Toward Systems Neuroscience of ADHD: A Meta-Analysis of 55 fMRI Studies
Abstract
Objective
Method
Results
Conclusions
Method
Search Strategy
Study Eligibility Criteria
Data Extraction
Meta-Analytic Technique
ADHDc | Comparison Subjectsd | |||||||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
Age | Age | |||||||||||||||
First Authorb | N | M | Mean | SD | N | M | Mean | SD | ADHD Type | Psychiatric Comorbidities | Treatment With Stimulants | Withdrawal From Stimulants | Task(s) | Contrast(s) | Number of Foci | Correction for Multiple Comparisonse |
Banich | 23 | 14 | 20 | 1.7 | 23 | 13 | 19 | 0.9 | Co | No | 20 lifetime, 14 current | 24 hours | Color word Stroop (variant) | Six contrasts included in the meta-analysisf | 20 (total) | Cluster-wise protection; voxel level threshold p=0.01 (AFNI AlphaSim) |
Bayerl | 30 | 16 | 31 | 0.6 | 30 | 16 | 31 | 8.4 | Co | No | All naive | N/A | 2-back working memory | C>A | 1 | Cluster-size thresholding (50 voxels); voxel level p=0.001 uncorrected (SPM99) |
Booth | 12 | 8 | 9.4 | 1.2 | 12 | 7 | 9.3 | 12 | 8 Co, 4 I | No | All current | 48 hours | Go/no-go selective attention | C>A; C>A | 17; 3 | Cluster-size thresholding (10 voxels); voxel level p<0.001 uncorrected (SPM99) |
Braet | 20 | 17 | 14 | 2.1 | 38 | 31 | 13 | 1.9 | NS | NS | Some (NS) current | 24 hours | Sustained Attention to Response Test (go/no-go) | C>A: successful inhibition | 5 | NS for second-level analysis (AFNI) |
Cao | 12 | 12 | 13 | 1.7 | 13 | 13 | 13 | 1.2 | 7 Co, 5 I | 5 ODD, 2 CD | 3 current | 2 weeks | Cued target detection | C>A: intrinsic alerting effect; C>A: phasic alerting effect; C>A: alerting effect | 3; 4; 3 | Cluster-size thresholding (10 voxels); voxel level p<0.001 uncorrected (SPM2) |
Cerullo | 10 | 7 | 14 | 2 | 13 | 7 | 15 | 1.9 | NS | 2 ODD, 2 tics | 8 current | Day of the scan | CPT-X | C>A; A>C | 1; 2 | Cluster-size thresholding (137 voxels); voxel-level p<0.05 uncorrected (AFNI) |
Cubillo (2010) | 11 | 11 | 29 | 1 | 14 | 14 | 28 | 2 | 6 Co, 2 HI, 3 I | 1 AD, 3 MD, 1 CD, 2 SUD, 1 ND | All naive | N/A | Tracking stop | C>A: successful stop-go trials; C>A: unsuccessful stop-go trials; C>A: switch task | 2; 1; 2 | Cluster-mass threshold; voxel-wide significance: p<0.05; cluster threshold p<0.01 (XBAM) |
Cubillo (2011) | 11 | 11 | 29 | 1 | 15 | 15 | 28 | 3 | 6 Co, 2 HI, 3 I | 1 AD, 3 MD, 1 CD, 2 SUD, 1 ND | All naive | N/A | Simon task | C>A: incongruent-congruent; C>A: oddball-congruent | 1; 1 | Cluster-mass threshold; voxel-wide significance: p<0.05; cluster threshold p<0.01 (XBAM) |
Cubillo (2012) | 11 | 11 | 29 | 1 | 15 | 15 | 28 | 3 | 6 Co, 2 HI, 3 I | 1 AD, 3 MD, 1 CD, 2 SUD, 1 ND | All naive | N/A | Rewarded CPT | C>A: effect of attention; C>A: effect of reward | 3; 2 | Cluster-mass threshold; voxel-wide significance: p<0.05; cluster threshold 0.01 (XBAM) |
Dibbets (2009) | 16 | 16 | 29 | 6.4 | 13 | 13 | 29 | 6.4 | All Co | No | 14 current | 24 hours | Modified go/no-go | A>C: overall activation | 1 | Cluster-size thresholding (3 voxels); voxel level p<0.05 (SPM2) |
