Reward-centricity and attenuated aversions: An adolescent phenotype emerging from studies in laboratory animals

Abstract

Adolescence is an evolutionarily conserved developmental period, with neural circuits and behaviors contributing to the detection, procurement, and receipt of rewards bearing similarity across species. Studies with laboratory animals suggest that adolescence is typified by a "reward-centric" phenotype-an increased sensitivity to rewards relative to adults. In contrast, adolescent rodents are reportedly less sensitive to the aversive properties of many drugs and naturally aversive stimuli. Alterations within the mesocorticolimbic dopamine and endocannabinoid systems likely contribute to an adolescent reward-sensitive, yet aversion-resistant, phenotype. Although early hypotheses postulated that developmental changes in dopaminergic circuitry would result in a "reward deficiency" syndrome, evidence now suggests the opposite: that adolescents are uniquely poised to seek out hedonic stimuli, experience greater "pleasure" from rewards, and consume rewarding stimuli in excess. Future studies that more clearly define the role of specific brain regions and neurotransmitter systems in the expression of behaviors toward reward- and aversive-related cues and stimuli are necessary to more fully understand an adolescent-proclivity for and vulnerability to rewards and drugs of potential abuse.

Keywords: Adolescent; Aversion; Behavior; Neurobiology; Rat; Reward.

Figure 1

Data representing alcohol consumption in both humans and rats are shown. When reporting number of drinks per drinking occasion (A), a developmental decline in alcohol intake from adolescence (12–20 years), to late adolescence (21–26), to adulthood (26+) was observed. Data are collapsed across gender and are adapted from the report to Congress on the “Prevention and Reduction of Underage Drinking,” U.S. Department of Health and Human Services, 2011. (B) When examining average daily alcohol (ethanol) consumption (as measured using a continuous-access, 2-bottle choice between water and sweetened ethanol) in adolescent (postnatal day 23–33) and adult (postnatal day 60–70) Sprague-Dawley rats, adolescents, similar to their human counterparts, were found to drink significantly more ethanol than adults. The data shown in panel B are collapsed across sex, as well as across 10 days of ethanol access, and are adapted from Doremus et al. (2005).

Figure 2

Using a conditioned taste aversion (CTA) paradigm, the aversive properties of acute ethanol exposure were examined in both adolescent and adult male Sprague-Dawley rats across a dose range from 0 – 2.0 g/kg in adolescents and 0 – 1.5 g/kg in adults. When tested in a non-social context (A), adolescents exhibited significant CTA to the saccharin test solution only at the highest dose of 2.0 g/kg ethanol. Testing in a social context (B), however, eliminated the acute ethanol-induced CTA to even this dose of ethanol among adolescents. Adults demonstrated significant CTA to ethanol at doses that were insufficient to induce ethanol CTA in adolescents, with adults receiving ethanol exposure in both a non-social (C) and social (D) context showing significant ethanol CTA after 1.0 and 1.5 g/kg ethanol. Data represent the mean for each experimental group, plus and minus the standard error of the mean (SEM). Asterisks denote a significant difference from the saline control group (0 g/kg ethanol) within each Age and Testing Context condition. Data are adapted from Vetter-O’Hagen et al. (2009).