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.

Adolescent binge ethanol exposure alters specific forebrain cholinergic cell populations and leads to selective functional deficits in the prefrontal cortex

“…Additionally, although our model did not employ an adult comparison group, previous studies have indicated the structural and functional deficits following intermittent binge EtOH exposure are an adolescent- specific phenomenon (Spear, 2011; Vetreno et al, 2014; Vetreno and Crews, 2015; Crews et al, 2016; Doremus-Fitzwater and Spear, 2016). Previous studies have found that regardless of potential age- related declines in cognition, binge EtOH exposure during adulthood does not typically lead to cognitive flexibility deficits (Coleman et al, 2014; Gass et al, 2014).…”

“…Alcohol exposure during adolescence has been tied to drug abuse vulnerability, as well as disruptions in cognitive functioning (DeWit et al, 2000; Jacobus and Tapert, 2013; Lisdahl et al, 2013). In rodents, exposure to ethanol (EtOH) during early adolescence has been linked to decreased behavioral inhibition and impairments in behavioral flexibility that are sustained into adulthood (Coleman et al, 2014; Gass et al, 2014; Doremus-Fitzwater and Spear, 2016). This distinctive behavioral phenotype results from sustained neural changes in critical brain regions such as the prefrontal cortex (Floresco et al, 2008; Fernandez et al, 2016; Vargas et al, 2014; Liu and Crews, 2015).…”

Sex-specific enhancement of palatability-driven feeding in adolescent rats

“…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.…”

“…A tendency to assign greater value to reward stimuli may partially contribute to these exaggerated levels of risky reward-seeking behaviors [4, 6]. Greater sensitivity to orosensory reward in adolescent male rats compared to adolescent female rats is interesting, particularly given reports of sex differences in human adolescent risk taking, in which boys tend to be more willing to accept risk than girls [72, 73].…”

Reduced sensitivity to reinforcement in adolescent compared to adult Sprague-Dawley rats of both sexes

“…Specifically, it has been hypothesized that adolescents are hypersensitive to rewards and that this characteristic of motivated behavior is one of the factors that contributes to heightened vulnerability to developing substance use disorders (Casey et al 2008;Doremus-Fitzwater and Spear 2016;Spear 2000;Steinberg, 2010).…”