Altered proactive control in adults with ADHD: Evidence from event-related potentials during cued task switching
Introduction
Attention-deficit/hyperactivity disorder (ADHD) is a prevalent, early onset neurodevelopmental condition with symptoms of impaired attention, and/or excessive hyperactivity-impulsivity, interfering with functioning or development. Many of the ADHD-related problems have been linked to impairments in cognitive control processes, associated with structural and functional anomalies in the prefrontal cortex (Nigg and Casey, 2005; Tamm et al., 2004).
Cognitive control is conceptualised as an ability to flexibly adapt to changing circumstances by regulating behaviours so that inappropriate ones are suppressed and required ones are facilitated in response to environmental demands (Braver et al., 2003). Existing models of ADHD (Barkley, 1997; Nigg, 2005; Sergeant et al., 2003) and experimental evidence, implicate abnormalities in cognitive control as a factor significantly contributing to ADHD symptomatology (Durston, 2003; Durston et al., 2009; Willcutt et al., 2005). Children as well as adults with ADHD often perform poorer than their healthy counterparts on tasks probing cognitive control (e.g., Cepeda et al., 2000; Dibbets et al., 2010). Neuroimaging studies provide further evidence for the deep-seated nature of these cognitive control deficits persisting into adulthood by implicating activation, functional connectivity, electrophysiological and structural abnormalities, in brain areas underlying these functions (Bush et al., 2005; Castellanos and Proal, 2012; Cortese et al., 2012, 2013; Dickstein et al., 2006; Fried et al., 2014; Valera et al., 2007; Weyandt et al., 2013).
Braver's, 2012 model postulates cognitive control as a dual mechanism operating via two distinct control modes – proactive and reactive. Proactive control is a form of active goal-relevant information activation and maintenance that helps us to prepare for cognitively challenging events and primes the attentional and response systems for a required reaction. Reactive control, in contrast, involves transient goal-relevant information reactivation upon the detection of interference and its resolution (Braver, 2012; Braver et al., 2003). Hence, proactive control represents anticipatory preparation, triggered by contextual cues, prior to the occurrence of an event, while reactive control relates to the detection and resolution of conflict or interference after its onset. In the context of ADHD, studies probing cognitive control, have primarily focused on the reactive control mode, i.e., target-related disturbances. However, event-related potential (ERP) studies suggest that in individuals with ADHD inferior task performance and target-related aberrant brain activity may be preceded by altered preparatory processing during the cue-target phase in paradigms where a cue precedes the target, e.g., cued-CPT, which may reflect altered proactive control. These studies performed in adults and children with ADHD demonstrated a reduced cue-locked P3, reflecting reduced attentional orienting to cues, and diminished contingent negative variation (CNV) amplitudes, indicating less motor preparation or stimulus anticipation in ADHD (Albrecht et al., 2013; Banaschewski et al., 2008; Hauser et al., 2014; Kenemans et al., 2005; McLoughlin et al., 2010; Valko et al., 2009). Adult and child functional magnetic resonance (fMRI) studies have revealed abnormal signal patterns (mostly hypo-activation) during stimulus anticipation (Cubillo et al., 2010; Dibbets et al., 2010; Fassbender et al., 2015; Plichta and Scheres, 2014; Sidlauskaite et al., 2015; Ströhle et al., 2008). While these findings provide clear indications of deviant ADHD-related preparatory processes, there is little systematic research on proactive control in ADHD. In a simple cued paradigm, it is hardly possible to differentiate between cue-related preparatory alerting effects, priming the subject for upcoming events in a bottom-up fashion, and proactive cognitive control, which refers to an active use of cue information in order to prepare for future stimuli in a top-down manner.
A way to systematically study proactive control processes is to manipulate cue-informativeness, hence the load on proactive control. Without manipulating cue-informativeness, it is difficult to tell whether the reduced preparation reflects proactive control impairments or it is the result of reduced general alerting in ADHD, as cues may convey advance information about the task and also have a general alerting property. Manipulating cue-informativeness, especially in combination with ERPs, has been shown to be very successful for distinguishing proactive and reactive control processes in healthy and clinical populations (Jamadar et al., 2010a; Karayanidis et al., 2009; Barcelo and Cooper, 2016; Czernochowski, 2015; Kiesel et al., 2010; Whitson et al., 2014; Wylie et al., 2008), but surprisingly has not yet been applied in ADHD. In the current study, we therefore followed this approach in order to disentangle the processes implicated in proactive and reactive control and to examine their modulation in a sample of adults with ADHD and healthy controls. We measured ERPs during a cued task switching paradigm, based on the work of Jamadar and colleagues (Jamadar et al., 2010a).
