Frontostriatal maturation predicts cognitive control failure to appetitive cues in adolescents

Abstract

Adolescent risk-taking is a public health issue that increases the odds of poor lifetime outcomes. One factor thought to influence adolescents' propensity for risk-taking is an enhanced sensitivity to appetitive cues, relative to an immature capacity to exert sufficient cognitive control. We tested this hypothesis by characterizing interactions among ventral striatal, dorsal striatal, and prefrontal cortical regions with varying appetitive load using fMRI scanning. Child, teen, and adult participants performed a go/no-go task with appetitive (happy faces) and neutral cues (calm faces). Impulse control to neutral cues showed linear improvement with age, whereas teens showed a nonlinear reduction in impulse control to appetitive cues. This performance decrement in teens was paralleled by enhanced activity in the ventral striatum. Prefrontal cortical recruitment correlated with overall accuracy and showed a linear response with age for no-go versus go trials. Connectivity analyses identified a ventral frontostriatal circuit including the inferior frontal gyrus and dorsal striatum during no-go versus go trials. Examining recruitment developmentally showed that teens had greater between-subject ventral-dorsal striatal coactivation relative to children and adults for happy no-go versus go trials. These findings implicate exaggerated ventral striatal representation of appetitive cues in adolescents relative to an intermediary cognitive control response. Connectivity and coactivity data suggest these systems communicate at the level of the dorsal striatum differentially across development. Biased responding in this system is one possible mechanism underlying heightened risk-taking during adolescence.

Figure 1

Schematic of four trials within an fMRI run. In this example, calm faces are the target stimuli, for which participants should `go' by pressing a button. Happy faces are the nontarget (`nogo') stimulus, to which participants should withhold a button press. Each face was displayed for 500 ms followed by a variable intertrial interval. Words above faces in quotes are not displayed during the experiment.

Figure 2

Behavioral performance by emotion and development. Gray line represents proportion of correct hits out of total go trials; black line represents proportion of false alarms out of total no-go trials. The y axis represents the proportion of responses for happy trials adjusted for proportion of responses for calm trials.

Figure 3

A) Brain regions showing differential activity as a function of age. Activations, threshold p < 0.05, svc are rendered on a representative high resolution anatomical scan. B) Plot of activity in the ventral striatum (circled in A) response to happy faces (nogo and go conditions collapsed) relative to rest as a function of age. Adolescents show a significantly larger magnitude of activation relative to both children and adults. The left side of image corresponds to the left side of the brain.

Figure 4

A) Brain regions showing differential activity as a function of task (nogo > go). Activations, thresholded p < 0.05, whole brain corrected are rendered on a representative high resolution anatomical scan. B) Plot of activity in the right inferior frontal gyrus (circled in A) to nogo relative to go trials (happy and calm conditions collapsed) as a function of age. Increasing age predicts a linear decrease in recruitment. C) Plot of activity in A) as a function of performance. Generally worse performance (greater false alarm rate on x-axis) predicted greater recruitment for successful suppression trials (correct nogo trials collapsed across emotion) relative to go trials (collapsed across emotion). The left side of image corresponds to the left side of the brain.

Figure 5

Psychophysiological interaction results based on seed region in right inferior frontal gyrus (IFG; circled in Figure 4A). The right dorsal striatum (caudate) demonstrates significantly greater functional coupling with the right IFG during nogo relative to go trials (threshold p < 0.05, whole brain corrected and rendered on a representative high resolution anatomical scan). The left side of image corresponds to the left side of the brain.

Figure 6

Between-subjects functional coactivation results for happy nogo trials relative to happy go trials in child, adolescent, and adult participants. Labeled bubbles represent regions depicted in Figure 3 (ventral striatum), Figure 4 (right IFG) and Figure 5 (dorsal striatum). P-values represent level of between-region co-activation across participants. Dotted line: coactivation not significant; gray line: significant at p < 0.05. All correlations are positive. IFG = inferior frontal gyrus.