Cited by 158Attention Deficit Hyperactivity DisorderDevelopmental and Educational NeuropsychologyNeural and Behavioral Psychology Studies

Electroencephalography Correlates of Spatial Working Memory Deficits in Attention-Deficit/Hyperactivity Disorder: Vigilance, Encoding, and Maintenance

Open access
Lenartowicz, Agatha, Delorme, Arnaud, Walshaw, Patricia D., Cho, Alex L., Bilder, Robert M., McGough, James J., McCracken, James T., Makeig, Scott +1 more·2014·The Journal of Neuroscience

Abstract

In the current study we sought to dissociate the component processes of working memory (WM) (vigilance, encoding and maintenance) that may be differentially impaired in attention-deficit/ hyperactivity disorder (ADHD). We collected electroencephalographic (EEG) data from 52 children with ADHD and 47 typically developing (TD) children, ages 7–14 years, while they performed a spatial Sternberg working memory task. We used independent component analysis and time-frequency analysis to identify midoccipital alpha (8–12 Hz) to evaluate encoding processes and frontal midline theta (4–7 Hz) to evaluate maintenance processes. We tested for effects of task difficulty and cue processing to evaluate vigilance. Children with ADHD showed attenuated alpha band event-related desynchronization (ERD) during encoding. This effect was more pronounced when task difficulty was low (consistent with impaired vigilance) and was predictive of memory task performance and symptom severity. Correlated with alpha ERD during encoding were alpha power increases during the maintenance period (relative to baseline), suggesting a compensatory effort. Consistent with this interpretation, midfrontal theta power increases during maintenance were stronger in ADHD and in high-load memory conditions. Furthermore, children with ADHD exhibited a maturational lag in development of posterior alpha power whereas age-related changes in frontal theta power deviated from the TD pattern. Last, subjects with ADHD showed age-independent attenuation of evoked responses to warning cues, suggesting low vigilance. Combined, these three EEG measures predicted diagnosis with 70% accuracy. We conclude that the interplay of impaired vigilance and encoding in ADHD may compromise maintenance and lead to impaired WM performance in this group.

AI snapshot

Written from the paper’s full text.

TL;DR

This EEG study tested whether spatial working memory deficits in ADHD stem from vigilance, encoding, or maintenance problems. It found weaker alerting and encoding responses in ADHD alongside stronger maintenance activity, suggesting vigilance and encoding contribute to working memory impairment.

Key findings

  • Children with ADHD were less accurate (0.76 vs. 0.81) and more variable in reaction time (0.44 vs. 0.39 s) than typically developing peers, with slower reaction times at trend level; groups did not differ in age or full-scale IQ.
  • During alerting, the midfrontal P2 response to the fixation cue was smaller in ADHD (0.21 vs. 0.56 µV; F(1,74)=10.2, p<0.002), while occipital P1 sensory responses did not differ by group.
  • During encoding, midoccipital alpha event-related desynchronization was weaker in ADHD (−0.14 vs. −0.81 dB; F(1,67)=12.0, p<0.001), with a larger group difference at low load (0.92 dB) than high load (0.42 dB), significant only at low load.
  • During maintenance, midfrontal theta synchronization was stronger in ADHD (0.17 vs. 0.09 dB; F=4.7, p<0.03) and midoccipital alpha synchronization was stronger in ADHD (0.82 vs. −0.01 dB; F=7.91, p<0.006); a logistic model using P2, encoding alpha, and theta predicted diagnosis with 70% accuracy, sensitivity 0.69, specificity 0.72, and odds ratio 5.56.

Methods

  • A total of 102 children were recruited; analyses included 80 children (37 ADHD, 43 typically developing) aged 7–14 after independent component analysis and accuracy criteria reduced the sample. Diagnosis used the KSADS-PL, IQ used the WASI, and symptoms used the SWAN scale.
  • Participants completed a Sternberg spatial working memory task with fixation (500 ms), encoding of 1, 3, 5, or 7 dots (2 s), maintenance (3 s), and a probe; there were 48 trials per block across two blocks.
  • EEG was recorded from 40 electrodes, decomposed with independent component analysis, fitted with equivalent dipoles, clustered with k-means into 12 component clusters, and analyzed for midoccipital alpha (8–12 Hz) during encoding and midfrontal theta (4–7 Hz) during maintenance using repeated-measures ANOVA with Group, Load, and Age, plus regression and sixfold logistic cross-validation.

Limitations

  • The authors state that the diagnostic classifier needs testing in a larger sample for generalizability and that the study lacked power for a stepwise analysis of individual measures, which would require about 150 sample points; they also note that the clustering method may not return the same clusters as other definitions, though adjusting the distance metric had small effects.
  • The authors note that higher load also increased stimulus richness, so encoding deficits could reflect sensory processing of more complex displays as well as top-down control; they argue against a bottom-up account based on preserved P1 responses and prior evidence of intact visuospatial orienting.
  • Evident from the text: the analyzed sample was reduced from 102 to 80 by independent component analysis and accuracy requirements, and the diagnostic prediction analysis used only 64 participants with components in both clusters; the task used spatial rather than verbal working memory and did not require manipulation, limiting generalization.

Model-written summary. Check it against the paper before relying on it.

