Distinct and temporally associated neural mechanisms underlying concurrent, postsuccess, and posterror cognitive controls: Evidence from a stop-signal task

Abstract

Cognitive control is built upon the interactions of multiple brain regions. It is currently unclear whether the involved regions are temporally separable in relation to different cognitive processes and how these regions are temporally associated in relation to different task performances. Here, using stop-signal task data acquired from 119 healthy participants, we showed that concurrent and poststop cognitive controls were associated with temporally distinct but interrelated neural mechanisms. Specifically, concurrent cognitive control activated regions in the cingulo-opercular network (including the dorsal anterior cingulate cortex [dACC], insula, and thalamus), together with superior temporal gyrus, secondary motor areas, and visual cortex; while regions in the fronto-parietal network (including the lateral prefrontal cortex [lPFC] and inferior parietal lobule) and cerebellum were only activated during poststop cognitive control. The associations of activities between concurrent and poststop regions were dependent on task performance, with the most notable difference in the cerebellum. Importantly, while concurrent and poststop signals were significantly correlated during successful cognitive control, concurrent activations during erroneous trials were only correlated with posterror activations in the fronto-parietal network but not cerebellum. Instead, the cerebellar activation during posterror cognitive control was likely to be driven secondarily by posterror activation in the lPFC. Further, a dynamic causal modeling analysis demonstrated that postsuccess cognitive control was associated with inhibitory connectivity from the lPFC to cerebellum, while excitatory connectivity from the lPFC to cerebellum was present during posterror cognitive control. Overall, these findings suggest dissociable but temporally related neural mechanisms underlying concurrent, postsuccess, and posterror cognitive control processes in healthy individuals.

Keywords: cerebellum; cingulo-opercular network; cognitive control; fronto-parietal network; posterror; poststop.

FIGURE 1

Activation maps for the modeled contrasts in the stop‐signal task. (a) For concurrent cognitive control, significant activations were shown in the cingulo‐opercular network, in particular the anterior cingulate cortex, insula, and thalamus, as well as the superior temporal gyrus, supplementary motor area and visual cortex. (b) In contrast, poststop cognitive control was associated with significant activations in the fronto‐parietal network and cerebellum. The maps are thresholded at voxel‐level p _FWE <.05 across the whole brain

FIGURE 2

Associations between concurrent and poststop activations for correct cognitive control (i.e., CR and post‐CR). Signal changes in concurrently activated regions significantly predicted signal changes in three postactivated regions. ACC, anterior cingulate cortex; CRB, cerebellum; CUN, cuneus; INS, insula; IPL, inferior parietal lobule; MFG, middle frontal gyrus; SMA, supplementary motor area; STG, superior temporal gyrus; TLM, thalamus

FIGURE 3

Associations between concurrent and poststop activations for incorrect cognitive control (i.e., FA and post‐FA). Signal changes in concurrently activated regions significantly predicted signal changes in the prefrontal and parietal cortices but not cerebellum. Instead, posterror signal changes in the prefrontal cortex were significantly correlated with those in the cerebellum. ACC, anterior cingulate cortex; CRB, cerebellum; CUN, cuneus; INS, insula; IPL, inferior parietal lobule; MFG, middle frontal gyrus; SMA, supplementary motor area; STG, superior temporal gyrus; TLM, thalamus

FIGURE 4

Dynamic causal modeling analysis for prefrontal‐cerebellar connectivity during poststop cognitive control. (a) Illustration for the examined models in the DCM analysis. For posterror cognitive control (post‐FA), driving input was fixed to the prefrontal cortex and modularity effect was fixed on top‐down connectivity from the prefrontal cortex to cerebellum, based on correlation results shown in Figure 3. For postsuccess cognitive control (post‐CR), three possibilities were considered for driving input (i.e., input to prefrontal cortex, input to cerebellum, and input to both) and for modulatory effect (i.e., from prefrontal to cerebellar, from cerebellar to prefrontal, and both directions) separately, thereby generating a total of nine models. (b) The Bayesian model selection identified a winning model with driving input to cerebellum and modularity effects on both directions during post‐CR. Notably, prefrontal → cerebellar connectivity was negatively modulated (inhibited) during post‐CR but positively modulated (excited) during post‐FA. (c) Group‐level parameters (mean ± SD) for the winning model estimated by Bayesian model averaging. Note that for intrinsic connectivity and driving inputs, significance is based on whether the parameters are different from zero (one‐sample t test); while for modularity effects, significance is based on whether they are different between post‐CR and post‐FA (paired t test)