Neural mechanisms underlying successful and deficient multi-component behavior in early adolescent ADHD

Abstract

Attention Deficit Hyperactivity Disorder (ADHD) is a disorder affecting cognitive control. These functions are important to achieve goals when different actions need to be executed in close succession. This type of multi-component behavior, which often further requires the processing of information from different modalities, is important for everyday activities. Yet, possible changes in neurophysiological mechanisms have not been investigated in adolescent ADHD. We examined N = 31 adolescent ADHD patients and N = 35 healthy controls (HC) in two Stop-Change experiments using either uni-modal or bi-modal stimuli to trigger stop and change processes. These stimuli were either presented together (SCD0) or in close succession of 300 milliseconds (SCD300). Using event-related potentials (ERP), EEG data decomposition and source localization we analyzed neural processes and functional neuroanatomical correlates of multicomponent behavior. Compared to HCs, ADHD patients had longer reaction times and higher error rates when Stop and Change stimuli were presented in close succession (SCD300), but not when presented together (SCD0). This effect was evident in the uni-modal and bi-modal experiment and is reflected by neurophysiological processes reflecting response selection mechanisms in the inferior parietal cortex (BA40). These processes were only detectable after accounting for intra-individual variability in neurophysiological data; i.e. there were no effects in standard ERPs. Multi-component behavior is not always deficient in ADHD. Rather, modulations in multi-component behavior depend on a critical temporal integration window during response selection which is associated with functioning of the inferior parietal cortex. This window is smaller than in HCs and independent of the complexity of sensory input.

Keywords: ADHD; Cognitive control; Event related potential (ERP); Multi-component behavior, inferior parietal cortex; Neurophysiology.

Fig. 1

Schematical illustration of the experimental setup. Participants were presented with a visual GO signal (white circle) above or below a central horizontal line at the beginning of all trials. In GO trials, the subjects needed to respond with the right hand (middle finger = “above” response, index finger = “below” response). In stop-change trials, the GO stimulus was followed by a visual STOP stimulus (red rectangle, see middle) after a variable and individually adjusted stop-signal delay (SSD). The CHANGE stimulus was either presented with a stimulus onset asynchrony (SOA)/stop-signal delay (SCD) of 0 ms or of 300 ms after the STOP stimulus. The CHANGE stimulus now indicated that the response needed to be made with the left hand. In the unimodal task, the CHANGE stimulus was a bold yellow line. By contrast, the bimodal task used 200 ms sine tones (1300 Hz, 900 Hz, and 500 Hz) as CHANGE stimuli. Participants were thus required to change their response according to the new indicated line (middle finger = “above” response, index finger = “below” response) or the pitch of the tone (middle finger = “high pitch”, index finger = “low pitch”).

Fig. 2

Behavioral data showing the RTs (top) and the frequency of errors (bottom) for the control and the ADHD group in the SCD0 (black bars) and the SCD300 condition (white bars). The mean and standard error of the mean are given.

Fig. 3

RIDE S-cluster data at electrodes Cz (top), pooled across P7/P8 (middle) and pooled across TP7/TP8 (bottom). The data are shown pooled across the uni-modal and the bi-modal condition, because there was no difference between these conditions. The different colors denote the different experimental conditions (SCD0, SCD300) in combination with the respective group (ADHD, controls). Time point zero denotes the time point of the STOP stimulus presentation. The scalp topographies for the ADHD and the control group are shown for the different condition (SCD0, SCD300). In the scalp topographies, blue colors show negativity, red colors positivity. The topographies are shown for the maximum amplitudes in the respective time windows for peak quantification as outlined in the methods section.

Fig. 4

RIDE C-cluster data at electrodes Cz (top), and CP4 (bottom). The data are shown pooled across the uni-modal and the bi-modal condition. The different line colors denote the different experimental conditions (SCD0, SCD300) in combination with the respective group (ADHD, controls). Time point zero denotes the time point of STOP stimulus presentation. The scalp topographies for the ADHD and the control group are shown for the different condition (SCD0, SCD300). In the scalp topographies, blue colors show negativity, red colors denote positivity. The topographies are shown for the maximum amplitudes in the respective time windows for peak quantification as outlined in the methods section. The sLORETA plots show activation differences between the groups in the SCD300 condition in the inferior parietal cortex (corrected for multiple comparisons). The sLORETA color scale shows critical t-values.

Fig. 5

RIDE R-cluster data at electrodes C4. The data are shown pooled across the uni-modal and the bi-modal condition, because there was no difference between these. The different line colors denote the different experimental conditions (SCD0, SCD300) in combination with the respective group (ADHD, controls). Time point zero denotes the time point of STOP stimulus presentation. The scalp topographies for the ADHD and the control group are shown for the different condition (SCD0, SCD300). In the scalp topographies, blue colors show negativity, red colors denote positivity. The topographies are shown for the maximum amplitudes in the respective time windows for peak quantification as outlined in the methods section.