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Registry

Crossref · 10.1523/jneurosci.1765-13.2014

Cites

73 of 73 references verified0 citation errors · 0 not checkable

Statistics

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Claims the paper makes

0 of 59 cited sources checked · 0 supported · 0 flagged

  • Findingown data

    Inspection of maintenance-interval ERSPs in the midoccipital cluster showed clear increases in mean alpha band spectral power during maintenance.

    “an inspection of the maintenance interval ERSPs in the midoccipital cluster (Fig. 4a) showed clear increases in mean alpha band spectral power (i.e., ERS) during the maintenance period”
    Quote in the paperSubstantial claim
  • Findingown data

    The maximal increase in alpha band power during working-memory maintenance appeared at a lower frequency than the maximal alpha band decrease during encoding.

    “the maximal increase in alpha band power during WM maintenance appeared at a lower frequency than the maximal alpha band decrease during encoding.”
    Quote in the paperSubstantial claim
  • Findingown data

    Children with ADHD had a smaller midfrontal-cluster P2 than typically developing children.

    “Children with ADHD had a smaller midfrontal cluster-component P2 (0.21 V) than TD children (0.56 V).”
    Quote in the paperSubstantial claim
  • Findingown data

    The repeated-measures ANOVA on maintenance-interval theta band power showed a significant main effect of Load.

    “and Load (F (1,74) ϭ 9.8, p Ͻ 0.002; Fig. 4b, bottom).”
    Quote in the paperNot a substantial claim
  • Findingown data

    Maintenance theta ERS did not show a significant age effect.

    “Unlike alpha ERD, the theta increase did not show a significant AGE effect (F (1,74) ϭ 0.02, p Ͻ 0.9).”
    Quote in the paperNot a substantial claim
  • May combine two claims. 58
  • Classified as probably not a substantial claim. 19
  • The quote only partly states this claim. 1
  • May combine two claims.

    Findingown data

    The study found group differences in vigilance, encoding, and maintenance that follow different developmental trajectories.

    “We show group differences in vigilance, encoding, and maintenance that differ in developmental trajectories, and suggest that variability in encoding efficacy contributes to impaired WM performance in ADHD.”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Findingown data

    Midfrontal-cluster P2 peak amplitude did not vary with age and did not interact with Load or Group.

    “The amplitude of the midfrontal cluster P2 peak did not vary as a function of Age (F (74) Ͻ 1, and this variable did not interact with Load or Group (F (74) Ͻ 1.”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Findingown data

    In the ADHD group, the main effects of Load and Age on encoding alpha ERD were significant, and their interaction was also significant.

    “In the ADHD group, in addition to these two main effects (F (1,31) Ͼ 11.6, p Ͻ 0.002) their interaction was also significant (F (1,31) ϭ 4.7, p Ͻ 0.04).”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Findingown data

    Theta synchronization decreased with age in the typically developing group but increased with age in the ADHD group, producing a significant group difference in older children but not in younger children.

    “theta synchronization decreased with age in the TD group but increased with age in the ADHD group, resulting in a significant Group difference in older children (t (32) ϭ 2.6, p Ͻ 0.02, two-tailed) but not in younger children (t (42) Ͻ 1).”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Findingown data

    For midfrontal-cluster P2 amplitude, neither the Load effect nor the Group-by-Load interaction was significant.

    “Neither the Load effect nor the Group-by-Load interaction were significant (F (1,74) Ͻ 1, p Ͼ 0.30)”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Findingown data

    When absolute baseline alpha power was used, the Group effect and its interaction with Load were not significant.

    “The Group effect was not significant (F (1,67) ϭ 0.001, p Ͼ 0.97) and neither was its interaction with Load (F (1,67) ϭ 0.21, p Ͻ 0.21)”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Findingown data

    In the ADHD group, only the Load-by-Age interaction on maintenance alpha ERS was significant, because only the high-load condition showed a maturational decrease in alpha recruitment.

    “By contrast, in the ADHD group only the interaction between Load and Age was significant (F (1,31) ϭ 4.16, p Ͻ 0.05) because only in the high-load condition was the maturational decrease in alpha recruitment observed (younger: 1.18 dB; older: 0.18 dB).”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Findingown data

    Maintenance alpha ERS was more pronounced in children with ADHD than in typically developing children, but did not differ between low and high load.

    “Alpha ERS during maintenance was more pronounced in children with ADHD (0.82 dB) than the TD group (Ϫ0.01 dB), but did not differ between lowload (0.39 dB) and high-load (0.36 dB).”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Findingown data

    Post hoc t tests showed that the group difference in encoding alpha ERD was significant at low load but not at high load.

    “Post hoc t tests revealed that the Group difference was significant at lowload (t (69) ϭ 3.91, p Ͻ 0.001) but not at high-load (t (69) ϭ 1.69, p Ͻ 0.1).”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Findingown data

    Post hoc tests confirmed that the age effect on maintenance alpha ERS was significant only in the high-load condition and not at low load.

    “Post hoc tests confirmed that only in the high-load condition was this age effect significant (t (31) ϭ 2.45, p Ͻ 0.02, two-tailed); it was not significant at low-load ( t (31) Ͻ 1).”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Findingown data

    The maximum encoding alpha ERD was at 11.1 Hz, the maximum maintenance alpha ERS was at 9.5 Hz, and this difference was significant across subjects.

