Brain Signal Variability Differentially Affects Cognitive Flexibility and Cognitive Stability

Abstract

Recent research yielded the intriguing conclusion that, in healthy adults, higher levels of variability in neuronal processes are beneficial for cognitive functioning. Beneficial effects of variability in neuronal processing can also be inferred from neurocomputational theories of working memory, albeit this holds only for tasks requiring cognitive flexibility. However, cognitive stability, i.e., the ability to maintain a task goal in the face of irrelevant distractors, should suffer under high levels of brain signal variability. To directly test this prediction, we studied both behavioral and brain signal variability during cognitive flexibility (i.e., task switching) and cognitive stability (i.e., distractor inhibition) in a sample of healthy human subjects and developed an efficient and easy-to-implement analysis approach to assess BOLD-signal variability in event-related fMRI task paradigms. Results show a general positive effect of neural variability on task performance as assessed by accuracy measures. However, higher levels of BOLD-signal variability in the left inferior frontal junction area result in reduced error rate costs during task switching and thus facilitate cognitive flexibility. In contrast, variability in the same area has a detrimental effect on cognitive stability, as shown in a negative effect of variability on response time costs during distractor inhibition. This pattern was mirrored at the behavioral level, with higher behavioral variability predicting better task switching but worse distractor inhibition performance. Our data extend previous results on brain signal variability by showing a differential effect of brain signal variability that depends on task context, in line with predictions from computational theories.

Significance statement: Recent neuroscientific research showed that the human brain signal is intrinsically variable and suggested that this variability improves performance. Computational models of prefrontal neural networks predict differential effects of variability for different behavioral situations requiring either cognitive flexibility or stability. However, this hypothesis has so far not been put to an empirical test. In this study, we assessed cognitive flexibility and cognitive stability, and, besides a generally positive effect of neural variability on accuracy measures, we show that neural variability in a prefrontal brain area at the inferior frontal junction is differentially associated with performance: higher levels of variability are beneficial for the effectiveness of task switching (cognitive flexibility) but detrimental for the efficiency of distractor inhibition (cognitive stability).

Keywords: BOLD-signal variability; behavioral variability; cognitive flexibility; cognitive stability; fMRI.

Figure 1.

Task paradigm and analysis pipeline for BOLD-signal variability. A, Task paradigm showing examples of ongoing task trials, distractor inhibition trials, and task-switch trials. B, Standard regression model including one regressor per condition (plus 1st and 2nd derivative; see also Model A). C, Trial-by-trial regression model including one regressor (plus 1st and 2nd derivative) per trial for the condition of interest (see also Model B). D, Brain map exemplifying a DoR (i.e., standard model minus trial-by-trial regression model) map for one subject.

Figure 2.

Brain activity and performance correlations with brain signal variability. A, Univariate activation for task switching (red) and distractor inhibition (yellow); overlap in orange (for visualization purposes, a strict threshold of p < 0.000000000001 was applied so that local maxima of activation patterns can be better identified.). B, Negative correlations between condition-specific BOLD-signal variability and error costs: areas in red show significant negative correlation with error costs in task switching, areas in blue correlate negatively with error costs in distractor inhibition, and overlap in magenta. BG, Basal ganglia; PCC, posterior cingulate corex; SFG, superior frontal gyrus.

Figure 3.

Positive relationship between RT costs and BOLD-signal variability during distractor inhibition and antagonistic relation between performance and BOLD-signal variability in left IFJ. A, Positive correlation between RT costs and condition-specific BOLD-signal variability during distractor inhibition, p < 0.05 (corrected). B, Conjunction in left IJF (k = 8 voxel) between (1) negative correlation of task-switching costs in error rates with BOLD-signal variability, as shown in Figure 2B and (2) positive correlation of distractor inhibition costs in RT and BOLD-signal variability. C, Scatter plots illustrating the antagonistic relationship between BOLD-signal variability and behavior for task switching (left) and distractor inhibition (right) in the overlapping part of the IFJ (note that, after exclusion of one multivariate outlier as detected by Mahalanobis distance, the result for distractor inhibition was still significant with r = 0.26, p = 0.02). **p < 0.01. ER, Error rate.