Environmental complexity differentially increases positive affect in a rat model of individual differences in novelty seeking.

R. Slusky; J. Garcia-Fuster; S.B. Flagel; J. Perez; W. Aldridge; S.J. Watson; H. Akil
Society for Neuroscience. 2010.


The inability to experience positive feelings or anhedonia is a central characteristic of depression. However, relatively few animal models have focused on the measurement of spontaneous positive affect or its modulation by environmental conditions. In this set of studies, we relied on rats selectively bred for differential reactivity to a novel environment to examine the genetic and environmental bases of positive affect. Bred high-responder rats (bHRs) show increased exploration in a novel environment and lower levels of anxiety compared to bred low-responder rats (bLRs). bHRs also exhibit increased risk-taking behavior, acquire drug-taking behavior more rapidly, show greater responsivity to reward-associated cues and appear "hyperdopaminergic" relative to bLRs. Rats emit frequency modulated ultrasonic vocalizations (USVs) in the 50-kHz range and it has been proposed that some of these may be a measure of positive affect. Increases in USV calls have been linked to increased activation of motivational reward circuits such as the mesolimbic dopamine system and associated with response to euphoria-inducing drugs such as amphetamine. In the current study we used these two rat lines to examine the impact of environmental complexity (EC) on USV calls. Rats in the EC group were exposed to an environment filled with toys for either 1 (acute group) or 9 (chronic group) sessions, each 30-min in duration. Rats were housed in pairs but exposed to EC in groups of six. Control groups consisted of groups of 6 rats exposed to the same cage as EC groups, but without toys. After acute exposure to EC, bHRs produced more USV calls than bLRs. Yet, following 9 exposures to EC, both groups emit the same number of USV calls. This was because extended exposure to EC increased 50-kHz calls in bLRs but decreased 50-kHz calls in bHRs. Interestingly, in bHR control groups USV calls also decreased with repeated exposure indicating that this group of animals was very prone to habituation when the context was no longer novel. By contrast, there was no change in USVs in bLR control groups over 9 exposures. This work demonstrates that inborn differences in emotional reactivity interact with environmental manipulations to determine positive responses to a complex environment. Moreover, the dynamics of these positive responses differ as a function of genetic background, with one group showing a gradual loss of positive affect while the other builds it over time. The neural correlates of USV emissions in the context of this animal model are under study, specifically focusing on levels of c-fos mRNA in the nucleus accumbens, amygdala, and mPFC.