Early Attentional Modulation by Working Memory Training in Young Adult ADHD Patients during a Risky Decision-Making Task

Abstract

Background: Working memory (WM) deficits and impaired decision making are among the characteristic symptoms of patients affected by attention deficit/hyperactivity disorder (ADHD). The inattention associated with the disorder is likely to be due to functional deficits of the neural networks inhibiting irrelevant sensory input. In the presence of unnecessary information, a good decisional process is impaired and ADHD patients tend to take risky decisions. This study is aimed to test the hypothesis that the level of difficulty of a WM training (WMT) is affecting the top-down modulation of the attentional processes in a probabilistic gambling task. Methods: Event-related potentials (ERP) triggered by the choice of the amount wagered in the gambling task were recorded, before and after WMT with a the dual n-back task, in young ADHD adults and matched controls. For each group of participants, randomly assigned individuals were requested to perform WMT with a fixed baseline level of difficulty. The remaining participants were trained with a performance-dependent adaptive n-level of difficulty. Results: We compared the ERP recordings before and after 20 days of WMT in each subgroup. The analysis was focused on the time windows with at least three recording sites showing differences before and after training, after Bonferroni correction ( p < 0.05 ). In ADHD, the P1 wave component was selectively affected at frontal sites and its shape was recovered close to controls' only after adaptive training. In controls, the strongest contrast was observed at parietal level with a left hemispheric dominance at latencies near 900 ms, more after baseline than after adaptive training. Conclusion: Partial restoration of early selective attentional processes in ADHD patients might occur after WMT with a high cognitive load. Modified frontal sites' activities might constitute a neural marker of this effect in a gambling task. In controls, conversely, an increase in late parietal negativity might rather be a marker of an increase in transfer effects to fluid intelligence.

Keywords: EEG; ERP; N500; P1; P3b; cognitive remediation; late parietal negativity; late posterior negative slow wave; selective attention; working-memory training.

Figure 1

Level n = 2 of the dual n-back task. Each stimulus was composed by an auditory and a visual cue presented during 500 ms. This means the participants had to compare the third stimulus (S3) with the first one (S1), S4 with S2, S5 with S3, and so on. For the first correct response (R1), no stimuli matched those presented two trials back in time and no key press was requested. For R2, both auditory and visual stimuli matched the target (S4 identical to S2, green arrow)), such that both “A” and “L” key were pressed. For R3, only the auditory stimulus matched the target (red arrow) and only the “L” key was pressed. For R4, only the visual stimulus matched the target (blue arrow) and only the “A” key was pressed. Notice that in this example only correct responses are illustrated.

Figure 2

Probabilistic gambling task. A trial started when the participant pressed the spacebar (event S in the timeline), followed (20 milliseconds later) by a screen with a message request to select the gamble. This screen stayed on until a response was made by clicking on the selected value of gamble (event 0). The response time was determined by the interval between that message and the selection of gamble. This button click (event 0) was used as triggering event for the electrophysiological analysis. A fixed interval of 4000 ms followed until the end of the trial with the same screen and with the highlighted selected gamble.

Figure 3

Grand average event-related potentials (ERPs) recorded before the working memory (WM) training at Fz, Cz and Pz sites triggered at lag 0, corresponding to button-click of the selected gamble, in attention deficit/hyperactivity disorder (ADHD) ($N=28$, green curves over light green shaded areas) and control participants ($N=37$, white curves over brown shaded areas) on a millisecond scale. The confidence interval (mean curve ± SEM) is shown by the shaded areas. We identified the decision preceding negativity (DPN), P1-like, N2, P3a, N500, and a late parietal negativity (LPN). Signal amplitude is scaled in microvolts ($\mathsf{\mu }$V). The topographic maps on the top represent the distribution of the mean amplitude of the signal between 70 and 120 ms (estimated P1-like component) using a color-coded scale in $\mathsf{\mu }$V.

Figure 4

Differential head maps of the topographical distribution of the Grand-Average ERP amplitude (in $\mathsf{\mu }$V) at post- minus pre-training sessions for ADHD and controls trained either by the baseline or adaptive protocol of the dual n-back task. ERPs were triggered by the choice of the selected gamble with the button-click. Differential head maps using a color-coded scale in $\mathsf{\mu }$V are plotted for the five major ERP time windows. The red squares correspond to those head maps with significant Bonferroni-corrected p-values in the given time window, computed from paired t-tests on the individual average signals (see Figure 5).

Figure 5

Grand average ERPs, triggered (at lag 0 ms) by the button-click at the time of the selection of the amount to gamble, recorded before working memory training (blue curves and shaded areas). The confidence interval (mean curve ± SEM) is shown by the shaded areas. The vertical scale represents the amplitude of the signal in $\mathsf{\mu }$V and the lag is scaled in milliseconds. (a). Grand average ERPs at sites F3, F4, Fz, FCz and Cz sites (blue marks in the head map) for ADHD participants recorded after training with the adaptive level protocol (red curves and shaded areas) for the dual n-back task. Green ticks show the significant Bonferroni-corrected $1-p$ values computed from paired t-test on individual average ERP signal with significance $p<0.05$ (**) and $p<0.01$ (***). The panel at the top, shows a head map with the significant sites after Bonferroni correction (red areas around F3, Fz and FCz), at a latency of 100 ms (dashed green vertical line), corresponding to the P1-like component discussed in the text. (b). Grand average ERPs at sites P1, P2, P5, Pz, POz, and Cz sites (blue marks in the head map) for controls recorded after training with the baseline level protocol (orange curves and shaded areas), i.e., after the dual 1-back task. In this figure, the head map on the top shows the significant sites (in red areas around P1, P2, P5, CP3 and POz) at a latency of 912 ms (dashed green vertical line), corresponding to the slow negative wave component associated with the expectation of the gambling outcome.