Frontostriatal activity and connectivity increase during proactive inhibition across adolescence and early adulthood

Abstract

During adolescence, functional and structural changes in the brain facilitate the transition from childhood to adulthood. Because the cortex and the striatum mature at different rates, temporary imbalances in the frontostriatal network occur. Here, we investigate the development of the subcortical and cortical components of the frontostriatal network from early adolescence to early adulthood in 60 subjects in a cross-sectional design, using functional MRI and a stop-signal task measuring two forms of inhibitory control: reactive inhibition (outright stopping) and proactive inhibition (anticipation of stopping). During development, reactive inhibition improved: older subjects were faster in reactive inhibition. In the brain, this was paralleled by an increase in motor cortex suppression. The level of proactive inhibition increased, with older subjects slowing down responding more than younger subjects when anticipating a stop-signal. Activation increased in the right striatum, right ventral and dorsal inferior frontal gyrus, and supplementary motor area. Moreover, functional connectivity during proactive inhibition increased between striatum and frontal regions with age. In conclusion, we demonstrate that developmental improvements in proactive inhibition are paralleled by increases in activation and functional connectivity of the frontostriatal network. These data serve as a stepping stone to investigate abnormal development of the frontostriatal network in disorders such as schizophrenia and attention-deficit hyperactivity disorder.

Neural correlates of response inhibition in children with attention-deficit/hyperactivity disorder: A controlled version of the stop-signal task

“…Although task instructions clearly stated that control trials did not require a response, their infrequency compared to go trials could have triggered partial inhibition, comparable to a nogo trial in a GNG task. The successful inhibition contrast showed activation in key motor inhibition areas, but effects in other brain areas, especially basal ganglia nuclei such as the striatum (Zandbelt and Vink, 2010;Vink et al, 2014), could have been diminished; although this could also be the result of the cluster-size thresholding method, which may be less likely to show smaller activation areas. Future study designs of the stop task could use a neutral stimulus in the control condition to reduce the go/no-go inhibition effect.…”

DRD2 Schizophrenia-Risk Allele Is Associated With Impaired Striatal Functioning in Unaffected Siblings of Schizophrenia Patients

“…That is, if the height of striatal activation would reflect only inhibitory processing, then our results would suggest striatal hyperactivation in the noncarriers during successful inhibition, as they show a significantly higher level of striatal activation compared to risk allele carriers. However, the level of activation in the noncarriers is comparable with that of healthy volunteers (scanned with the same scanner and task; 7,33 ). Rather, striatal activation during successful inhibition may in part also reflect anticipatory processing triggered by contextual cues.…”

Adolescent impatience decreases with increased frontostriatal connectivity

“…Finally, we performed several analyses to determine whether our results were selective with respect to another critical impulse control measure: response inhibition as assayed using the stop signal reaction time (SSRT) (50). It is known that there are improvements in SSRTs across adolescence (51,52), but also that behavior on this task is dependent on distinct neural pathways [i.e., inferior frontal gyrus (IFG)] from those involved in delay discounting. Consistent with previous findings, we found that SSRT decreased with age (linear: r = 0.55, P < 0.001; asymptotic: r = 0.58, P < 0.001; Fig.…”