Neural Sensitivity to Absolute and Relative Anticipated Reward in Adolescents
Magnotta V (2013) Neural Sensitivity to Absolute and Relative Anticipated Reward in Adolescents. PLoS
ONE 8(3): e58708. doi:10.1371/journal.pone.0058708
Neural Sensitivity to Absolute and Relative Anticipated Reward in Adolescents
Jatin G. Vaidya 0
Brian Knutson 0
Daniel S. O'Leary 0
Robert I. Block 0
Vincent Magnotta 0
Amanda Bruce, University of Missouri-Kansas City, United States of America
0 1 Department of Psychiatry, University of Iowa Carver College of Medicine , Iowa City , Iowa, United States of America, 2 Department of Psychology, Stanford University, Stanford, California, United States of America, 3 Department of Radiology, University of Iowa Carver College of Medicine , Iowa City , Iowa, United States of America, 4 Department of Anesthesia, University of Iowa Carver College of Medicine , Iowa City, Iowa , United States of America
Adolescence is associated with a dramatic increase in risky and impulsive behaviors that have been attributed to developmental differences in neural processing of rewards. In the present study, we sought to identify age differences in anticipation of absolute and relative rewards. To do so, we modified a commonly used monetary incentive delay (MID) task in order to examine brain activity to relative anticipated reward value (neural sensitivity to the value of a reward as a function of other available rewards). This design also made it possible to examine developmental differences in brain activation to absolute anticipated reward magnitude (the degree to which neural activity increases with increasing reward magnitude). While undergoing fMRI, 18 adolescents and 18 adult participants were presented with cues associated with different reward magnitudes. After the cue, participants responded to a target to win money on that trial. Presentation of cues was blocked such that two reward cues associated with $.20, $1.00, or $5.00 were in play on a given block. Thus, the relative value of the $1.00 reward varied depending on whether it was paired with a smaller or larger reward. Reflecting age differences in neural responses to relative anticipated reward (i.e., reference dependent processing), adults, but not adolescents, demonstrated greater activity to a $1 reward when it was the larger of the two available rewards. Adults also demonstrated a more linear increase in ventral striatal activity as a function of increasing absolute reward magnitude compared to adolescents. Additionally, reduced ventral striatal sensitivity to absolute anticipated reward (i.e., the difference in activity to medium versus small rewards) correlated with higher levels of trait Impulsivity. Thus, ventral striatal activity in anticipation of absolute and relative rewards develops with age. Absolute reward processing is also linked to individual differences in Impulsivity.
-
Funding: This work was supported by an R03 grant from the National Institutes of Health (DA023442) to JGV. The funders had no role in study design, data
collection and analysis, decision to publish, or preparation of the manuscript.
Competing Interests: The authors have declared that no competing interests exist.
Adolescence is marked by a dramatic increase in risky,
impulsive behaviors that are associated with significant morbidity
and mortality [1] Individual differences on trait measures of
Impulsivity peak during adolescence and decline thereafter into
young adulthood [2,3]. Immaturities in frontal lobe executive
control systems have been posited to contribute to problems with
impulse control during adolescence [4,5]. However, shifts in the
activity of dopamine modulated incentive motivational circuitry
may additionally alter approach-oriented behaviors [6]. Animal
research, for instance, has shown that dopaminergic receptor
density in the striatum is highest during adolescence [7].
Additionally, peri-adolescent rats show greater sensitivity to
dopamine antagonists (e.g., haloperidol) but less sensitivity to
dopamine agonists than younger and older animals [8].
Many human developmental neuroimaging studies have
focused on determining whether adolescents demonstrate
hyperor hypo-sensitivity to monetary rewards compared to adults [9
13]. These studies have sometimes reported disparate findings. For
instance, using variations of the widely-used monetary incentive
delay (MID) task, Bjork and colleagues reported reduced activity
in the ventral striatum (VS) in adolescents compared to adults
during reward anticipation [9,14]. On the other hand, Galvan and
colleagues [11], using a somewhat different monetary reward task,
found evidence for adolescent hyper-activity in the VS in response
to reward outcomes. Geier and colleagues [12] using an elegantly
designed protocol that parsed distinct phases of reward processing
(reward cue assessment, response preparation/anticipation, and
behavioral response), demonstrated that the exact pattern of
developmental differences depended on the specific phase of
reward processing under exami (...truncated)