    “The maximum of the alpha ERD during encoding was at 11.1 Hz (SE ϭ 0.16 Hz) whereas the maximum of the alpha power ERS during maintenance was at 9.5 Hz (SE ϭ 0.13 Hz), and this difference was significant across subjects (t (70) ϭ 7.5, p Ͻ 0.001)”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Findingown data

    Age effects on maintenance alpha ERS followed trends very similar to those for encoding alpha ERD, consistent with the strong correlation between these variables.

    “Additionally, effects of age on the alpha ERS during maintenance (Fig. 5b) followed trends very similar to those for alpha ERD during encoding, which is consistent with the strong correlation that we observed between these variables.”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Findingown data

    The maintenance-interval analysis of midoccipital alpha showed a significant Group effect but no main effect of Load.

    “this maintenance interval analysis revealed a significant effect of Group (F (1,67) ϭ 7.91, p Ͻ 0.006), but unlike the former it did not show a main effect of Load (F (1,67) Ͻ 1).”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Findingown data

    In the typically developing group, only Load and Age effects on encoding alpha ERD were significant, with stronger ERD in older children and at high load; the interaction was not significant.

    “In the TD group only the effects of Load (F (1,36) ϭ 9.1, p Ͻ 0.01) and Age (F (1,36) ϭ 8.8, p Ͻ 0.01) were significant, meaning that alpha ERD responses were stronger in older children and at high-load.The interaction was not significant (F (1,36) Ͻ 1.”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Findingown data

    Peak alpha frequency during baseline was significantly higher than during encoding and maintenance, while encoding and maintenance did not differ.

    “Post hoc t tests (twotailed), with Bonferroni corrected alpha set at .017, showed that peak frequency during baseline (9.87 Hz) was significantly higher than during encoding (9.51 Hz; t (70) ϭ 2.81, p Ͻ 0.006) and maintenance (9.65 Hz; t (70) ϭ 2.38, p Ͻ 0.02); the peak frequencies during encoding and maintenance did not differ (t (70) ϭ 1.42, p Ͻ 0.16).”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Findingown data

    A repeated-measures ANOVA on peak absolute alpha power showed no significant Group effect or Group-by-Time interaction, implying that peak alpha frequency did not differ by group.

    “A repeated-measure ANOVA with Group (ADHD vs TD) and Time interval (baseline, encoding, maintenance) showed neither a significant effect of Group (F (1,69) Ͻ 1, or an interaction between GROUP and TIME (F (1,69) ϭ 1.78, p Ͻ 0.19) implying that the peak frequency of alpha did not differ by group.”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Findingown data

    Age was associated with higher accuracy, faster responses, and less variable responses.

    “Age was associated with higher accuracy (b accuracy ϭ 0.34; t (62) ϭ 2.8, p Ͻ 0.009) faster responses (b RT ϭ Ϫ0.4; t (62) ϭ Ϫ3.4,p Ͻ 0.001) and less variable responses (b RTsd ϭ 0.33; t (62) ϭ 2.6, p Ͻ 0.01).”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Findingown data

    The model predicted a significant portion of SWAN inattentiveness subscale variability but not hyperactive scale variability.

    “The SWAN analysis revealed that the model predicted a significant portion of SWAN score variability for the inattentiveness subscale (R 2 adj Ͼ 0.14; F (5,62) ϭ 3.2, p Ͻ 0.01), but not the hyperactive scale (R 2 adj Ͼ 0.05; F (5,62) ϭ 1.7, p Ͻ 0.16).”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Findingown data

    The overall models accounted for significant variance in accuracy, reaction time, and reaction-time variability.

    “Overall-model statistics indicated that these models accounted for a significant amount of variance in accuracy (R 2 adj Ͼ 0.25; F (5,62) ϭ 5.4, p Ͻ 0.001), RT (R 2 adj Ͼ 0.31; F (5,62) ϭ 7.0, p Ͻ 0.001), and RT SD (R 2 adj Ͼ 0.22; F (5,62) ϭ 4.9, p Ͻ 0.001).”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Findingreasoning

    The positive likelihood of the test was 2.44, the negative likelihood was 0.44, and the odds ratio was 5.56.

    “The positive likelihood of the test was 2.44, meaning that the probability of a positive test being correct was 2.44 times stronger than of it raising a false alarm.The negative likelihood was 0.44, meaning that the probability of a negative test correctly identifying a TD child was 2.3 times stronger than of it missing an ADHD diagnosis.The odds ratio (2.44/0.44)was 5.56.”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Findingown data

    Sensitivity of ADHD detection and test specificity were both significant.

    “Thus, sensitivity of ADHD detection was significant (0.69, CI 0.95 ϭ 0.50 -0.83), as was test specificity (0.72, CI 0.95 ϭ 0.53-0.86).”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Findingown data

    The sixfold logistic regression classifier predicted diagnosis with 70% accuracy, exceeding the upper 95% confidence interval for by-chance accuracy.

    “The sixfold logistic regression classifier predicted diagnosis with 70% accuracy, exceeding the upper 95% CI (CI 0.95 ϭ 0.38 -0.62) for by-chance accuracy (0.5).”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Findingreasoning

    Age was not a significant predictor in either SWAN model, likely because of the restricted age range.

    “In neither of the SWAN models was age a significant predictor (b Ͻ Ϫ0.09; t (62) Ͻ 1) likely because of the restricted age range.”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Findingown data

    P2 peak amplitude was weakly predictive of SWAN inattentive scores, and no other relationships for either midfrontal measure were significant.