Dibbets (2010) | 15 | 15 | 29 | 6.2 | 14 | 14 | 29 | 6.4 | All Co | No | 14 current | 24 hours | Switch | C>A; A>C | 6; 6 | Cluster-level thresholding (1,000 iterations; p<0.05) (Brainvoyager QX) |
Dillo | 15 | 11 | 21–42 | N/A | 15 | 11 | 21–46 | N/A | 5 Co, 7 I, 3 HI | No | Some (NS) current | 3 weeks | Go/no-go | A>C | 2 | N/S (SPM2) |
Durston (2003) | 7 | 6 | 8.5 | 1.6 | 7 | 6 | 8.7 | 1.5 | 4 Co, 3 I | ODD or CD (NS) | All current | 24 hours | Go/no-go | C>A: no-go > go; A>C: no-go > go | 1; 8 | Cluster-size thresholding (3 voxels); voxel-level p<0.05 (NeuroImaging Software) |
Durston (2007) sample 1 | 10 | 8 | 12 | 2.6 | 10 | 8 | 12 | 2.1 | 5 Co, 2 I, 3 HI | 4 ODD | 5 current | 24 hours | Variant go/no-go | C>A: unexpected stimulus-unexpected time | 1 | Cluster-size thresholding (5 voxels); voxel-level p<0.05 (SPM2) |
Durston (2007) sample 2 | 12 | 12 | 15 | 2.3 | 12 | 12 | 15 | 2.1 | 9 Co, 3 HI | 4 ODD | 9 current | 24 hours | Variant go/no-go | C>A: expected stimulus-unexpected time; C>A: unexpected stimulus-expected time | 1; 2 | Cluster-size thresholding (5 voxels); voxel-level p<0.05 (SPM2) |
Hale | 10 | 9 | 35 | 8.1 | 10 | 9 | 27 | 4.1 | 3 Co, 7 I | 1 GAD + SoP + SP, 1 SP | 4 current | 2 weeks | WAIS forward/ backward digit span | C>A: backward; A>C: forward; A>C: backward | 5; 7; 3 | Cluster-size thresholding (25 voxels); voxel level p<0.001 uncorrected (SPM2) |
Karch | 8 | 7 | 38 | 7.8 | 8 | 7 | 38 | 6.6 | All Co | No | All naive | N/A | Auditory go/no-go (modified) | C>A | 7 | Cluster-size thresholding; p<0.001 uncorrected; threshold: 10 voxels (BrainVoyager) |
Kobel (2009) | 14 | 14 | 10 | 1.3 | 12 | 12 | 11 | 1.6 | 9 Co, 5 I | 5 ODD-CD, 4 GAD | All current | 24 hours | n-back | C>A: averaged 2- and 3-back | 5 | Family-wise error correction (p<0.05); cluster size: 10 voxels (SPM5) |
Kobel (2010) | 14 | 14 | 10 | 1.3 | 12 | 12 | 11 | 1.6 | 9 Co, 5 I | 5 ODD-CD, 4 GAD | All current | No | n-back | C>A: activation in 3-back task | 1 | Correction applied but type of correction NS (SPM 5) |
Konrad | 16 | 16 | 10 | 1.9 | 16 | 16 | 10 | 1.3 | 9 Co, 6 I, 1 HI | 5 ODD, 3 AD | All naive | N/A | Attention Network Test (modified) | C>A: alerting; C>A: executive control; A>C: alerting; A>C: reorienting; A>C: executive control | 1; 2; 1; 3; 1 | Cluster-size thresholding (10 voxels); p<0.001 uncorrected (SPM2) |
Kooistra | 10 | 10 | 22 | NS | 10 | 10 | 22 | NS | NS | N/A | No after age 16 years | N/A | Go/no-go | C>A: go; A>C: go | 16; 2 | Corrected cluster significance threshold: p=0.01 (FSL) |
Krauel | 12 | 12 | 15 | 0.7 | 12 | 12 | 15 | 1.3 | 6 Co, 5 I, 1 HI | 3 ODD, 2 CD | 5 current | 24 hours | Recognition memory | C>A: neutral; A>C: emotional; A>C: neutral | 1; 4; 4 | Cluster-size thresholding (10 voxels); voxel-level p<0.001 uncorrected (SPM99) |
Mostofsky | 11 | 8 | 10 | 1.2 | 11 | 8 | 10 | 1.4 | 9 Co, 2 I | No | 8 current | 24 hours | Sequential finger tapping | C>A | 2 | Cluster-size thresholding (84 voxels); voxel-level p<0.001 uncorrected (SPM99) |
