Transition from reactive control to proactive control across conflict adaptation: An sLORETA study

Highlights

• Alpha activity was enhanced in trials preceded by incompatible stimuli.

• N1 amplitude was decreased in trials preceded by incompatible stimuli.

• The superior/medial frontal cortex was associated with proactive control.

• The right inferior frontal cortex was associated with reactive control.

• Frontal alpha activity was negatively correlated with N1.

Abstract

In a flanker task, behavioral performance is modulated by previous trial compatibility (i.e., conflict adaptation); a longer response time (RT) is found for a compatible stimulus preceded by an incompatible stimulus than by a compatible stimulus, whereas a shorter RT is found for an incompatible stimulus preceded by an incompatible stimulus than by a compatible stimulus. We examined the temporal characteristics of cognitive control across conflict adaptation using prestimulus electroencephalogram oscillatory activity and an event-related potential component, N1. Prestimulus frontal (Fz) and posterior (O1 and O2) alpha1 (7–9 Hz) and alpha2 (10–13 Hz) activities were enhanced in trials preceded by incompatible stimuli more than those preceded by compatible stimuli. Furthermore, there were significant differences of alpha2 current densities between previous trial compatibilities in the superior/medial frontal cortex. We suggested that the modulation of alpha activity by previous trial compatibility was associated with proactive attentional control. N1 amplitude was decreased in trials preceded by incompatible stimuli more than in those preceded by compatible stimuli. N1 current densities in the right inferior frontal cortex were smaller for an incompatible stimulus preceded by an incompatible stimulus than those preceded by a compatible stimulus, suggesting that demands of transient cognitive control induced by an incompatible stimulus were decreased by the proactive control. Moreover, correlational analysis showed that participants with a larger increase in alpha2 activity tended to have a larger decrease in N1 in trials preceded by incompatible stimulus. These findings revealed that the manner of cognitive control for the incompatible stimulus was transited from reactive control to proactive control across conflict adaptation.

Introduction

It is important for adaption to the environment to be able to flexibly change the manner of cognitive control according to the context. Types of cognitive control are temporally distinguished into at least two cognitive controls (Braver, 2012, Braver et al., 2009),¹ i.e., “proactive” control and “reactive” control. Proactive control represents anticipatory and preparatory attentional control for the interference of the upcoming stimulus. Reactive control is postulated as transient recruitment of cognitive control after the stimulus presentation.

Cognitive control has been well-studied using interference tasks such as the flanker task (Eriksen & Eriksen, 1979), the Stroop task (Stroop, 1935), and the Simon task (Simon, 1969). For example, in the flanker task, participants are required to respond to targets presented in the central visual field, while flankers appear that aid (i.e., a compatible stimulus) or interfere with (i.e., an incompatible stimulus) participants’ accomplishment of the task. Gratton, Coles, and Donchin (1992) reported that shorter response times (RTs) and higher accuracies were observed for a compatible stimulus preceded by a compatible stimulus (cC) than by an incompatible stimulus (iC), whereas longer RTs and lower accuracies were observed for an incompatible stimulus preceded by a compatible stimulus (cI) than by an incompatible stimulus (iI). This phenomenon is called conflict adaptation (or the Gratton effect).

Conflict has been used to refer to the competition between target information and irrelevant information induced by an incompatible stimulus (Botvinick, Braver, Barch, Carter, & Cohen, 2001). Researchers have interpreted conflict adaptation as a cognitive control mechanism driven by the degree of conflict (Botvinick et al., 2001). Then, it is hypothesized that a high degree of conflict (i.e., induced by an incompatible stimulus) causes the attention to be focused on the central visual field in order to inhibit the interference of flankers on the next trial, whereas a low degree of conflict (i.e., induced by a compatible stimulus) makes the attentional area broaden in order to utilize information about flankers on the next trial (Botvinick et al., 2001, Kerns et al., 2004). In accordance with this hypothesis, cognitive control is transiently required to resolve a high degree of conflict when an incompatible stimulus is presented after a compatible stimulus (Wang et al., 2015). On the other hand, when responding to an incompatible stimulus preceded by an incompatible stimulus, cognitive control is preliminarily executed before the presentation of the stimulus. Thus, we postulate that conflict adaptation is associated with a transition from reactive control to proactive control.