Task switching paradigms are frequently used as proxies to investigate cognitive control processes involved in cognitive flexibility (Kok et al., 2006; Ruge et al., 2013). In such paradigms, participants have to repeat or switch between tasks. Typically, participants respond more slowly on switch versus repeat trials – referred to as the switch cost. In cued task switching paradigms, the switches or repeats can be indicated at the cue level, enabling investigation of proactive control processes. As in previous research (e.g., Jamadar et al., 2010a), in the current study we included informative as well as non-informative alerting cues. Informative cues indicate a repeat or switch target, rendering advance anticipatory preparation, while non-informative cues act as an alerting signal, signalling that the target is about to appear without specific task information (a repeat or a switch) at the cue level. By studying cue- and target-locked ERPs, one can investigate covert proactive and reactive control processes, which is not possible with behavioural measures alone (reaction time or switch cost), that represent the cumulative endpoint of all these processes.
Within cued task switching paradigms, proactive control is reflected by the usage of informative cues to prepare for an upcoming task. Research applying such paradigms has revealed two cue-locked ERP components linked to the usage of cue information. Both components have a parietal scalp distribution but have been shown to have distinct temporal and functional characteristics. First, the informative-positivity (~300 ms post cue) – is linked to the information content of a cue, appearing as a difference ERP component in the contrast between informative and non-informative alerting cues. Hence, the informative-positivity has been argued to index early task-goal related activation processes (e.g., perform the colour, not the shape task), as well as the orienting of selective attention (e.g., attend to the colour, ignore the shape) (Jamadar et al., 2010a; Karayanidis et al., 2010a, 2010b; Swainson et al., 2006). This component is followed by the switch-positivity (~450 ms post-cue), reflecting differential switch-related activity (greater for switch than repeat trials), specifically for informative cues. The switch-positivity has been argued to be an index of anticipatory task-set reconfiguration and specific response rule activation (e.g., colour task, blue stimulus – press left button; yellow stimulus – press right button) (Jamadar et al., 2010a; Karayanidis et al., 2010a, 2010b; Swainson et al., 2006).
Target-locked ERPs, related to reactive control, also show differential switch-related activity. A decrease in parietal positive activity has been observed for switch relative to repeat trials, referred to as the switch-negativity. This component reflects the effort to overcome interference due to task-set inertia that cannot be initiated until stimulus onset (Karayanidis et al., 2011).
In keeping with the hypothesis of impaired proactive control processes, we expected adults with ADHD to show a smaller cue-locked informative-positivity (comparing informative to non-informative alerting cues, as in Jamadar et al., 2010a) and/or smaller switch-positivity (comparing informative cue switches to informative cue repeats, as in Jamadar et al., 2010a). The target-locked switch-negativity amplitude was also examined to explore potential group differences in processes related to reactive control. Finally, we also included no-cue trials in our paradigm, in which switch or repeat targets were not preceded by any cue. This manipulation allowed us to additionally test for potential group differences in general alerting.
Section snippets
Participants
Twenty-three adults with a clinical diagnosis of ADHD (9-inattentive type; 14-combined type) and 23 healthy control individuals participated. Each participant gave their written informed consent prior to the study and received a monetary reward for participation. The study was approved by the local ethics committee. Both groups of participants were recruited via advertising in local magazines, social websites, word-of-mouth, or from the lab's pool of participants who had agreed to be contacted
Behavioural data
Fig. 2 depicts RTs per cue type and switch/repeat condition. There was a main effect of cue type on RT (F(1.46, 64.34) = 674.64, p < 0.001; η2 = 0.939) – participants responded fastest during informative cue trials (M = 692.09 ms), followed by alerting (M = 952.74 ms) and no-cue (M = 995.30) conditions (all conditions differed significantly from each other, all p's < 0.001). Switch and repeat conditions also differentially modulated RT (F(1, 44) = 79.82, p < 0.001; η2 = 0.645) – participants
Cue-locked
As depicted in the difference waves in Fig. 4A (raw cue-locked ERPs are shown in Fig. 3; for topographies please see Supplementary material), there is an early difference in cue-related activity between informative and alerting cues, referred to as the informative-positivity, 300–500 ms post cue at POz (see also Jamadar et al., 2010a).
The repeated measures ANOVA showed a main effect of cue type (F(1, 44) = 58.13, p < 0.001; η2 = 0.569), i.e., amplitudes were more positive for cue-locked
Discussion
In the current experiment, we tested for ADHD-related proactive and reactive control impairments by measuring EEG during performance on a cued task switching paradigm, in which cue-informativeness was manipulated. In accord with previous studies, we observed the cue-locked informative-positivity and switch-positivity, and the target-locked switch-negativity (Jamadar et al., 2010b, c). Groups did not differ for task-switching at the performance level; adults with ADHD tended to respond slower
Conclusions
In the current EEG experiment, we investigated cognitive control processes in adults with ADHD from the perspective of Braver’s (2012) dual model of cognitive control. At the performance level, only a trend to generally slower responding was found in the ADHD group. The ERP findings however suggest preparatory proactive rather than reactive cognitive control difficulties in adults with ADHD, evidenced by reduced usage of cue information and potentially deviant preparatory switch-related
Acknowledgments
This work is supported by the Fund for Scientific Research - Flanders (project number: 3G084810).
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