Deficit in observational learning in experimental epilepsy

Abstract

Individuals use the observation of a conspecific to learn new behaviors and skills in many species. Whether observational learning is affected in epilepsy is not known. Using the pilocarpine rat model of epilepsy, we assessed learning by observation in a spatial task. The task involves a naive animal observing a demonstrator animal seeking a reward at a specific spatial location. After five observational sessions, the observer is allowed to explore the rewarded space and look for the reward. Although control observer rats succeed in finding the reward when allowed to explore the rewarded space, epileptic animals fail. However, epileptic animals are able to successfully learn the location of the reward through their own experience after several trial sessions. Thus, epileptic animals show a clear deficit in learning by observation. This result may be clinically relevant, in particular in children who strongly rely on observational learning.

Keywords: animal model; observational learning; social behavior; 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. In Step 1, the observer (red) watches the demonstrator (blue), which has been trained to remember the location of a reward hidden in one of the 12 wells. (B) Image of the experimental apparatus with the lower wall of the transparent inner box open. The reward is 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. During 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 directly explore.

FIGURE 2

Epileptic animals fail to learn by observation. The percentage of animals successfully finding the reward is displayed as a function of trials. Naive control animals (blue, n = 5) learn the location of the reward, and do not make any mistakes after a certain time. They become demonstrators. After control observers (red, n = 5) are first exposed to the rewarded space, they go straight to the reward; they have learned by observation. Epileptic observers (black, n = 5) fail to find the reward during the first exposure, but learn the task as naive control rats. Error bars are mean ± SEM. The black dashed line represents success by chance (8.3%). *p < .05, **p < .01, ***p < .001. PILO, pilocarpine.