An oscillation of the electroencephalogram (EEG) or magnetoencephalogram (MEG) of approximately 10 Hz (i.e., alpha) is sensitive to the proactive attentional state before the stimulus presentation. Typically, enhanced alpha activity in a sensory area is interpreted as functional inhibition (Klimesch, Sauseng, & Hanslmayr, 2007). Consistent with this view, enhanced posterior alpha activity predicted a decrease in the visual perceptual performance (Babiloni et al., 2006, Ergenoglu et al., 2004, Hanslmayr et al., 2007). Moreover, the change in alpha activity has been considered as reflecting top-down attentional control, which enhances relevant sensory inputs and inhibits irrelevant ones. Several previous studies have shown that posterior alpha activity is enhanced on the ipsilateral side of the visual field attended to, while it is attenuated at the contralateral side (Freunberger et al., 2008, Rihs et al., 2007, Rihs et al., 2009, Sauseng et al., 2005, Thut et al., 2006, Worden et al., 2000). In terms of interference tasks, Compton, Huber, Levinson, and Zheutlin (2012) reported that alpha activity is reduced in trials preceded by compatible stimuli in the Stroop task, as compared with neutral stimuli, suggesting that reduced alpha activity is related to the enhancement of information processing about the irrelevant aspect. In addition, Min and Park (2010) examined prestimulus alpha activity in color and shape discrimination tasks, in which participants discriminated colors or shapes of objects, ignoring other aspects. They reported that task performance was worse and posterior alpha activity was enhanced more for the shape-discrimination task than the color task, suggesting that alpha activity was enhanced for inhibition of irrelevant sensory processing. These findings suggest that proactive control for the inhibition of flankers is associated with an increase in posterior alpha activity during the prestimulus interval.

Posterior alpha activity has been reported to be regulated by frontoparietal areas. Previous studies have shown that the reduced excitability in the frontal eye fields and intraparietal sulcus cause the loss of the modulation of posterior alpha activities by the attending visual field (Capotosto et al., 2009, Sauseng et al., 2011). A simultaneous EEG and functional magnetic resonance imaging (fMRI) study has shown that activity of the superior/medial frontal cortex is positively correlated with alpha lateralization by selective attention (Liu, Bengson, Huang, Mangun, & Ding, 2014). Rana and Vaina (2014) reported that alpha activity of frontoparietal areas was increased when controlling spatial attention. Thus, it is predicted that the alpha activity derived from these regions is also modulated by previous trial compatibility.

We consider that N1 reflects the demands of the recruitment of cognitive control after stimulus presentation. N1 is an event-related potential (ERP) component observed as a negative peak from 100 to 200 ms at the occipital scalp electrode (Hillyard, Teder-Salejarvi, & Munte, 1998), preceding ERP components relevant to detection of conflict (i.e., N2 and ERN; Yeung, Botvinick, & Cohen, 2004). Typically, N1 is called a “mesogenous” component (Fabiani & Gratton, 2007). That is, both physical stimulus properties (e.g., size and luminance) and internal processing (e.g., attention) influence N1 (Johannes, Munte, Heinze, & Mangun, 1995). Some previous studies have reported the inverse relationship between N1 and the prestimulus alpha activity (Basar and Stampfer, 1985, Rahn and Basar, 1993), suggesting that N1 is reduced by the functional inhibition of sensory processing concerning flankers associated with alpha activity. Thus, it is predictable that N1 would be enhanced in trials preceded by compatible stimuli as compared with those preceded by incompatible stimuli, as the visual area of flankers is not inhibited before stimulus presentation.

The main purpose of this study is to elucidate the change in cognitive control across conflict adaptation. Thus, we examine the difference of alpha activity and N1 between previous trial compatibilities. Furthermore, we estimate the source of alpha activity and N1 associated with conflict adaptation using standardized Low Resolution Brain Electromagnetic Tomography (sLORETA) (Pascual-Marqui, 2002).