    “P2 peak amplitude was weakly predictive of scores on the inattentive subscale of the SWAN (b ϭ 0.2; t (62) ϭ 1.7, p Ͻ 0.10); however, no other relationships (accuracy, RT, RT SD , SWN inatt ) were significant (t (62) Ͻ 1.53, p Ͼ 0.13) for either measure.”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Findingown data

    Midfrontal cluster ERSP showed theta band (4-7 Hz) ERS during maintenance that was stronger in ADHD children and during high-load trials.

    “The ERSP for the midfrontal cluster showed a (4 -7 Hz) theta band ERS during the maintenance interval (broken-line box) that was stronger in children with ADHD and during high-load trials.”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Findingown data

    Alpha ERD increased with age in both groups and task intervals, but the increase in the ADHD group lagged behind the TD group.

    “Although in both groups and task intervals, alpha ERD increased with age, the increase in the ADHD group lagged behind that of the TD group.”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Findingown data

    In TD children, theta power showed a load effect in younger but not older children; in ADHD children, the opposite was observed, with a load effect emerging with age.

    “In the TD group, theta power showed a load effect in younger children but not in older children.In the ADHD group, the opposite effect was observed.In these children a load effect emerged with age.”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Findingown data

    Alpha ERD during encoding was enhanced in TD children and during high-load.

    “during which alpha ERD was enhanced in TD children and during high-load.”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Findingown data

    Mid-occipital cluster ERSPs showed alpha band (8-12 Hz) ERD during encoding and probe periods, and lower-frequency ERS during maintenance.

    “The ERSPs for the mid-occipital cluster were characterized by an alpha band (8 -12 Hz) ERD during encoding (E) and probe (P) periods, and by a somewhat lower-frequency ERS during memory maintenance (M).”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Findingown data

    Maturational delay was observed in the ADHD group for mid-occipital alpha ERD during encoding and mid-occipital ERS during maintenance.

    “Maturational delay was observed in the ADHD group for the (a) mid-occipital cluster alpha ERD during encoding and the (b) midoccipital ERS during maintenance.”
    Quote in the paperSubstantial claim
  • Classified as probably not a substantial claim.

    Premisecitation

    Independent components have been proposed to reflect spatially coherent local field activity from a single cortical area.

    “The independent components (ICs) produced by this analysis have temporally near-independent activity time courses and near-dipolar scalp projections, and have been proposed to represent spatially coherent local field activity within a single cortical area (Makeig et al., 1996(Makeig et al., , 2004;;Onton et al., 2006;Delorme et al., 2012).”
    Quote in the paperSubstantial claim0 of 3 sources checked
    • cites Makeig et al., 1996

      Not checked in the free run.

    • cites Makeig et al., 2004

      Not checked in the free run.

    • cites Onton et al., 2006

      Not checked in the free run.

  • Classified as probably not a substantial claim.

    Premisecitation

    Executive functioning deficits are considered central in neuropsychological models of ADHD.

    “Deficits of executive functioning are generally agreed to play a key role in neuropsychological models of attention-deficit/ hyperactivity disorder (ADHD; Barkley, 1997;Tannock, 1998;Castellanos and Tannock, 2002).”
    Quote in the paperSubstantial claim0 of 3 sources checked
    • cites Barkley, 1997

      Not checked in the free run.

    • cites Tannock, 1998

      Not checked in the free run.

    • cites Castellanos and Tannock, 2002

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Study design and conductown data

    For this dataset, changing the cluster distance metric had little effect on clustering, which was mainly driven by similarity in equivalent dipole locations.

    “However, for these data adjusting the cluster distance metric had relatively small effects on the clustering, which was (intentionally) dominated by similarity in IC equivalent dipole locations.”
    Quote in the paperNot a substantial claim
  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductown data

    The number of retained independent components did not differ significantly between TD (17.6, SD=3.2) and ADHD (17.1, SD=3.5) groups.

    “Between groups, 17.6 (SD ϭ 3.2) ICs were retained for TD subjects, 17.1 (SD ϭ 3.5) for ADHD subjects (nonsignificant by t test, t (100) Ͻ 1).”
    Quote in the paperNot a substantial claim
  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductown data

    All independent component clusters were tested for group differences, including those not expected a priori.

    “Although we had prior expectations for clusters of interest, all clusters were evaluated for group differences and are illustrated and described fully in Figure 2.”
    Quote in the paperNot a substantial claim
  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    Working memory problems in ADHD are commonly attributed to frontostriatocerebellar dysfunction and catecholaminergic dysregulation of the prefrontal cortex.

    “WM problems are widely interpreted to be due to frontostriatocerebellar dysfunctions, reflecting catecholaminergic dysregulation of prefrontal cortex (PFC; McCracken, 1991;Arnsten, 2006).”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites McCracken, 1991 source

      Not checked in the free run.

    • cites Arnsten, 2006

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductown data

    The retained independent components accounted for an average of 67.8% (SD=16.3%) of the whole-channel EEG data across subjects.

    “Across subjects, the retained ICs accounted for an average of 67.8% (SD ϭ 16.3%) of the EEG data.”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Interpretationreasoning

    The observed pattern of poorer short-term memory but intact distractor filtering contradicts the predominant frontostriatal dysfunction model, which predicts impairment across prefrontal-cortex-related functions.

