Date Published: July 14, 2017
Publisher: Public Library of Science
Author(s): Andrew T. Marshall, Angela T. Liu, Niall P. Murphy, Nigel T. Maidment, Sean B. Ostlund, Jeff A Beeler.
It has been hypothesized that brain development during adolescence perturbs reward processing in a way that may ultimately contribute to the risky decision making associated with this stage of life, particularly in young males. To investigate potential reward dysfunction during adolescence, Experiment 1 examined palatable fluid intake in rats as a function of age and sex. During a series of twice-weekly test sessions, non-food-deprived rats were given the opportunity to voluntarily consume a highly palatable sweetened condensed milk (SCM) solution. We found that adolescent male, but not female, rats exhibited a pronounced, transient increase in SCM intake (normalized by body weight) that was centered around puberty. Additionally, adult females consumed more SCM than adult males and adolescent females. Using a well-established analytical framework to parse the influences of reward palatability and satiety on the temporal structure of feeding behavior, we found that palatability-driven intake at the outset of the meal was significantly elevated in adolescent males, relative to the other groups. Furthermore, although we found that there were some group differences in the onset of satiety, they were unlikely to contribute to differences in intake. Experiment 2 confirmed that adolescent male rats exhibit elevated palatable fluid consumption, relative to adult males, even when a non-caloric saccharin solution was used as the taste stimulus, demonstrating that these results were unlikely to be related to age-related differences in metabolic need. These findings suggest that elevated palatable food intake during adolescence is sex specific and driven by a fundamental change in reward processing. As adolescent risk taking has been hypothesized as a potential result of hypersensitivity to and overvaluation of appetitive stimuli, individual differences in reward palatability may factor into individual differences in adolescent risky decision making.
Adolescence is associated with a heightened propensity for substance abuse and other risky behaviors [1–4], a phenomenon that seems to be particularly apparent in males . It is widely believed that this penchant for risk taking is the product of an ontogenetic change in reward processing [3, 6]. While there is some evidence that reward processing may actually be attenuated during adolescence (e.g., [3, 7]), the majority of recent studies support what is essentially the opposite view: that adolescents engage in risky behavior because they overvalue rewarding stimuli (e.g., ). For example, not only do adolescent rats exhibit suboptimal decision making  and greater willingness to exert effort for palatable food rewards relative to adults [9, 10], they also exhibit elevated consumption of palatable food  and increased hedonic taste reactivity to palatable food stimuli .
The results of Experiment 1 indicate that adolescent males, but not adolescent females, exhibit a transient elevation in palatable food intake and demonstrate that this effect is likely related to a heightened sensitivity to orosensory reward and not a resistance to satiety. While the sex specificity of this result may be influenced by sex differences in age relative to puberty at testing, the results of Experiment 1 do illuminate potential mechanisms for maladaptive reward-seeking behavior in adolescents (i.e., greater hedonic value attributed to reward) (see ).
Individual differences in palatable reward consumption has become a particularly important area of study, given the prevalence of obesity in the United States  and a rising prevalence among children . Both drug addiction and obesity have been suggested to involve similar neurobiological substrates, and may be driven by stronger preferences for or sensitivities to reward [6, 59]. Accordingly, greater reward sensitivity in adolescents may facilitate engagement in maladaptive behaviors. Also, differential exposure to sucrose during adolescence may have strong impacts on behavior in adulthood [60, 61]. As described above, adolescent risk taking may be driven by adolescent hypersensitivity to and overvaluation of appetitive stimuli . Accordingly, greater understanding of adolescent reward processing (e.g., reward palatability) relative to that of adults has potential implications for future age- and sex-dependent treatments to alleviate any elevated propensities for risk-taking behaviors .