Passarotti (2010, J Intl Neuropsychol Soc) | 15 | 12 | 13 | 2.6 | 14 | 7 | 14 | 2.4 | All C | No | 5 current | Over a 3-week period | Emotional valence Stroop | C>A: negative > neutral; C>A: positive > neutral words; A>C: negative > neutral words; A>C: positive > neutral words | 2; 2; 4; 5 | Contiguity threshold: p<0.01 uncorrected; experiment-wise type 1: p <0.02 corrected (AFNI AlphaSim) |
Passarotti (2010, J Am Acad Child Adolesc Psychiatry) | 14 | 9 | 13 | 2.3 | 19 | 9 | 14 | 3.1 | All Co | No | NS | At least 4 days | Affective 2-back working memory | C>A: angry > neutral faces; A>C: angry > neutral faces; A>C: happy > neutral faces | 13; 1; 12 | Contiguity threshold: p<0.01 uncorrected; experiment-wise type 1: p<0.02 corrected (AFNI AlphaSim) |
Passarotti (2010, Psychiatry Res) | 11 | 6 | 13 | 2.7 | 15 | 7 | 14 | 3.1 | All Co | No | 6 current | 3 weeks | Response inhibition | C>A; A>C | 7; 3 | Contiguity threshold: p<0.01 uncorrected; experiment-wise type 1: p<0.02 corrected (AFNI AlphaSim) |
Prehen-Kristensen | 12 | NS | 13 | 1.8 | 12 | NS | 14 | 2 | 12 Co, 2 I | 5 ODD | All current | 48 hours | Delayed-match-to-sample paradigm | C>A | 15 | Cluster-size thresholding (5 voxels); voxel-level p<0.05 (SPM5) |
Rubia (1999) | 7 | 7 | 16 | NS | 9 | 9 | 15 | NS | All Co | CD (NS) | NS | 1 week | Stop; delay | C>A; C>A | 4; 2 | Permutation; voxel-wise probability type I error: 0.05 |
Rubia (2005) | 16 | 16 | 13 | 2.1 | 21 | 21 | 14 | 1.6 | All Co | 5 CD | All naive | N/A | Stop | C>A: successful > unsuccessful inhibition; C>A: unsuccessful inhibition > baseline go | 2; 2 | Cluster level difference; <1 false activated cluster at p<0.05 (voxel comparison); p<0.01 (cluster comparison) |
Rubia (2007) | 17 | 17 | 14 | 2 | 18 | 18 | 13 | 2 | All Co | No | All naive | N/A | Oddball | C>A: successful oddball > standard; C>A: standard > oddball | 3; 2 | Cluster level difference; <1 false activated cluster at p<0.05 (voxel comparison); p<0.01 (cluster comparison) |
Rubia (2008) | 20 | 20 | 13 | 1.5 | 20 | 20 | 14 | 2 | All Co | No | All naive | N/A | Tracking stop | C>A: successful > failed stop; C>A: failed stop > go; C>A: go > stop | 1; 1; 1 | Cluster level difference; <1 false activated cluster at p<0.05 (voxel comparison); p<0.03 (cluster comparison) |
Rubia (2009, Am J Psychiatry) | 18 | 18 | 13 | 1 | 16 | 16 | 13 | 3 | All Co | No | All naive | N/A | Rewarded CPT | C>A: effect of attention; C>A: effect of reward; A>C: effect of attention | 2; 1; 9 | Cluster level difference; <1 false activated cluster at p<0.05 (voxel comparison); p<0.01 (cluster comparison) |
Rubia (2009, J Child Psychol Psychiatry) | 20 | 20 | 13 | 1.4 | 20 | 20 | 14 | 1.9 | All Co | No | All naive | N/A | Simon | C>A: incongruent > oddball; C>A: oddball > congruent | 2; 2 | Cluster level difference; <1 false activated cluster at p<0.05 (both voxel and cluster comparison) |
