Independent component analysis of functional networks for response inhibition: Inter‐subject variation in stop signal reaction time

Inhibitory control requires precise regulation of activity and connectivity within multiple brain networks. Previous studies have typically evaluated age-related changes in regional activity or changes in interregional interactions. Instead, we test the hypothesis that activity and connectivity make distinct, complementary contributions to performance across the life span and the maintenance of successful inhibitory control systems. A representative sample of healthy human adults in a large, population-based life span cohort performed an integrated Stop-Signal (SS)/No-Go task during functional magnetic resonance imaging (n = 119; age range, 18–88 years). Individual differences in inhibitory control were measured in terms of the SS reaction time (SSRT), using the blocked integration method. Linear models and independent components analysis revealed that individual differences in SSRT correlated with both activity and connectivity in a distributed inhibition network, comprising prefrontal, premotor, and motor regions. Importantly, this pattern was moderated by age, such that the association between inhibitory control and connectivity, but not activity, differed with age. Multivariate statistics and out-of-sample validation tests of multifactorial functional organization identified differential roles of activity and connectivity in determining an individual's SSRT across the life span. We propose that age-related differences in adaptive cognitive control are best characterized by the joint consideration of multifocal activity and connectivity within distributed brain networks. These insights may facilitate the development of new strategies to support cognitive ability in old age.SIGNIFICANCE STATEMENT The preservation of cognitive and motor control is crucial for maintaining well being across the life span. We show that such control is determined by both activity and connectivity within distributed brain networks. In a large, population-based cohort, we used a novel whole-brain multivariate approach to estimate the functional components of inhibitory control, in terms of their activity and connectivity. Both activity and connectivity in the inhibition network changed with age. But only the association between performance and connectivity, not activity, differed with age. The results suggest that adaptive control is best characterized by the joint consideration of multifocal activity and connectivity. These insights may facilitate the development of new strategies to maintain cognitive ability across the life span in health and disease.

show abstract

“…3; Whelan et al, 2012; Zhang et al, 2015). However, the ICA approach has potential advantages over a GLM approach.…”

Section: Discussionmentioning

confidence: 99%

Activity and Connectivity Differences Underlying Inhibitory Control Across the Adult Life Span

et al. 2018

View full text Add to dashboard Cite

show abstract

“…The time between the go and stop signals, the stop signal delay (SSD), started at 200 ms and varied from one stop trial to the next according to a staircase procedure, increasing and decreasing by 67 ms each after a successful and failed stop trial (Levitt, 1971). The 67 ms step reflects four screen frames (monitor refreshing rate = 60 Hz) during stimulus presentation, as used in almost all of our previous studies (Chao et al, 2012; Farr et al, 2014; Ide et al, 2013; Liao et al, 2014; Luo et al, 2013; Winkler et al, 2013; Zhang et al, 2014, in press). In an earlier work we have tried a smaller staircase (32 ms) in a pilot study, which yielded similar performance profiles (Li et al, 2005).…”

Section: Methodsmentioning

confidence: 99%

Anticipating conflict: Neural correlates of a Bayesian belief and its motor consequence

Ide

Zhang

et al. 2015

NeuroImage

Self Cite

View full text Add to dashboard Cite

Previous studies have examined the neural correlates of proactive control using a variety of behavioral paradigms; however, the neural network relating the control process to its behavioral consequence remains unclear. Here, we applied a dynamic Bayesian model to a large fMRI data set of the stop signal task to address this issue. By estimating the probability of the stop signal – p(Stop) – trial by trial, we showed that higher p(Stop) is associated with prolonged go trial reaction time (RT), indicating proactive control of motor response. In modeling fMRI signals at trial and target onsets, we distinguished activities of proactive control, prediction error, and RT slowing. We showed that the anterior pre-supplementary motor area (pre-SMA) responds specifically to increased stop signal likelihood, and its activity is correlated with activations of the posterior pre-SMA and bilateral anterior insula during prolonged response times. This directional link is also supported by Granger causality analysis. Furthermore, proactive control, prediction error, and time-on-task are each mapped to distinct areas in the medial prefrontal cortex. Together, these findings dissect regional functions of the medial prefrontal cortex in cognitive control and provide system level evidence associating conflict anticipation with its motor consequence.

