up a single trial throughout the discrimination learning, compound phase, and probe trials.

Figure 1—figure supplement 1
Group assignments and pellet dispenser configuration over different experiment subgroups.

The table column 1 shows the experiment subgroup names. Column 2 shows the associative learning details per subgroup. Column 3 shows the active pellet dispenser configuration during discrimination learning. Column 4 shows the active pellet dispenser configuration during social learning. Column 5 shows the group size.

Figure 1—figure supplement 2
Cue overview for each subgroup.

This table shows the cue overview for each experimental subgroup throughout the different phases of the experiment. Column 1 shows the different subgroups. Column 2 shows the cues used during discrimination learning. Column 3 shows the cues used during social learning. Column 4 shows the cues used during the probe trials.

Figure 2 with 1 supplement
Conditioning per experimental phase.

Experimental group (combined social-appetitive and social-only subgroups). (a) Percentage of time spent in food cup for discrimination learning between aCS+ and aCS- over days. (b) Percentage of time spent in food cup for the compounds BR (aCS+, pCS+), OR (aCS+, pCS-), and NR (aCS-, pCS-) over days. Control group 1 (combined inserted wall and no partner present subgroups). (c) Percentage of time spent in food cup for discrimination learning between aCS+ and aCS- over days. (d) Percentage of time spent in food cup for the compounds BR (aCS+, pCS+), OR (aCS+, pCS-), and NR (aCS-, pCS-) over days. Control group 2 (unequal outcomes). (e) Percentage of time spent in food cup for discrimination learning between aCS+ and aCS- over days. (f) Percentage of time spent in food cup for the compounds PR (aCS-, pCS+), OR (aCS+, pCS-), and NR (aCS-, pCS-) over days. Error bars indicate SEM.

Figure 2—figure supplement 1
Effect of adding a novel cue on the aCS+.

Experimental group (combined social-appetitive and social-only subgroups). (a) Comparison of the different scores during the compound phase (BR-NR, OR-NR) with the discrimination learning phase (aCS+-aCS-). (d) Comparison of the percentage time spent in the food cup of the compound phase (NR) with the discrimination learning phase (aCS-). Control group 1 (combined inserted wall and no partner present subgroups). (b) Comparison of the different scores during the compound phase (BR-NR, OR-NR) with the discrimination learning phase (aCS+- aCS-). (e) Comparison of the percentage time spent in the food cup of the compound phase (NR) with the discrimination learning phase (aCS-). Control group 2 (unequal outcomes). (c) Comparison of the different scores during the compound phase (PR-NR, OR- NR) with the discrimination learning phase (aCS+-aCS-). (f) Comparison of the percentage time spent in the food cup of the compound phase (NR) with the discrimination learning phase (aCS-).

Figure 3 with 1 supplement
Food cup response during the probe trials.

Experimental group 1 (combined social-appetitive and social-only subgroups). (a) Percentage of time spent in the food cup in the 10 s period after cue onset during extinction. (d) Percentage of time spent in the food cup in the 30 s period after cue onset (g) Food cup rate per minute in the 10 s period after cue onset. Control group 1 (combined inserted wall and no partner present subgroups). (b) Percentage of time spent in the food cup in the 10 s period during extinction after cue onset. (e) Percentage of time spent in the food cup in the 30 s period after cue onset. (h) Food cup rate per minute in the 10 s period after cue onset. Control group 2 (unequal outcomes). (c) Percentage of time spent in the food cup in the 10 s period after cue onset during extinction. (f) Percentage of time spent in the food cup in the 30 s period after cue onset. (i) Food cup rate per minute in the 10 s period after cue onset. Extinction in all groups is depicted in five bins of two trials per bin. Bar plots indicate averaged time spent in the food cup over 10 probe trials between aCS+, pCS+ (unblocked), pCS- (blocked), and aCS-. Error bars indicate SEM.

Figure 3—figure supplement 1
Latency to entry for the different groups.

(a) Experimental group (combined social-appetitive and social-only subgroups), (b) control group (combined inserted wall and no partner present subgroups) 1 (c) control group 2 (unequal outcomes). In all groups, the median latency to enter the food cup during the probe trials is shown over five bins (two trials per bin). Black dots indicate the median and bars display the interquartile range. Notched boxplot on the right display the distribution per condition over all bins. (d) Bootstrap distributions of mean latency differences between trial types pCS+ and pCS-.

Different scores of the actor rats during extinction for 10 s and 30 s data for experimental group (combined social-appetitive and social-only subgroups: E, black squares), control group 1 (combined inserted wall and no partner present subgroups: C1, gray circles) and control group 2 (unequal outcomes: C2, gray triangles).