Rubia (2009, Neuropsychopharmacology) | 13 | 13 | 13 | 1.4 | 13 | 13 | 13 | 1.8 | All Co | 1 CD | All naive | N/A | Rewarded CPT | C>A: attention; C>A: reward; A>C: reward | 13; 2; 4 | Cluster level difference; <1 false activated cluster at p<0.05 (voxel comparison); p<0.02 (cluster comparison) (XBAM) |
Rubia (2009, Philos Trans R Soc Lond B Biol Sci) | ||||||||||||||||
Study 1 | 10 | 10 | 14 | 2 | 10 | 10 | 15 | 4 | All Co | 1 CD | 4 naive, 6 current | 36 hours (N=6) | Delay discounting | C>A | 6 | Cluster level difference; <1 false activated cluster at p<0.05 (voxel comparison); p<0.006 (cluster comparison) |
Study 2 | 12 | 12 | 13 | 1 | 12 | 12 | 13 | 1 | All Co | 1 CD | All naive | N/A | Time discrimination | C>A; A>C | 1; 2 | Cluster level difference; <1 false activated cluster at p<0.05 (voxel comparison); p<0.006 (cluster comparison) |
Rubia (2010, Hum Brain Mapp, p 1823) | 14 | 14 | 13 | 1.1 | 20 | 20 | 14 | 1.9 | All Co | No | All naive | N/A | Switch | C>A | 2 | Cluster level difference; <1 false activated cluster at p<0.05 for both voxel and cluster comparison (XBAM) |
Rubia (2010, Hum Brain Mapp, p 287) | 18 | 18 | 14 | 1.1 | 20 | 20 | 15 | 1.1 | All Co | No | All naive | N/A | Visual tracking stop; Meiran switch | C>A: successful-stop; C>A: failed stop; C>A | 1; 2; 3 | Cluster level difference; <1 false activated cluster at p<0.05 (voxel comparison); p<0.003 (cluster comparison) (XBAM) |
Rubia (2011, Biol Psychiatry) | 12 | 12 | 13 | 1 | 13 | 13 | 13 | 1 | All Co | No | All naive | N/A | Visual tracking stop | C>A: successful inhibition; C>A: inhibition failure | 13; 13 | Threshold-free cluster enhancement (p<0.05) |
Rubia (2011, Neuropsychopharmacology) | 12 | 12 | 13 | 1 | 13 | 13 | 13 | 1 | All Co | No | All naive | N/A | Simon | C>A: Simon > oddball condition | 4 | Cluster level difference; <1 false activated cluster at p<0.05 (voxel comparison); p<0.01 (cluster comparison) (XBAM) |
Rubia (2011, Hum Brain Mapp) | 18 | 18 | 14 | 2 | 20 | 20 | 16 | 1 | All Co | No | All naive | N/A | Simon | C>A: oddball > congruent; C>A: incongruent > oddball | 2; 2 | Cluster level difference; <1 false activated cluster at p<0.05 (voxel comparison); p<0.01 (cluster comparison) (XBAM) |
Schulz | 5g | 5 | 18 | 1.3 | 5 | 5 | 18 | 1.4 | 1 Co, 3 I, 1 HI | 1 CD | 4 lifetimeh | N/A | Go/no-go | C>A: correct no-go > correct go; A>C: correct no-go > correct go | 2; 3 | Cluster-size thresholding (120 voxels); voxel level p<0.01 uncorrected (SPM99) |
Sheridan | 10 | 0 | 15 | 2 | 10 | 0 | 15 | 1.3 | 6 Co; 4 I | 2 ODD, 2 SP | 5 lifetimei, 2 current | 24 hours | Delay match-to-sample | C>A: activation at high load period | 2 | Gaussian field theory; p=0.05 corrected at cluster level (fMRIstat program) |
Silk (2008) | 12 | 12 | 11 | 1.5 | 12 | 12 | 11 | 1.5 | All Co | No | All naive | N/A | Raven’s Standard Progressive Matrices | C>A | 45 | Clusters of voxels (z>2.33) with cluster level p<0.05 corrected (FSL) |
Silk (2005) | 7 | 7 | 14 | 1.8 | 7 | 7 | 15 | 1.8 | All Co | No | All naive | N/A | Mental rotation | C>A; A>C | 8; 4 | Voxel level p<0.001 uncorrected; cluster level p<0.05 corrected |
