Social Learning of a Spatial Task by Observation Alone

Abstract

Interactions between conspecifics are central to the acquisition of useful memories in the real world. Observational learning, i.e., learning a task by observing the success or failure of others, has been reported in many species, including rodents. However, previous work in rats with NMDA-receptor blockade has shown that even extensive observation of an unexplored space through a clear barrier is not sufficient to generate a stable hippocampal representation of that space. This raises the question of whether rats can learn a spatial task in a purely observed space from watching a conspecific, and if so, does this somehow stabilize their hippocampal representation? To address these questions, we designed an observational spatial task in a two-part environment that is nearly identical to that of the aforementioned electrophysiological study, in which an observer rat watches a demonstrator animal to learn the location of a hidden reward. Our results demonstrate that rats do not need to physically explore an environment to learn a reward location, provided a conspecific demonstrates where it is. We also show that the behavioral memory is not affected by NMDA receptor blockade, suggesting that the spatial representation underlying the behavior has been consolidated by observation alone.

Keywords: learning by observation; memory; social behavior; social memory; spatial memory.

Figure 1

Experimental design. (A) The experimental environment consisted of a transparent inner box and an opaque outer box. The gray areas indicate the regions explored by the tested rat. (B) Image of the experimental apparatus with the right wall of the transparent inner box open. The reward is hidden in one of the 12 wells and covered with gravel. One of the four walls of the opaque outer box is white and provides a distal cue to the animals. (C) Schematic representation of the experiment. The familiarization phase, in which the experimental animal is confined to the inner box, is followed by the observational training phase, in which it can observe the demonstrator animal navigating the outer space (blue). Finally, on the day of direct exploration, the observer animal is allowed to navigate in the observed space. One session is held daily, for a total of nine sessions (three for familiarization, five for observational training, and one for direct exploration). The red and blue areas correspond respectively to the space that the observer and demonstrator animals can physically explore.

Figure 2

Spatial memory task learned through exploratory experience. (A) Learning progress of naive rats across 15 reward retrievals (3 days) calculated as the percentage of successful animals for each trial (n = 14). Error bars are mean ± standard error of the mean (SEM). Gray dashed line represents success by chance. (B) The number of mistakes per trial by naive rats across 15 reward retrievals (n = 14). The number of mistakes is the average normalized number of mistakes made for each reward, relative to the first trial (M₁ = 2.0). ^*p < 0.05, ^***p < 0.001.

Figure 3

Spatial memory task learned by observational experience in an unexplored environment. (A) Effect of learning an unexplored space by observation by the percentage of success on the task for naive (blue) and observer animals (red) on the first direct exploration. Performance on the first direct exploration was statistically different for the observer animals compared to the naive animals (Pearson chi square = 14.44, 99.9% confidence, n naive = 16, n observer = 6). Error bars are mean ± standard error of the mean (SEM). The gray dashed line represents success by chance. (B) Effect of learning the unexplored space by observation using the average time to find the reward across trials (n naive = 17, n observer = 5). Performance on the first and second direct explorations was statistically different in the observer (red) compared with naive animals (blue; unpaired mean difference on the first reward = −1.17^*10³, 99.9% confidence; unpaired mean difference on the second reward = −1.85^*10², 95.0% confidence). Demonstrator (green) for comparison. Error bars are mean ± standard error of the mean (SEM). ^*p < 0.05, ^***p < 0.001.

Figure 4

Success on the spatial task is independent of olfactory cues. (A) Mean number of mistakes on the first trial for rewarded and unrewarded naive animals. Performance on the first direct exploration was statistically different for rewarded and non-rewarded naive animals (Pearson chi-square = 15.44, 95% confidence, n naive rewarded = 16, n naive non-rewarded = 7). Error bars are mean ± standard error of the mean (SEM). The gray dashed line represents success by chance. (B) Effect of learning an unexplored space by observation using the percentage of success in the unrewarded task for naive (blue) and observer animals (red) on the first direct exploration. Performance on the first direct exploration was statistically different for observer animals without reward (red) compared to naive animals without reward (blue; Pearson chi-square = 10.50, 99.9% confidence, n naive animals without reward = 7, n observer without reward = 8). No statistical difference was found between unrewarded observer animal control and CPP groups (n observer non-rewarded = 8, n observer non-rewarded CPP = 5). Error bars are mean ± standard error of the mean (SEM). The gray dashed line represents success by chance. ^*p < 0.05, ^***p < 0.001.