Role of oxytocin in the ventral tegmental area in social reinforcement

Abstract

The rewarding properties of social interactions play a critical role in the development and maintenance of social relationships, and deficits in social reward are associated with various psychiatric disorders. In the present study, we used a novel Operant Social Preference (OSP) task to investigate the reinforcing properties of social interactions under conditions of high or low reward value, and high or low behavioral effort in male Syrian hamsters. Further, we investigated the role of oxytocin (OT) in a key structure of the mesolimbic reward system, the ventral tegmental area (VTA), in mediating the reinforcing properties of social interaction. Adult male hamsters were placed in a three-chambered apparatus, and allowed access to either a social chamber containing an unrestrained conspecific or a non-social chamber, by pushing through a one-way entry, vertical-swing door. Increasing the duration of social interaction (reward value) decreased the frequency of entering the social interaction chambers, whereas decreasing the duration of social interaction conversely increased the frequency of entries. Moreover, increasing behavioral effort required to access social interaction decreased the frequency of entries, especially under conditions when the duration of social interaction was only 5 s. OT injected into the VTA decreased the frequency of entering social interaction chambers in a manner similar to that observed when duration was increased, whereas injection of an OT receptor antagonist in the VTA increased the frequency of seeking social interaction. Taken together, these data support the hypothesis that activation of OT receptors in the VTA are critical for the reinforcing properties of social interactions. Furthermore, social interactions may exhibit duration and cost dependent reinforcing effects on behavior similar to those observed with food and drugs of abuse.

Sex-dependent regulation of social reward by oxytocin receptors in the ventral tegmental area

“…The utility of this hypothesis for understanding social reward will depend, at least in part, on the ability to define more clearly the critical elements of the duration or intensity of social interactions that are responsible for their rewarding properties. Parametric relationships between the duration of social interactions and its rewarding properties have been identified [4] and appear to be similar to at least some of the parametric relationships between drug dose and drug reward [5,7]. In contrast, while the notion of an inverted U relationship between the intensity of social interactions and social reward is intuitively appealing, the concept of social intensity needs to be more fully developed.…”

“…The relationships between the characteristics of social interactions and their rewarding properties are not well understood. For example, only recently has it been shown that there is an inverse relationship between the reward value of social interactions and the frequency of seeking those interactions [4] that is similar to the relationship between drug seeking and the reward value of drugs (e.g., cocaine dose) [5][6][7]. In other words, the duration of social interaction is analogous to the dose or concentration dependent effects seen with drugs of abuse.…”

Role of oxytocin in the control of stress and food intake

“…193,194,202,203 Oxytocin has been shown to enhance tonic activity of dopamine neurones of the ventral tegmental area in mice. 193,194,202,203 Oxytocin has been shown to enhance tonic activity of dopamine neurones of the ventral tegmental area in mice.…”

“…On the other hand, oxytocin has been shown in laboratory rodents to facilitate social reward by acting on the ventral tegmental area or the nucleus accumbens via facilitation of dopamine release. 193,194,202,203 Oxytocin has been shown to enhance tonic activity of dopamine neurones of the ventral tegmental area in mice. 191,193 The differential actions of oxytocin to control the activity of dopamine neurones in response to addictive drugs and palatable food and to control the activity of dopamine neurones in response to social behaviour remain to be clarified.…”

Sex-dependent regulation of social reward by oxytocin: an inverted U hypothesis

“…Similarly, in a novel operant social preference test, the rewarding properties of social interactions were significantly greater in females compared to males. Specifically, hamsters were placed in a three-chambered apparatus and allowed access to either a chamber containing an unrestrained same-sex stimulus hamster or an empty chamber, accessed through one-way entry, verticalswing doors [122]. Females made about twice as many entries into the chamber containing the stimulus hamster as did males.…”