Smith (2006) | ||||||||||||||||
Study 1 | 17 | 17 | 13 | 2 | 18 | 18 | 14 | 2 | All Co | 5 CD | All naive | N/A | Go/no-go | C>A: successful no-go stimuli | 1 | Cluster level difference; <1 false activated cluster at p<0.05 (voxel comparison); p<0.01 (cluster comparison) |
Study 2 | 14 | 14 | 13 | 1.8 | 27 | 27 | 14 | 1.8 | All Co | 5 CD | All naive | N/A | Switch | C>A: switch | 9 | Cluster level difference; <1 false activated cluster at p<0.05 (voxel comparison); p<0.01 (cluster comparison) |
Smith (2008) | 21 | 21 | 13 | 1.6 | 17 | 17 | 14 | 2.1 | All Co | 3 CD/ODD | All naive | N/A | Time discrimination | C>A: time discrimination > temporal order judgment | 2 | Cluster level difference; <1 false activated cluster at p<0.05 (voxel comparison); p<0.01 (cluster comparison) (XBAM) |
Spinelli (2011, J Am Acad Child Adolesc Psychiatry) | 13 | 9 | 11 | 1.4 | 17 | 8 | 11 | 1.2 | 10 Co, 3 I | 3 ODD, 1 SP | 2 current | 24 hours | Go/no-go | A>C: preerror versus precorrect inhibition | 2 | Spatial extent cluster size threshold to achieve a corrected statistical threshold of p=0.05 (SPM5) |
Spinelli (2011, J Child Psychol Psychiatry) | 13 | 9 | 11 | 1.4 | 17 | 8 | 11 | 1.2 | 10 Co, 3 I | 3 ODD, 1 SP | 2 current | 24 hours | Go/no-go | A>C: posterror versus postcorrect inhibition trials | 9 | Spatial extent cluster size threshold to achieve a corrected statistical threshold of p=0.05 (SPM5) |
Strohle | 10 | 10 | 32 | 8.1 | 10 | 10 | 32 | 9.9 | 4 Co, 4 I, 2 HI | No | All naive | N/A | Monetary Incentive Delay | C>A: anticipation of gain > nongain; A>C: outcome of gain > nongain | 1; 7 | p<0.05 false discovery rate-corrected (SPM2) |
Tamm (2004) | 10 | 10 | 16 | 1.4 | 12 | 12 | 16 | 0.8 | All Co | No | 5 current | 18 hours | Modified go/no-go | C>A: “A–B” contrast; A>C: “A–B” contrast | 1; 1 | Deactivation mask (z=1.67; p<0.05) (SPM99) |
Tamm (2006) | 14 | 14 | 14–18 | N/A | 12 | 12 | 14–18 | N/A | All Co | No | 5 current | 18 hours | Oddball | C>A: activation during the oddball event | 4 | NS |
Valera (2005) | 20 | 12 | 34 | 11.8 | 20 | 12 | 33 | 11.0 | NS | No | 10 lifetime | 24 hours | Variant of visual n-back test | C>A: 2-back minus X-task contrast | 2 | p=0.001 (uncorrected) with extent threshold determined by Gaussian random field theory (SPM99) |
Valera (2010, Biol Psychiatry) | 21 | 15 | 34 | 10.1 | 19 | 12 | 33 | 11.0 | 5 Co, 12 I | No | 9 current | 24 hours | Paced and unpaced finger tapping | C>A: paced finger tapping; C>A: unpaced finger tapping | 24; 17 | p<0.05, family-wise error corrected, with extent threshold of 20 contiguous voxels (SPM5) |
Valera (2010, Am J Psychiatry) | 44 | 23 | 37 | 11.0 | 49 | 23 | 33 | 10.0 | 13 Co, 17 I, 1 HI | No | 18 current | 24 hours | 2-back | C>A: 2-back visual memory task | 2 | p<0.05, corrected (Gaussian random field theory) (SPM2) |
Vance | 12 | 12 | 11 | 1.5 | 12 | 12 | 10 | 1.3 | All Co | No | All naive | N/A | Mental rotation | C>A | 4 | Cluster-level threshold p<0.05, corrected (FSL) |
