Training-induced changes in inhibitory control network activity

Abstract

Despite extensive research on inhibitory control (IC) and its neural systems, the questions of whether IC can be improved with training and how the associated neural systems change are understudied. Behavioral evidence suggests that performance on IC tasks improves with training but that these gains do not transfer to other tasks, and almost nothing is known about how activation in IC-related brain regions changes with training. Human participants were randomly assigned to receive IC training (N = 30) on an adaptive version of the stop-signal task (SST) or an active sham-training (N = 30) during 10 sessions across 3 weeks. Neural activation during the SST before and after training was assessed in both groups using functional magnetic resonance imaging. Performance on the SST improved significantly more in the training group than in the control group. The pattern of neuroimaging results was consistent with a proactive control model such that activity in key parts of the IC network shifted earlier in time within the trial, becoming associated with cues that anticipated the upcoming need for IC. Specifically, activity in the inferior frontal gyrus decreased during the implementation of control (i.e., stopping) and increased during cues that preceded the implementation of IC from pretraining to post-training. Also, steeper behavioral improvement in the training group correlated with activation increases during the cue phase and decreases during implementation in the dorsolateral prefrontal cortex. These results are the first to uncover the neural pathways for training-related improvements in IC and can explain previous null findings of IC training transfer.

Figures

Figure 1.

Behavioral improvement as a function of training. a, The significant group–time interaction on SSRT at the baseline and endpoint session for the training and sham-training groups (F(1,58) = 4.76, p < 0.05). Error bars indicate 2 SEs around the mean. b, The significant negative linear slope of SSRT across training sessions within the training group (with 95% confidence interval, dashed lines; F(1,29) = 7.17, p < 0.05). Dashed curves indicate 95% confidence interval around the linear regression line.

Figure 2.

The IC network as identified by the correct stop > correct go contrast at baseline. The image shows the activation for the training group in yellow, the sham-training group in red, and the overlap in orange. Contrast thresholded at FWE rate of 0.05 as implemented in SPM8.

Figure 3.

The group–time interaction in the right IFG during the cue phase. The right IFG showed greater increases immediately preceding each trial from pretraining to post-training in the training group compared with the sham-training group.

Figure 4.

Simple effects of time (from pretraining to post-training) in the training group during the preparation (cue) phase (left side) and implementation (stopping) phase (right side). Increases over time are shown on the top and decreases are on the bottom. Activation in supramarginal gyrus increased during preparation and decreased during implementation, along with ACC/preSMA, right IFG, and rMFG. Conversely, activation in putamen decreased during preparation and increased during implementation. Asterisk indicates cluster that emerged at a slightly lower threshold but was significant at the default threshold in the whole-sample (N = 60) mask.

Figure 5.

Simple effect of group (training group > sham-training) at the endpoint session following training during the preparation (cue) phase. The training group showed greater activation in right IFG at endpoint than the sham-training group, and increased to a greater extent over time.

Figure 6.

Regions where activity was moderated by the effectiveness of training as measured by the linear slope of SSRT across training sessions. Greater training effectiveness (i.e., steeper negative slopes) were associated with increased activation in DLPFC during preparation (left) and decreased activation during implementation (right).