    “These findings are contrary to the prediction of the predominant model of frontostriatal dysfunction in ADHD, which would predict impairment across PFC-related functions.”
    Quote in the paperSubstantial claim
    • Rests on an assumption: The predominant frontostriatal dysfunction model of ADHD predicts impairment across functions that rely on the prefrontal cortex.
  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductcitation

    The clustering method used for independent components is not guaranteed to produce the same clusters as alternative definitions.

    “Note that this method of clustering ICs is not guaranteed to return the same clusters as other possible definitions, as discussed by Bigdely-Shamlo et al. (2013).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Bigdely-Shamlo et al. (2013)

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Study design and conductown data

    The analysis retained an average of 17.3 independent components per subject (SD=3), totaling 1766 components across subjects, with dipole models explaining on average 93.3% (SD=1.4%) of the component scalp maps.

    “This procedure left an average of 17.3 (of a maximum of 40) ICs per subject (SD ϭ 3), and 1766 ICs across all subjects, whose single-equivalent dipole models on average accounted for 93.3% (SD ϭ 1.4%) of the IC scalp map.”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Premisecitation

    Independent components from ICA have nearly independent time courses and nearly dipolar scalp projections.

    “The independent components (ICs) produced by this analysis have temporally near-independent activity time courses and near-dipolar scalp projections, and have been proposed to represent spatially coherent local field activity within a single cortical area (Makeig et al., 1996(Makeig et al., , 2004;;Onton et al., 2006;Delorme et al., 2012).”
    Quote in the paperSubstantial claim0 of 3 sources checked
    • cites Makeig et al., 1996

      Not checked in the free run.

    • cites Makeig et al., 2004

      Not checked in the free run.

    • cites Onton et al., 2006

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductown data

    The medial frontal cluster explained the largest variance (30.4%) in the grand mean ERP during fixation.

    “For analysis of alerting responses (ERPs) during fixation, we used the same midfrontal cluster as for theta, as the spatial topography is comparable across both of these metrics and the medial frontal cluster contributed the most variance (30.4%) to the grand mean ERP during fixation.”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Interpretationown data

    The age-related decrease in maintenance alpha ERS is consistent with the interpretation that ERS reflects effort to engage working-memory maintenance mechanisms and disengage sensory attention, a need that may decrease with age as attentional mechanisms mature.

    “which is consistent with the interpretation that the ERS reflects effort to engage WM maintenance mechanisms and disengage sensory attention; a need that may decrease with age as attentional mechanisms mature.”
    Quote in the paperSubstantial claim
    • Rests on an assumption: Age-related differences in the EEG measures reflect developmental maturation.
  • May combine two claims.

    Interpretationreasoning

    The encoding finding is conceptually consistent with the fixation alerting result and suggests that lowered or more variable vigilance may compromise encoding in ADHD.

    “This is conceptually consistent with the analysis of the alerting response during fixation and suggests that lowered or more variable vigilance may compromise the ability to encode information in this group.”
    Quote in the paperNot a substantial claim
  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Interpretationown data

    These performance findings align with prior reports that spatial working memory is impaired in children with ADHD.

    “These findings are consistent with previous reports that SWM is impaired in children with ADHD.”
    Quote in the paperNot a substantial claim
  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductown data

    The ADHD and TD groups did not differ in the proportion of males to females.

    “The ADHD and TD groups did not differ in mean age (t (78) Ͻ 1) or FSIQ (t (78) ϭ 1.5, p Ͻ 0.14) or the proportion of males to females in each group [ 2 (1, N ϭ 80) ϭ 0.16, p Ͻ 0.7].”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Interpretationown data

    With age, children with ADHD develop mechanisms necessary for stimulus encoding but do not consistently recruit them when task difficulty is low.

    “This suggests that, with age, children with ADHD do develop mechanisms necessary for stimulus encoding but, consistent with the reduced-vigilance hypothesis, it appears that this mechanism is not (consistently) recruited when task difficulty is low.”
    Quote in the paperSubstantial claim
    • Rests on an assumption: Age-related differences in the EEG measures reflect developmental maturation.
  • May combine two claims.

    Interpretationown data

    No larger group difference at high load than at low load was observed, which would be expected if the ADHD deficit were specific to working-memory maintenance.

    “In particular, we did not observe a larger Group difference at high-load than at low-load, which would be expected if the deficit in the ADHD group were specific to WM maintenance.”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Interpretationown data

    Attenuated alpha ERD and exaggerated alpha ERS during encoding and maintenance may be functionally related and may represent a processing profile more often adopted by the ADHD group.

    “The similarity of this finding across encoding and maintenance may imply that attenuated alpha ERD and exaggerated alpha ERS during the two respective intervals are functionally related and may represent a processing profile more often adopted by the ADHD group.”
    Quote in the paperSubstantial claim
  • The quote only partly states this claim.

    Interpretationown data

    The correlation between encoding alpha ERD and maintenance theta ERS suggests that maintenance efficacy is related to encoding efficacy.

    “suggesting that the efficacy of maintenance is related to efficacy of encoding processes.”
    Quote in the paperSubstantial claim
  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Study design and conductown data

    Each cluster contained independent components from most participants, with cluster sizes ranging from 12 to 97 participants.

    “Each cluster therefore included one or more positionally and functionally more similar ICs from most participants [range, 12 participant/cluster (cluster containing eye blinks) to 97 participants/cluster of 102].”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Interpretationown data

    The stronger midfrontal theta response in ADHD emerged with development, a trajectory that differed from typically developing controls.