Wolf | 13 | 13 | 22 | 4.4 | 12 | 12 | 22 | 4.7 | 9 Co, 2 I, 2 HI | No | All lifetime | 6 at least 6 weeks, 6 for 3 days | Cognitive activation | C>A: increasing working memory load | 5 | p<0.05, false discovery rate-corrected (SPM5) |
Activation Liklihood Estimation Results in Relation to Neuronal Networks
Results
Studies Included in the Meta-Analysis
Activation Likelihood Estimation Results
Weighted Centera | Maximum Activation Likelihood Estimate Valuea | ||||||||
---|---|---|---|---|---|---|---|---|---|
Contrast, Analysis, and Cluster Number | Volume (mm3) | x | y | z | Extrema Value | x | y | z | Anatomical Labelb |
Comparison subjects > participants with ADHD | |||||||||
Children, all tasksc | |||||||||
1 | 1,864 | −0.35 | 15.56 | 48.61 | 0.0211 | 0 | 16 | 54 | Medial superior frontal gyrus/supplementary motor area (BA 6) R, L (frontoparietal/ventral attention) |
0.0186 | 0 | 14 | 44 | Paracingulate gyrus (BA 32) R, L (ventral attention) | |||||
2 | 688 | 31.42 | 0.19 | 3.33 | 0.0148 | 32 | 0 | 4 | Putamen R |
3 | 464 | −21.92 | 2.37 | 4.1 | 0.0119 | −20 | 4 | 4 | Putamen L |
4 | 424 | 33.7 | −27.47 | 50.75 | 0.0136 | 34 | −28 | 52 | Postcentral gyrus R (somatomotor) |
5 | 400 | 42.23 | 9.52 | 29.36 | 0.0134 | 42 | 10 | 30 | Inferior frontal sulcus; inferior precentral sulcus R (frontoparietal) |
6 | 384 | 57.29 | −25.00 | 28.42 | 0.0145 | 58 | −26 | 28 | Inferior parietal lobule (supramarginal gyrus; BA 40) R (ventral attention) |
7 | 368 | 55.66 | 12.64 | −6.64 | 0.0136 | 56 | 12 | −6 | Superior temporal gyrus (BA 22) R (somatomotor) |
8 | 280 | −41.26 | 31.46 | 23.46 | 0.0131 | −42 | 32 | 24 | Middle frontal gyrus (BA 9/46) L (frontoparietal) |
9 | 248 | 47.46 | 25.85 | 31.84 | 0.0115 | 48 | 26 | 32 | Middle frontal gyrus (BA 9/46) R (frontoparietal) |
Adults, all tasksc | |||||||||
1 | 400 | 21.7 | −27.31 | 50.84 | 0.0106 | 22 | −28 | 50 | Central sulcus/precentral gyrus R |
2 | 232 | 34.38 | 56.96 | 13.62 | 0.0103 | 34 | 56 | 14 | Middle frontal gyrus (BA 10) R (frontoparietal) |
Participants with ADHD > comparison subjects | |||||||||
Children, all tasksd | |||||||||
1 | 680 | 39.72 | −58.51 | 18.51 | 0.0135 | 40 | −58 | 20 | Angular gyrus; middle occipital gyrus R |
0.0079 | 40 | −66 | 14 | Angular gyrus; middle occipital gyrus R (visual) | |||||
2 | 400 | 15.02 | −50.94 | 31.01 | 0.0101 | 16 | −52 | 32 | Posterior cingulate cortex; subparietal sulcus R |
3 | 392 | 31.22 | −7.23 | 16.7 | 0.0107 | 32 | −8 | 16 | White matter R (suboperculum) |
4 | 352 | 4.67 | −13.72 | 42.61 | 0.0101 | 4 | −14 | 42 | Midcingulate cortex R (ventral attention) |
Adults, all tasksd | |||||||||
1 | 872 | 40.39 | −58.08 | 16.91 | 0.0152 | 40 | −58 | 18 | Angular gyrus; middle occipital gyrus R |
Results in Relation to Neuronal Networks
Discussion
Meta-Analyses
Children.
Adults.
Stimulant-naive individuals.
Comorbidity-free individuals.
Specific tasks.
Omnibus meta-analysis.
Subtraction analyses.
General Overview
Limitations
Conclusions
Supplementary Material
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