The system-neurophysiological basis for how methylphenidate modulates perceptual-attentional conflicts during auditory processing

Abstract

The ability to selectively perceive and flexibly attend to relevant sensory signals in the environment is essential for action control. Whereas neuromodulation of sensory or attentional processing is often investigated, neuromodulation of interactive effects between perception and attention, that is, high attentional control demand when the relevant sensory information is perceptually less salient than the irrelevant one, is not well understood. To fill this gap, this pharmacological-electroencephalogram (EEG) study applied an intensity-modulated, focused-attention dichotic listening paradigm together with temporal EEG signal decomposition and source localization analyses. We used a double-blind MPH/placebo crossover design to delineate the effects of methylphenidate (MPH)-a dopamine/norepinephrine transporter blocker-on the resolution of perceptual-attentional conflicts, when perceptual saliency and attentional focus favor opposing ears, in healthy young adults. We show that MPH increased behavioral performance specifically in the condition with the most pronounced conflict between perceptual saliency and attentional focus. On the neurophysiological level, MPH effects in line with the behavioral data were observed after accounting for intraindividual variability in the signal. More specifically, MPH did not show an effect on stimulus-related processes but modulated the onset latency of processes between stimulus evaluation and responding. These modulations were further shown to be associated with activation differences in the temporoparietal junction (BA40) and the superior parietal cortex (BA7) and may reflect neuronal gain modulation principles. The findings provide mechanistic insights into the role of modulated dopamine/norepinephrine transmitter systems for the interactions between perception and attention.

Keywords: EEG; attention; auditory; conflict; dopamine; methylphenidate; norepinephrine; perception; source localization.

Figure 1

Behavioral data showing (a) performance accuracy (hit rate) and (b) reaction times (RTs). The different experimental conditions are shown on the x‐axis for the placebo (light gray) and the MPH condition (dark gray). The mean and SEM are shown

Figure 2

(a) ERPs showing the P1 and N1 ERP component at electrode C5 (top) and electrode C6 (bottom). The scalp topography plots show the voltage distribution across the scalp for the peak of the P1 and the N1 in all high conflict experimental conditions. (b) The N2 ERP component is shown pooled across electrode Cz and FCz. (c) the N450 ERP component is shown. The scalp topography plots in (b) and (c) show the placebo and MPH condition for high conflict trials in the FL and FR condition. Time point zero denotes the time point of target stimulus presentation. The different colors denote the experimental conditions as stated in the figure. In the scalp topography plots, negative amplitudes are shown in blue, positive amplitudes in red [Color figure can be viewed at http://wileyonlinelibrary.com]

Figure 3

(a) The C‐cluster data at electrode Cz are shown. Time point zero denotes the time point of target stimulus presentation. The different colors denote the experimental conditions as stated in the figure. (b) The drug effect (placebo minus MPH) is shown for the C‐cluster at electrode Cz. As can be seen, there is a strong drug effect in the FL high conflict condition. The scalp topography plots show the voltage distribution across the scalp for this drug effect in the experimental conditions. The sLORETA plots show the source of the differences in the magnitude of the drug effect in the left inferior and superior parietal cortex (BA40 and BA7) (corrected for multiple comparisons). (c) C‐cluster data at electrode Cz are shown for the high conflict trials (left plot) and low conflict trials (right plot). Strong shifts in the C‐cluster onset latency can be seen between the placebo and MPH condition for FL high conflict trials [Color figure can be viewed at http://wileyonlinelibrary.com]