    “In other words, the stronger midfrontal theta response in the ADHD group emerged with development, a trajectory that differed from that of TD controls.”
    Quote in the paperSubstantial claim
    • Rests on an assumption: Age-related differences in the EEG measures reflect developmental maturation.
  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductown data

    The number of artifact-free epochs used in analyses was 65 (SD=13) per TD subject and 60 (SD=12) per ADHD subject.

    “Remaining epochs used in the analyses were as follows: 65 (SD ϭ 13) per subject for the TD group and 60 (SD ϭ 12) for the ADHD group.”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Interpretationown data

    Children with ADHD had a weaker midfrontal cortical evoked response to the alerting fixation stimulus, consistent with weakened vigilance during the task.

    “These results indicate that children with ADHD had a weaker midfrontal cortical evoked response to the alerting fixation stimulus, consistent with weakened vigilance during the task.”
    Quote in the paperSubstantial claim
    • Rests on an assumption: The midfrontal P2 response to the fixation stimulus indexes vigilance.
  • May combine two claims.

    Premisecitation

    The dependence of encoding alpha ERD magnitude on task load replicates the pattern of behavioral deficits in ADHD reported by Friedman-Hill et al. (2010), who suggested that poor responses at low loads reflect sluggish recruitment of working-memory processes.

    “The dependence of encoding alpha ERD magnitude on task load in the current study replicates the pattern of behavioral deficits in ADHD reported by Friedman-Hill et al. (2010) who suggested that poor responses at low-loads reflect “sluggish recruitment” of WM processes (Robertson and Garavan, 2004).”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites Friedman-Hill et al. (2010)

      Not checked in the free run.

    • cites Robertson and Garavan, 2004

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Alpha is an index of gating or filtering of stimuli to be encoded, a process likely constituent of the working-memory recruitment described by Friedman-Hill et al. (2010).

    “Alpha is therefore an index of a sort of “gating” or “filtering” of stimuli to be encoded (Klimesch, 1997, 2007) a process that is a likely constituent of the “WM recruitment” described by Friedman-Hill et al. (2010).”
    Quote in the paperSubstantial claim0 of 3 sources checked
    • cites Klimesch, 1997

      Not checked in the free run.

    • cites Klimesch, 2007

      Not checked in the free run.

    • cites Friedman-Hill et al. (2010)

      Not checked in the free run.

  • Classified as probably not a substantial claim.

    Premisecitation

    Alpha desynchronization or blocking reflects release of such inhibition, allowing enhanced processing of attended stimuli.

    “conversely, alpha desynchronization or alpha blocking (Berger, 1930;Jasper and Penfield, 1949;Chatrian et al., 1959) is thought to reflect a release of such inhibition, allowing enhanced processing of attended stimuli.”
    Quote in the paperSubstantial claim0 of 3 sources checked
    • cites Berger, 1930

      Not checked in the free run.

    • cites Jasper and Penfield, 1949

      Not checked in the free run.

    • cites Chatrian et al., 1959

      Not checked in the free run.

  • May combine two claims.

    Interpretationreasoning

    The results indicate deficient recruitment of working memory in ADHD, accompanied by or possibly caused by task disengagement.

    “Together these results point to deficient recruitment of WM in ADHD, accompanied by or possibly produced by task disengagement.”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Interpretationown data

    The P2 difference was present in both younger and older children, suggesting it is an early ADHD trait that may not normalize with age.

    “That this difference was present in both younger and older children suggests this is an early trait of ADHD that may not normalize with age.”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Interpretationown data

    Stronger alpha ERD during encoding predicted both better task performance and lower symptom severity.

    “Hence, stronger alpha ERD during stimulus encoding predicted both better performance on the task and lower symptom severity.”
    Quote in the paperSubstantial claim
    • The authors state this as an assumption: Higher SWAN scores indicate lower symptom severity.
  • May combine two claims.

    Premisecitation

    Most prior studies of alpha and theta band power in ADHD examined absolute EEG frequency power and only at individual or averaged scalp channels.

    “Most prior studies of alpha and theta band power in ADHD examined absolute EEG frequency power and only at individual or averaged scalp channels (Barry et al., 2003;Mitchell et al., 2008).”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites Barry et al., 2003

      Not checked in the free run.

    • cites Mitchell et al., 2008

      Not checked in the free run.

  • May combine two claims.

    Interpretationown data

    The results indicate an age-invariant vigilance deficit in the ADHD group, supported by reduced alerting responses at fixation and enhanced group differences during encoding and maintenance for alpha ERD/ERS at low load.

    “Our results indicate an age invariant deficit in vigilance in the ADHD group, supported by reduced alerting responses at fixation and enhanced group differences during encoding and maintenance (for alpha ERD/ERS) during low-load.”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Interpretationreasoning

    Coupled with elevated occipital alpha ERS and midfrontal theta ERS during maintenance in ADHD, the findings suggest that encoding problems in ADHD lead to compensatory efforts during maintenance.

    “Coupled with the elevated occipital alpha ERS and midfrontal theta ERS during maintenance in the ADHD group, this finding suggests that problems during encoding in the ADHD group lead to compensatory efforts during maintenance.”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Interpretationown data

    Working-memory performance deficits in ADHD are at least in part the result of poor vigilance and atypical encoding, possibly from a deficit or variability in the degree of focus of attention first to the alerting fixation cue and then to the encoding stimulus.

