Differential and distributed effects of dopamine neuromodulations on resting-state network connectivity

Cole, David M.; Beckmann, Christian F.; Oei, Nicole Y.L.; Both, Stephanie; Gerven, Joop M. A. van; Rombouts, Serge A.R.B.

doi:10.1016/j.neuroimage.2013.04.034

Cited by 114 publications

(116 citation statements)

References 74 publications

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“…We speculate that these distributed effects may be driven by stimulant-induced increase in catecholamine levels within prefrontal neural circuits. This hypothesis is supported by neuroimaging evidence that functional connectivity involving frontal cortex is strongly modulated by catecholamines (Cole et al 2013;Sripada et al 2013;Mueller et al 2014;Schrantee et al 2015). Although our prefrontal findings are consistent with previous work, other brain regions are discrepant.…”

Section: Discussionsupporting

confidence: 92%

“…Importantly, the magnitude of functional connectivity reduction was linked to the degree of amelioration of ADHD symptoms. These results are consistent with recent R-fMRI studies in healthy adults showing that stimulants reduced within-and between-network functional connectivity in central executive, salience, and default networks (Cole et al 2013;Sripada et al 2013;Mueller et al 2014;Schrantee et al 2015). These results are also in line with recent resting-state studies examining stimulant effects in children and adolescents with ADHD, which demonstrated that good responders to MPH were characterized by significantly reduced frontostriatal functional connectivity compared with poor responders (Hong et al 2015).…”

Section: Discussionsupporting

confidence: 91%

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Neural Correlates of Symptom Improvement Following Stimulant Treatment in Adults with Attention-Deficit/Hyperactivity Disorder

Yang

Kelly

Castellanos

et al. 2016

Journal of Child and Adolescent Psychopharmacology

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Objective: The purposes of this study were to examine the impact of 3 weeks of amphetamine administration on intrinsic connectome-wide connectivity patterns in adults with attention-deficit/hyperactivity disorder (ADHD) and explore the association between stimulant-induced symptom improvement and functional connectivity alteration. Methods: Participants included 19 adults (age 20-55 years) diagnosed with ADHD using the Diagnostic and Statistical Manual of Mental Disorders, 4th ed., Text Revision (DSM-IV-TR) criteria per the Adult Clinician Diagnostic Scale taking part in amphetamine trials. For each patient, two 6-minute resting-state functional magnetic resonance imaging (R-fMRI) scans were acquired at baseline and after treatment. A fully data-driven multivariate analytic approach (i.e., multivariate distance matrix regression [MDMR]) was applied to R-fMRI data to characterize the distributed pharmacological effects in the entire functional connectome. Clinical efficacy was assessed using ADHD rating scale with adult prompts and the Adult Self-Report Scale v1.1 Symptom Checklist. We linked stimulant-induced functional connectivity changes to symptom amelioration using Spearman's correlation. Results: Three weeks of administration of a stimulant significantly reduced ADHD symptoms. MDMR-based analyses on RfMRI data highlighted the left dorsolateral prefrontal cortex (DLPFC, a key cognitive control region) and the medial prefrontal cortex (MPFC, the anterior core of default network) whose distributed patterns of functional connectivity across the entire brain were altered by psychostimulants. Follow-up intrinsic functional connectivity revealed that stimulants specifically decreased the positive functional connectivity between DLPFC-insula, DLPFC-anterior cingulate cortex, and MPFC-insula. Importantly, these functional connectivity changes are associated with symptom improvement. Conclusion: These results suggested that ADHD is associated with increased functional integration or decreased functional segregation between core regions of cognitive control, default, and salience networks. The apparent normalization of intrinsic functional interaction in these circuits (i.e., increased functional segregation) may underlie the clinical benefits produced by 3 weeks of amphetamine treatment.

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Section: Discussionsupporting

confidence: 92%

Section: Discussionsupporting

confidence: 91%

Neural Correlates of Symptom Improvement Following Stimulant Treatment in Adults with Attention-Deficit/Hyperactivity Disorder

Yang

Kelly

Castellanos

et al. 2016

Journal of Child and Adolescent Psychopharmacology

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“…The approach has been successfully used previously. 39,40 Moreover, the template can be reused to test reproducibility of original findings on a separate group, as done in our study, and may serve to identify pathologic changes in at-risk groups in the future.…”

mentioning

confidence: 99%

Functional connectivity in the basal ganglia network differentiates PD patients from controls