show abstract

“…In fact, SSRT is thought to be a product of competition between go and stop processes based on the interactive race model (Boucher et al, 2007; Verbruggen and Logan, 2008). Hence, in addition to indexing inhibition, SSRT likely also measures some form of switching between the two response modalities, as supported by experimental data (Emeric et al, 2007; Kenner et al, 2010; Zhang et al, 2015). Indeed, multiple lines of evidence have emerged to suggest that the dorsomedial frontal cortex, including the dACC and pre-SMA, play a crucial role in response switching as well as inhibition.…”

Section: Discussionmentioning

confidence: 71%

“…On the other hand, salience detection essentially involves enhanced attention to infrequency and/or diminished planning for the prepotent response and these preparatory processes may be represented differently and influence inhibitory control differently between SST25 and SST75 (Cai et al, 2014; Hu and Li, 2012; Zhang et al, 2015). Thus, we performed paired t tests to identify differences in voxelwise responses to SS > GS in SST25 vs. SST75.…”

Section: Methodsmentioning

confidence: 99%

“…A shorter SSRT indicates a more efficient process of response inhibition. Thus, greater regional activations to stop as compared to go success trials in association with the SSRT serves to expedite response inhibition (Chao et al, 2009; Zhang et al, 2015). Greater regional activations both to stop as compared to go trials in SST25 and to go as compared to stop trials in SST75 support salience detection.…”

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

A dual but asymmetric role of the dorsal anterior cingulate cortex in response inhibition and switching from a non-salient to salient action

Manza

Chao

et al. 2016

NeuroImage

Self Cite

View full text Add to dashboard Cite

Response inhibition and salience detection are among the most studied psychological constructs of cognitive control. Despite a growing body of work, how inhibition and salience processing interact and engage regional brain activations remains unclear. Here, we examined this issue in a stop signal task (SST), where a prepotent response needs to be inhibited to allow an alternative, less dominant response. Sixteen adult individuals performed two versions of the SST each with 25% (SST25) and 75% (SST75) of stop trials. We posited that greater regional activations to the infrequent trial type in each condition (i.e., to stop as compared to go trials in SST25 and to go as compared to stop trials in SST75) support salience detection. Further, successful inhibition in stop trials requires attention to the stop signal to trigger motor inhibition, and the stop signal reaction time (SSRT) has been used to index the efficiency of motor response inhibition. Therefore, greater regional activations to stop as compared to go success trials in association with the stop signal reaction time (SSRT) serves to expedite response inhibition. In support of an interactive role, the dorsal anterior cingulate cortex (dACC) increases activation to salience detection in both SST25 and SST75, but only mediates response inhibition in SST75. Thus, infrequency response in the dACC supports motor inhibition only when stopping has become a routine. In contrast, although the evidence is less robust, the pre-supplementary motor area (pre-SMA) increases activity to the infrequent stimulus and supports inhibition in both SST25 and SST75. These findings clarify a unique role of the dACC and add to the literature that distinguishes dACC and pre-SMA functions in cognitive control.

show abstract

Independent component analysis of functional networks for response inhibition: Inter‐subject variation in stop signal reaction time

Cited by 36 publications

References 119 publications

Activity and Connectivity Differences Underlying Inhibitory Control Across the Adult Life Span

Activity and Connectivity Differences Underlying Inhibitory Control Across the Adult Life Span

Anticipating conflict: Neural correlates of a Bayesian belief and its motor consequence

A dual but asymmetric role of the dorsal anterior cingulate cortex in response inhibition and switching from a non-salient to salient action

Contact Info

Product

Resources

About