Evaluating the rewarding nature of social interactions in laboratory animals

Abstract

Positive social interactions are essential for emotional well-being, healthy development, establishment and maintenance of adequate social structures and reproductive success of humans and animals. Here, we review the studies that have investigated whether forms of social interaction that occur in different phases of the lifespan of animals, i.e., maternal behavior, social play and sexual interaction are rewarding in rodents and non-human primates. We show that these three forms of social interaction can be used as incentive for place conditioning, lever pressing and maze learning, three setups that have been extensively used to study the rewarding properties of food and drugs of abuse and their neural underpinnings. The experience of positive social interactions during key developmental ages has profound and long-lasting effects on brain function and behavior in emotional, motivational and cognitive domains. For instance, pup interaction is more rewarding than cocaine for early postpartum dams and rats deprived of the opportunity to play during adolescence show social and cognitive impairments at adulthood. Furthermore, sexual behavior is only overtly rewarding when animals can control the rate at which the sexual interaction occurs. Last, we discuss how animal models contributed to our understanding of social reward mechanisms and its psychological components throughout development.

Fig. 1

A standard CPP apparatus consists of two conditioning compartments with distinct visual, olfactory, or tactile cues, separated by a third, neutral compartment used as a “start box” into which the animal is introduced during the test session. During conditioning, closed dividers between the compartments are used to confine the animals to the conditioning compartment. During habituation and testing, the closed dividers are replaced by dividers that contained an arched gateway, allowing the animals access to all compartments.

Fig. 2

An operant conditioning chamber is a computer-controlled box (a so-called “Skinner box”) with one or more levers that protrude from a wall and some cue lights. After pressing the lever, the animal obtains a reward, like release of food from a dispenser, infusion of a drug of abuse, or opportunity for social contact (for instance, by opening of a sliding door). The animal learns the contingency between lever pressing and reward delivery and, when placed again in the box, it is likely to press the lever again to obtain the reward.

Fig. 3

The T-maze is shaped like a T. The experimental animal is placed in a start box at the base of the T and, following a short delay, it is allowed to explore the maze and choose to enter either the right or left arm. A reward may be placed in one arm of the maze, or different rewards may be placed in each arm.