    “Together, these data indicate that WM performance deficits in ADHD are at least in part the result of poor vigilance and atypical encoding; possibly from a deficit and/or variability in degree of focus of attention first to the alerting fixation cue and then to the ensuing encoding stimulus.”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Interpretationown data

    The findings indicate that manipulating working memory contents during maintenance is not required to observe ADHD performance deficits, consistent with the interpretation that other impairments (e.g., vigilance and encoding) may contribute to WM impairments.

    “our findings indicate that manipulating the contents of WM during maintenance is not required to observe ADHD deficits in performance, consistent with the interpretation that other system impairments (such as, vigilance and encoding) may contribute to the WM impairments.”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Interpretationown data

    The observed decrease in alpha power during encoding and increase during maintenance were accompanied by a decrease in alpha peak frequency relative to baseline.

    “Hence, the observed decrease in alpha power during encoding and increase during maintenance were accompanied by a decrease in alpha peak frequency relative to baseline.”
    Quote in the paperSubstantial claim
  • Classified as probably not a substantial claim.

    Interpretationcitation

    The finding is consistent with prior observations that medial frontal theta power during memory maintenance increases with task difficulty.

    “This is consistent with the observation that medial frontal theta power during memory maintenance increases with task difficulty (Gevins et al., 1997;Jensen and Tesche, 2002;Onton et al., 2005).”
    Quote in the paperSubstantial claim0 of 3 sources checked
    • cites Gevins et al., 1997

      Not checked in the free run.

    • cites Jensen and Tesche, 2002

      Not checked in the free run.

    • cites Onton et al., 2005

      Not checked in the free run.

  • Classified as probably not a substantial claim.

    Premisecitation

    Alpha band activities support active inhibition of processing of task-irrelevant visual or other stimuli.

    “This conclusion is consistent with the common interpretation of alpha band activities as supporting active inhibition of processing of taskirrelevant visual or other stimuli (Worden et al., 2000;Pfurtscheller, 2003;Klimesch et al., 2007;Foxe and Snyder, 2011)”
    Quote in the paperSubstantial claim0 of 3 sources checked
    • cites Worden et al., 2000 source

      Not checked in the free run.

    • cites Pfurtscheller, 2003

      Not checked in the free run.

    • cites Klimesch et al., 2007

      Not checked in the free run.

  • May combine two claims.

    Interpretationcitation

    Prior work on preserved visuospatial orienting in ADHD suggests a top-down problem is likely, and this aligns with the current study's lack of group difference in P1 responses to encoding stimuli.

    “Prior studies indicating preserved visuospatial orienting in ADHD (Huang-Pollock and Nigg, 2003) hint at a top-down problem being the likely culprit, and are consistent with the absence of a group difference in the (more bottom-up) P1 responses to encoding stimuli in the current study.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Huang-Pollock and Nigg, 2003

      Not checked in the free run.

  • May combine two claims.

    Interpretationown data

    The midoccipital encoding deficit, measured by alpha ERD, was predictive of the ensuing maintenance effect, task performance, and symptom severity.

    “The midoccipital encoding deficit, measured by alpha ERD, was predictive of the ensuing maintenance effect (alpha ERS), but also task performance and symptom severity.”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Premisecitation

    Verbal task and combined subtype are less reliably associated with WM deficits.

    “both conditions less reliably associated with WM deficits (van der Meere and Sergeant, 1988;Martinussen et al., 2005).”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites van der Meere and Sergeant, 1988

      Not checked in the free run.

    • cites Martinussen et al., 2005

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Mazaheri et al. (2010) reported attenuated posterior scalp alpha ERD following attended versus to-be-ignored stimuli in ADHD individuals, which agrees with our findings.

    “Using a different cued-attention paradigm, Mazaheri et al. (2010) reported attenuated posterior scalp alpha ERD following presentations of attended versus tobe-ignored stimuli in ADHD individuals, in agreement with our findings.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Mazaheri et al., 2010

      Not checked in the free run.

  • Classified as probably not a substantial claim.

    Premisenone given

    This study presents a first analysis of cortical source-level event-related EEG dynamics underlying often-reported spatial working memory deficits in ADHD.

    “In this study we present a first analysis of cortical source-level event-related EEG dynamics underlying often-reported deficits of SWM in ADHD.”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Premisecitation

    That study used a verbal rather than spatial working memory task and only children with the combined ADHD subtype.

    “That study, however, used a verbal rather than SWM task and only children with the combined subtype of ADHD”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Gomarus et al., 2009

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    That study found no group differences in alpha.

    “There, no group differences in alpha were found.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Gomarus et al., 2009

      Not checked in the free run.

75 of 75
  • The paper relies on this without support.

    Working memory is among the most impaired executive functions in ADHD.

    “Meta-analyses identify working memory (WM) performance as one of the most impaired of executive processes in individuals with ADHD and have been noted to respond inconsistently to drug therapy.”
  • The paper relies on this without support.

    The predominant frontostriatal dysfunction model of ADHD predicts impairment across functions that rely on the prefrontal cortex.

    “These findings are contrary to the prediction of the predominant model of frontostriatal dysfunction in ADHD, which would predict impairment across PFC-related functions.”
  • The paper relies on this without support.

