Increased default-mode variability is related to reduced task-performance and is evident in adults with ADHD

Athanasia M Mowinckel, Dag Alnæs, Mads L Pedersen, Sigurd Ziegler, Mats Fredriksen, Tobias Kaufmann, Edmund Sonuga-Barke, Tor Endestad, Lars T Westlye, Guido Biele, Athanasia M Mowinckel, Dag Alnæs, Mads L Pedersen, Sigurd Ziegler, Mats Fredriksen, Tobias Kaufmann, Edmund Sonuga-Barke, Tor Endestad, Lars T Westlye, Guido Biele

Abstract

Insufficient suppression and connectivity of the default mode network (DMN) is a potential mediator of cognitive dysfunctions across various disorders, including attention deficit/hyperactivity disorder (ADHD). However, it remains unclear if alterations in sustained DMN suppression, variability and connectivity during prolonged cognitive engagement are implicated in adult ADHD pathophysiology, and to which degree methylphenidate (MPH) remediates any DMN abnormalities. This randomized, double-blinded, placebo-controlled, cross-over clinical trial of MPH (clinicaltrials.gov/ct2/show/NCT01831622) explored large-scale brain network dynamics in 20 adults with ADHD on and off MPH, compared to 27 healthy controls, while performing a reward based decision-making task. DMN task-related activation, variability, and connectivity were estimated and compared between groups and conditions using independent component analysis, dual regression, and Bayesian linear mixed models. The results show that the DMN exhibited more variable activation patterns in unmedicated patients compared to healthy controls. Group differences in functional connectivity both between and within functional networks were evident. Further, functional connectivity between and within attention and DMN networks was sensitive both to task performance and case-control status. MPH altered within-network connectivity of the DMN and visual networks, but not between-network connectivity or temporal variability. This study thus provides novel fMRI evidence of reduced sustained DMN suppression in adults with ADHD during value-based decision-making, a pattern that was not alleviated by MPH. We infer from multiple analytical approaches further support to the default mode interference hypothesis, in that higher DMN activation variability is evident in adult ADHD and associated with lower task performance.

Keywords: Adult ADHD; DMN; Decision-making; Dopamine; Functional networks; Reward; fMRI.

Figures

Fig. 1
Fig. 1
Network overview. The 18 nodes identified from the independent component analysis, classified into networks by referencing the Smith et al. (2009) published ICA atlas. Purple = frontoparietal network; Dark blue = orbitofrontal cortex (OFC); Light blue = sensorimotor; Orange = cerebellum; Red = default mode network (DMN); Dark green = visual network; Yellow = auditory network; Light green = subcortical network; Pink = executive control network (Exec.Contr.). (For interpretation of the references to color in this figure legend, the reader is referred to the online version of this chapter.)
Fig. 2
Fig. 2
Node change by decision-making task parameters. Eleven nodes showed credible difference between groups in relation to decision phase and/or trial accuracy. Triangles are the estimated mean distributions for the groups, circles are the calculated difference distributions between groups (effect of ADHD: controls-placebo; effect of MPH: methylphenidate-placebo). The error bars denote the 95% highest density interval of the distributions. Solid horizontal lines are the value limits of the plots. Particularly DMN node 1 showed interesting negative co-variation with both decision phase and accuracy, which was stronger in the patient placebo condition compared to controls in the decision-phase. The node with the strongest positive association with choice onset was frontoparietal node 6 (DAN), where controls show increased activity compared to patients. This node encompasses the intraparietal sulcus, an area implicated in evidence accumulation in value-based decision-making (Basten et al., 2010). Activation in node 5 (executive control) showed a strong negative association with trial accuracy, which was more pronounced in controls compared to patients. Cereb. = cerebellum; DMN = default mode network; Exec.Contr. = executive control network; Frontopari. = frontoparietal network; Subcort. = subcortical network.
Fig. 3
Fig. 3
Component time series signal variance and the DMN. Nodes showing credible difference between groups/conditions with regards to node variance. Triangles are the estimated mean distributions for the groups, circles are the calculated difference distributions between groups (effect of ADHD: controls- placebo; effect of MPH: methylphenidate-placebo). (B) The DMN temporal variance showed negative correlation to task accuracy, participants who performed well on the task also had little variance in the DMN, with no difference between the groups. (C) The precuneus was more strongly connected to the rest of the DMN when patients were on placebo than on methylphenidate (C left: inflated brain). Mean connectivity scores (error bars are 2 * standard deviation in both directions) from this ROI (p 

Fig. 4

Edge correlations. Top panel: Triangles…

Fig. 4

Edge correlations. Top panel: Triangles are the estimated mean distributions for the groups,…

Fig. 4
Edge correlations. Top panel: Triangles are the estimated mean distributions for the groups, circles are the calculated difference distributions between groups. Error bars denote the 95% highest density interval of the distribution. Bottom two rows depict the two nodes connected by the edge. Bottom panels: Graph representation of edges between nodes for contrasts between patients when on placebo and controls (left), and edges correlated with overall task accuracy that are also different between patients and controls (right). Blue lines indicate a negative difference; red lines indicate a positive difference. The line thickness represents the magnitude of the difference. (For interpretation of the references to color in this figure legend, the reader is referred to the online version of this chapter.)
Fig. 4
Fig. 4
Edge correlations. Top panel: Triangles are the estimated mean distributions for the groups, circles are the calculated difference distributions between groups. Error bars denote the 95% highest density interval of the distribution. Bottom two rows depict the two nodes connected by the edge. Bottom panels: Graph representation of edges between nodes for contrasts between patients when on placebo and controls (left), and edges correlated with overall task accuracy that are also different between patients and controls (right). Blue lines indicate a negative difference; red lines indicate a positive difference. The line thickness represents the magnitude of the difference. (For interpretation of the references to color in this figure legend, the reader is referred to the online version of this chapter.)

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