et al. 2014

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Objective: To examine functional connectivity within the basal ganglia network (BGN) in a group of cognitively normal patients with early Parkinson disease (PD) on and off medication compared to age-and sex-matched healthy controls (HC), and to validate the findings in a separate cohort of participants with PD.Methods: Participants were scanned with resting-state fMRI (RS-fMRI) at 3T field strength.Resting-state networks were isolated using independent component analysis. A BGN template was derived from 80 elderly HC participants. BGN maps were compared between 19 patients with PD on and off medication in the discovery group and 19 age-and sex-matched controls to identify a threshold for optimal group separation. The threshold was applied to 13 patients with PD (including 5 drug-naive) in the validation group to establish reproducibility of findings.Results: Participants with PD showed reduced functional connectivity with the BGN in a wide range of areas. Administration of medication significantly improved connectivity. Average BGN connectivity differentiated participants with PD from controls with 100% sensitivity and 89.5% specificity. The connectivity threshold was tested on the validation cohort and achieved 85% accuracy. Conclusions:We demonstrate that resting functional connectivity, measured with MRI using an observer-independent method, is reproducibly reduced in the BGN in cognitively intact patients with PD, and increases upon administration of dopaminergic medication. Our results hold promise for RS-fMRI connectivity as a biomarker in early PD. Classification of evidence:This study provides Class III evidence that average connectivity in the BGN as measured by RS-fMRI distinguishes patients with PD from age-and sex-matched controls. Functional changes in the basal ganglia (BG) lie at the heart of Parkinson disease (PD). fMRI employing motor tasks has identified abnormalities in BG and supplementary motor area. 1,2However, interpretation of those changes may be confounded by the fact that patients with PD have difficulty with performing motor tasks. Resting-state fMRI can overcome this problem by providing an index of activity across the whole brain while the participant is at rest. Independent component analysis (ICA) enables isolation of resting-state brain networks, where individual areas in a given network show tight functional connectivity.3 Recent studies demonstrated effectiveness of this technique in identifying changes in the default mode network 4,5 and sensorimotor network 6 in PD. Although ICA-derived BG network (BGN) has been reliably identified in other disease states, 7-9 to our knowledge, no study so far has investigated it in PD.

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“…Citalopram, on the other hand, has a high affinity on histamine H 1 receptors [Carrasco and Sandner, 2005]. It is possible that these properties may account for differences in network changes between the two SSRIs [Cole et al, 2013; Villemagne et al, 1991]. However, it is yet to be established what the value is of specific network versus region effects in connectivity analyses.…”

Section: Discussionmentioning

confidence: 99%

“…Evidence is growing on the sensitivity of resting state networks, consisting of regions with coherent blood‐oxygen‐level‐dependent fluctuations, to pharmacological challenges [Cole et al, 2013; Khalili‐Mahani et al, 2015, 2012; Klumpers et al, 2012; Niesters et al, 2012]. These networks have consistently been found in healthy and clinical conditions, and are related to specific functions of the brain (i.e., motor, auditory, visual, emotional, and executive function) [Beckmann et al, 2005; Damoiseaux et al, 2006; Seeley et al, 2007; Smith et al, 2009].…”

Section: Introductionmentioning

confidence: 99%

Time related effects on functional brain connectivity after serotonergic and cholinergic neuromodulation

Klaassens

Rombouts

Winkler

et al. 2016

Human Brain Mapping

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Psychopharmacological research, if properly designed, may offer insight into both timing and area of effect, increasing our understanding of the brain's neurotransmitter systems. For that purpose, the acute influence of the selective serotonin reuptake inhibitor citalopram (30 mg) and the acetylcholinesterase inhibitor galantamine (8 mg) was repeatedly measured in 12 healthy young volunteers with resting state functional magnetic resonance imaging (RS‐fMRI). Eighteen RS‐fMRI scans were acquired per subject during this randomized, double blind, placebo‐controlled, crossover study. Within‐group comparisons of voxelwise functional connectivity with 10 functional networks were examined (P < 0.05, FWE‐corrected) using a non‐parametric multivariate approach with cerebrospinal fluid, white matter, heart rate, and baseline measurements as covariates. Although both compounds did not change cognitive performance on several tests, significant effects were found on connectivity with multiple resting state networks. Serotonergic stimulation primarily reduced connectivity with the sensorimotor network and structures that are related to self‐referential mechanisms, whereas galantamine affected networks and regions that are more involved in learning, memory, and visual perception and processing. These results are consistent with the serotonergic and cholinergic trajectories and their functional relevance. In addition, this study demonstrates the power of using repeated measures after drug administration, which offers the chance to explore both combined and time specific effects. Hum Brain Mapp 38:308–325, 2017. © 2016 Wiley Periodicals, Inc.

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Differential and distributed effects of dopamine neuromodulations on resting-state network connectivity

Cited by 114 publications

References 74 publications

Neural Correlates of Symptom Improvement Following Stimulant Treatment in Adults with Attention-Deficit/Hyperactivity Disorder

Neural Correlates of Symptom Improvement Following Stimulant Treatment in Adults with Attention-Deficit/Hyperactivity Disorder

Functional connectivity in the basal ganglia network differentiates PD patients from controls

Time related effects on functional brain connectivity after serotonergic and cholinergic neuromodulation

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