Altered cortical activation associated with mirror overflow driven by non-dominant hand movement in attention-deficit/hyperactivity disorder

Abstract

Mirror overflow is involuntary movement that accompanies unilateral voluntary movement on the opposite side of the body, and is commonly seen in Attention-Deficit/Hyperactivity Disorder (ADHD). Children with ADHD show asymmetry in mirror overflow between dominant and non-dominant hand, yet there are competing mechanistic accounts of why this occurs. Using EEG during a sequential, unimanual finger-tapping task, we found that children with ADHD exhibited significantly more mirror overflow than typically developing (TD) controls, especially during the tapping of the non-dominant hand. Furthermore, source-level EEG oscillation analysis revealed that children with ADHD showed decreased alpha (8-12 Hz) event-related desynchronization (ERD) compared with controls in both hemispheres, but only during tapping of the non-dominant hand. Moreover, only the ERD ipsilateral to the mirror overflow during non-dominant hand movement correlated with both magnitude of overflow movements and higher ADHD symptom severity (Conners ADHD Hyperactivity/Impulsiveness scale) in children with ADHD. TD controls did not show these relationships. Our findings suggest that EEG differences in finger-tapping in ADHD are related primarily to voluntary movement in the non-dominant hand. Our results are also consistent with the Ipsilateral Corticospinal Tract (CST) Hypothesis, which posits that the atypical persistence of mirror overflow in ADHD may originate in the sensorimotor areas ipsilateral to mirror overflow and be transmitted via non-decussating CST fibers.

Keywords: Attention-deficit/hyperactivity disorder; Event-related desynchronization; Hand skill asymmetry; Mirror overflow.

Figure 1.

Behavioral mirror overflow results. (A) and (B) showed mirror overflow in children with ADHD and TD controls during LHFT and RHFT, respectively. Children with ADHD demonstrated significantly greater amount of mirror overflow than TD controls during LHFT only. (C) and (D) showed mirror overflow during LHFT vs. RHFT in both ADHD and TD groups. Children with ADHD had significantly more mirror overflow during LHFT than RHFT, but TD participants did not. *p<0.05, **p<0.01. Error bars are the standard error of the mean (s.e.m.) and n.s. denotes not significant.

Figure 2.

Alpha ERD in children with ADHD and TD controls during LHFT and RHFT. Children with ADHD showed decreased alpha ERD compared with TD controls in contralateral and ipsilateral sensorimotor areas, especially during LHFT.

Figure 3.

Between-group differences in contralateral and ipsilateral alpha ERD during both LHFT and RHFT in both ADHD and TD group. The two groups differed significantly during LHFT in (A) contralateral alpha ERD in sensorimotor areas, and (B) ipsilateral alpha ERD in sensorimotor areas. No diagnostic effect was observed for RHFT in either (C) contralateral and (D) ipsilateral alpha ERD. In summary, group differences were seen in both ipsilateral and contralateral sensorimotor areas during LHFT but not RHFT. *p<0.05, **p<0.01, and n.s. = not significant. Error bars are the standard error of the mean (s.e.m.).

Figure 4.

Within-group, between-hand differences in contralateral and ipsilateral alpha ERD in sensorimotor areas. Children with ADHD showed significant differences in contralateral (A) and ipsilateral alpha ERD (B) in sensorimotor areas between LHFT vs. RHFT, whereas TD controls did not show significant differences in contralateral (C) or ipsilateral alpha ERD (D) between LHFT vs. RHFT. *p<0.05, **p<0.01, and n.s. = not significant. Error bars are the standard error of the mean (s.e.m.).

Figure 5.

Correlations between contralateral alpha ERD and behavioral overflow during LHFT and RHFT in children with ADHD vs. TD controls. (A) and (B) showed correlations between behavioral overflow and contralateral or ipsilateral alpha ERD during LHFT in the ADHD and TD group. (C) and (D) showed correlations between behavioral overflow and contralateral or ipsilateral alpha ERD during RHFT in the ADHD and TD group. Note that the regression lines have different slopes by group for LHFT but not for RHFT; restated, the relationship between overflow (behavior) and contralateral ERD (brain) is different for children with ADHD vs. TD controls, but only for LHFT (moderation effect p=0.04). Significant correlation was seen in the relationship between overflow and contralateral ERD in sensorimotor areas (p = 0.004).

Figure 6.

Correlations between ADHD symptoms and alpha ERD. (A) showed correlations between contralateral alpha ERD during LHFT and Conners ADHD Hyperactivity/Impulsiveness (Conners H/I) in the ADHD and TD group. (B) showed correlations between ipsilateral alpha ERD during LHFT and Conners H/I in the two groups. There were significant correlation between contralateral alpha ERD and Conners H/I in children with ADHD during LHFT, whereas the contralateral alpha ERD of TD controls did not show a linear relationship with Conners ADHD Hyperactivity/Impulsiveness.

Figure 7.

Mirror overflow models. (A) showed the Transcallosal Hypothesis, (B) showed the Ipsilateral CST Hypothesis. Contralateral hemisphere and ipsilateral hemisphere in the figure refer to contralateral/ipsilateral to the voluntary movement, whereas “ipsilateral” in the title of the Ipsilateral CST Hypothesis refers to non-decussating CST fibers that travel to the hand with overflow from the hemisphere ipsilateral to the overflow hand.