    Theta band spectral changes during the maintenance interval are associated with working-memory maintenance-related processes.

    “To the extent that these theta band spectral changes are associated with WM maintenance-related processes, these results indicate that during the maintenance interval children with ADHD activated these processes more strongly than TD children.”
  • The paper relies on this without support.

    The midfrontal P2 response to the fixation stimulus indexes vigilance.

    “These results indicate that children with ADHD had a weaker midfrontal cortical evoked response to the alerting fixation stimulus, consistent with weakened vigilance during the task.”
  • The paper relies on this without support.

    The occipital P1 indexes sensory visual processing.

    “We tested this explicitly by comparing the peak amplitude of the occipital P1, a positive potential occurring ϳ100 ms following stimulus onset and indexing sensory visual processing, in response to both fixation and the encoding stimuli.”
  • The paper relies on this without support.

    Age-related differences in the EEG measures reflect developmental maturation.

    “These data suggest that children with ADHD exhibit maturational delay in occipital mechanisms underlying both encoding and maintenance of spatial locations such that only older children with ADHD (and only at high-load) demonstrate the typical patterns of occipital alpha ERD/ERS.”
  • The authors state this as an assumption.

    Higher SWAN scores indicate lower symptom severity.

    “Note that SWAN scores correlate negatively with symptom severity (higher scores indicate lower severity of symptoms).”
  • The paper relies on this without support.

    Working memory performance in childhood is related to ADHD symptom severity, academic attainment, does not normalize over time, and predicts social functioning and other psychopathology over long-term follow-up.

    “The impact of these WM deficits is strongly supported by findings that WM performance in childhood is related to ADHD symptom severity, academic attainment, does not normalize over time, and predicts social functioning and the emergence of other psychopathology over long-term follow-up.”
8 of 8

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

Each contradiction between two passages listed here was confirmed by an independent check.

  • Group-specific diagnostic accuracy conflicts with sensitivity and specificity

    Minor

    The reported accuracy within the ADHD group is 71%, but sensitivity-accuracy among participants with ADHD-is given as 69%. Likewise, the TD group's 70% accuracy conflicts with the reported 72% specificity.

  • Age effect on response variability has opposite signs

    Minor

    The prose gives a positive age coefficient for RT variability while saying variability decreases with age. Table 2 instead reports a negative t value for the age effect on RT variability.

  • Hyperactivity regression t statistic changes sign

    Minor

    The prose reports a positive t statistic for encoding alpha and SWAN hyperactivity, whereas Table 2 reports a negative one. The negative table value also matches the negative coefficient stated in the prose.

3 of 3

Cites

Flagged first, then by citations

Research works printed but not linked: 2

  1. Berger, 1930, Electroencephalogram of humans, J Fur Psychologie Und Neurologie, 40, 160
  2. Robertson IH Garavan H (2004) in The cognitive neurosciences, Vigilant attention, ed Gazzaniga MS (MIT, Cambridge), Ed 3, pp 563–578.

Cited by

Sorted by citations

Authors
Lenartowicz, A., Delorme, A., Walshaw, P. D., Cho, A. L., Bilder, R. M., McGough, J. J., McCracken, J. T., Makeig, S., & Loo, S. K.
Affiliations
  • Centre National de la Recherche Scientifique (FR)
  • University of California, Los Angeles (US)
  • University of California San Diego (US)
Venue
The Journal of Neuroscience
Published
2014-01-22
Volume
34
Issue
4
Pages
1171-1182
ISSN
  • 0270-6474 (ISSN-L)
  • 1529-2401
OpenAlex
W2056082868
Cited by
158
References
73
Citations by year
2026: 7 · 2025: 6 · 2024: 16 · 2023: 10 · 2022: 16 · 2021: 15 · 2020: 14 · 2019: 12 · 2018: 14 · 2017: 11 · 2016: 16 · 2015: 12 · 2014: 9
FWCI
12.22
Type
journal article
Language
en
Open access
Locations
  • Journal of Neuroscience (publishedVersion, other-oa)
  • Europe PMC (PubMed Central) (publishedVersion)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
  • HAL (submittedVersion, other-oa)
  • eScholarship (California Digital Library) (submittedVersion)
  • eScholarship (California Digital Library) (submittedVersion, cc-by-nc-sa)
Funders
  • Servier
  • National Institutes of Health
  • University of California, San Diego
  • National Institute of Mental Health (MH092829, P50MH077248, MH077248, R03MH092829)
  • National Institute of Neurological Disorders and Stroke (NS047293, R01NS047293)
Topics
  • Health Sciences › Medicine › Psychiatry and Mental health › Attention Deficit Hyperactivity Disorder
  • Social Sciences › Psychology › Neuropsychology and Physiological Psychology › Developmental and Educational Neuropsychology
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
Keywords
attention deficit hyperactivity disorder, spatial working memory, sustained attention, memory encoding, memory maintenance, alpha event-related desynchronization, Sternberg task, children, EEG biomarkers, symptom severity
MeSH terms
Adolescent, Arousal, Attention, Attention Deficit Disorder with Hyperactivity, Child, Electroencephalography, Female, Humans, Male, Memory, Short-Term

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Claims read by deepseek-v4.1-flash under definition version 3 (extract-v3) on 2026-10-07.

Classified by jev-1.13-20260917 (gold-guideline-v0.2) on 2026-10-07.

Statistics and arithmetic are recomputed, not judged.

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