(a, e) Different scores of the percentage of time spent in food cup in the 10 s period (a) and 30 s (e) after cue onset over six trials for the [aCS+]-[aCS-] difference scores. Bar plots show the average over trials of the [aCS+]-[aCS-] difference scores with dots showing the mean per rat. (b, f) Difference of the percentage of time spent in food cup in the 10 s (b) and 30 s (f) period after cue onset over six trials for the [pCS+]-[pCS-] difference scores. Bar plots show the average over six trials of the [pCS+]-[pCS-] difference scores with dots showing the mean per rat. (c, g) Difference of the percentage of time spent in the food cup in the 10 s (c) and 30 (g) second period after cue onset over six trials for the [pCS+]-[aCS-] difference scores. Bar plots show the average over six trials of the [pCs+]-[aCS-] difference scores with dots showing the mean per rat. (d, h) Difference of the percentage of time spent in the food cup in the 10 s (d) and 30 s period after cue onset over six trials for the [pCS-]-[aCS-] difference scores. Bar plots show average over six trials of the [pCs-]-[aCS-] difference scores with dots showing the mean per rat. Error bars indicate SEM.

Figure 4—source data 1

Strength of the social unblocking effect over trials.

https://cdn.elifesciences.org/articles/60755/elife-60755-fig4-data1-v2.xlsx
Food cup responses of the partner rat during learning.

Experimental group 1 (combined social-appetitive and social-only subgroups): (a) Percentage of time spent in the food cup during discrimination learning. (b) Percentage of time spent in the food cup during social learning. (c) Percentage of time spent in the food cup during the first six trials of the probe phase. Control group 1a (inserted wall): (d) Percentage of time spent in the food cup during discrimination learning. (e) Percentage of time spent in the food cup during social learning. (f) Percentage of time spent in the food cup during the first six trials of the probe phase. Bar plots indicate averaged time spent in the food cup over six probe trials between aCS+, pCS+ (unblocked), pCS- (blocked), and aCS-. Error bars indicate SEM.

Effect of secondary reinforcement, impeding wall and partner absence on food cup occupancy in the first 10 s after cue onset.

(a, b) Mean percentage of spent in the food cup, for the 10 s period (a) and 30 s period. (b) After cue onset for pCS+ versus pCS- for trial 1-6 for the experimental group 1 (social-appetitive and social-only) and control group 1 (wall impeded and no partner present). (c) Average cumulative food cup occupancy over six trials for the 10 s pre and post cue on for the social-appetitive group. (d) Average cumulative food cup occupancy over six trials for the 10 s pre and post cue on for the wall inserted group. (e) Average cumulative food cup occupancy over six trials for the 10 s pre and post cue on for the social-only group. (f) Average cumulative food cup occupancy over six trials for the 10 s pre and post cue on for the no partner present group. The 3D plot depicts cumulative food cup occupancy per trial per group. Error bars indicate SEM.

Videos

Video 1
Conditioned response of the actor rats during the presentation of the aCS+ on day 14 of discrimination learning.

This video shows the conditioned response of the actor rats of the social-appetitive subgroup on trial 1 day 14. Shown here are the 5 s before cue onset and the first 10 s after cue onset.

Video 2
Conditioned response of the actor and partner rats during the presentation of the BR (aCS+, pCS+) on day 4 of social learning.

This video shows the conditioned response of both the actor (top compartment) and partner (bottom compartment) rats of the social-appetitive subgroup on trial 1 day 4. Shown here are the 5 s before cue onset and the first 20 s after cue onset.

Video 3
Conditioned response of the actor and partner rats during the presentation of the OR (aCS+, pCS-) on day 4 of social learning.

This video shows the conditioned response of both the actor (top compartment) and partner (bottom compartment) rats of the social-appetitive subgroup on trial 2 day 4. Shown here are the 5 s before cue onset and the first 20 s after cue onset.

Video 4
Conditioned response of the actor rats during the presentation of the pCS+ on trial 1 of the probe trials.

This video shows the conditioned response the actor rats of the social-appetitive subgroup on trial 1 of the pCS+ during the probe trials. Shown here are the 10 s before cue onset and the first 10 s after cue onset.

Video 5
Conditioned response of the actor rats during the presentation of the pCS- on trial 1 of the probe trials.

This video shows the conditioned response the actor rats of the social-appetitive subgroup on trial 1 of the pCS- during the probe trials. Shown here are the 10 s before cue onset and the first 10 s after cue onset.

Data availability

Dryad data deposited at https://doi.org/10.5061/dryad.v9s4mw6qp.

The following data sets were generated
  1. 1
    Dryad Digital Repository
    1. S van Gurp
    2. J Hoog
    3. T Kalenscher
    4. M van Wingerden
    (2020)
    Vicarious reward unblocks associative learning about novel cues in male rats.
    https://doi.org/10.5061/dryad.v9s4mw6qp

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