Brain dynamics underlying training-induced improvement in suppressing inappropriate action

Abstract

Inhibitory control, a core component of executive functions, refers to our ability to suppress intended or ongoing cognitive or motor processes. Mostly based on Go/NoGo paradigms, a considerable amount of literature reports that inhibitory control of responses to "NoGo" stimuli is mediated by top-down mechanisms manifesting ∼200 ms after stimulus onset within frontoparietal networks. However, whether inhibitory functions in humans can be trained and the supporting neurophysiological mechanisms remain unresolved. We addressed these issues by contrasting auditory evoked potentials (AEPs) to left-lateralized "Go" and right NoGo stimuli recorded at the beginning versus the end of 30 min of active auditory spatial Go/NoGo training, as well as during passive listening of the same stimuli before versus after the training session, generating two separate 2 × 2 within-subject designs. Training improved Go/NoGo proficiency. Response times to Go stimuli decreased. During active training, AEPs to NoGo, but not Go, stimuli modulated topographically with training 61-104 ms after stimulus onset, indicative of changes in the underlying brain network. Source estimations revealed that this modulation followed from decreased activity within left parietal cortices, which in turn predicted the extent of behavioral improvement. During passive listening, in contrast, effects were limited to topographic modulations of AEPs in response to Go stimuli over the 31-81 ms interval, mediated by decreased right anterior temporoparietal activity. We discuss our results in terms of the development of an automatic and bottom-up form of inhibitory control with training and a differential effect of Go/NoGo training during active executive control versus passive listening conditions.

Figure 1.

Experimental design. Each participant completed one training session (active Go/NoGo training) as well as two sessions of passive listening before and immediately after the training sessions (passive pretraining and posttraining sessions).

Figure 2.

Active Go/NoGo training: electrical neuroimaging results. a, The AEP in response to the beginning for Go (LG, black trace) and NoGo (RNG, red) and end for Go (green) and NoGo (blue) of the experiment are displayed in microvolts as a function of time for the Cz electrode. Topographic pattern analyses identified six time periods of stable electric field topography across the collective 452 ms poststimulus period. All topographies (i.e., maps) are shown with the nasion upward and left scalp leftward. For one of these time periods (61–104 ms), multiple maps were identified in the group-averaged AEPs. These maps are framed in blue. b, The reliability of this observation at the group-averaged level was then assessed at the single-subject level using a spatial correlation fitting procedure. The GEV of each template map provides a measure across subjects of how well a given template map accounts for a given condition over the 61–104 ms time period (see Materials and Methods). Over the 61–104 ms period after stimulus, different maps (framed in dark and light blue) described AEPs in response to the Go and NoGo stimuli as a function of training (beginning/end). There was a significant three-way interaction between section, stimulus, and map. Error bars indicate SEM. c, Group-averaged distributed linear source estimations were calculated over the 61–104 ms poststimulus period for each experimental condition (scale indicated), when AEPs analyses revealed a significant topographic modulation across conditions. d, Node-wise section × stimulus ANOVA on source estimation over the 61–104 ms interval revealed significant section × stimuli interactions within a left temporoparietal cluster. e, Follow-up analyses on the mean scalar value of the ROI revealed a decrease in the left temporoparietal cortex for the NoGo stimuli as a function of training. f, Node-wise correlations between response time to Go stimuli and the activity within the cluster showing the significant section × stimulus interaction revealed that the more performance improved, the more response strength to NoGo stimuli decreased within the left temporoparietal ROI.

Figure 3.

Pretraining and posttraining passive listening: electrical neuroimaging results. a, The AEP in response to the pretraining Go (LG, black trace) and NoGo (RNG, red) and posttraining Go (green) and NoGo (blue) stimuli are displayed in microvolts as a function of time for the Cz electrode. Topographic pattern analyses identified six time periods of stable electric field topography across the collective 452 ms poststimulus period. All topographies (i.e., maps) are shown with the nasion upward and left scalp leftward. For the 31–81 ms period, multiple maps were identified in the group-averaged AEPs. These maps are framed in purple. b, The reliability of this observation at the group-averaged level was then assessed at the single-subject level using a spatial correlation fitting procedure. The GEV of each template map provides a measure across subjects of how well a given template map accounts for a given condition over the 61–104 ms time period (see Materials and Methods). Over the 31–81 ms period after stimulus, different maps (framed in dark and light purple) described AEPs in response to the Go and NoGo stimuli as a function of training (pre/post). There was a significant three-way interaction between section, stimulus, and map. Error bars indicate SEM. c, Group-averaged distributed linear source estimations were calculated over the 31–81 ms poststimulus period for each experimental condition (scale indicated), when AEPs analyses revealed a significant topographic modulation across conditions. d, Node-wise section × stimulus ANOVA on source estimation over the 31–81 ms interval revealed significant section × stimuli interactions within a right temporoparietal cluster. e, Follow-up analyses on the mean scalar value of the ROI revealed a decrease in the right temporoparietal cortex for the Go stimuli as a function of training.