ERP indices for response inhibition are related to anxiety-related personality traits

Abstract

Anxiety is often associated with impaired cognitive control and avoidance behaviour. The aim of this study was to investigate the effect of anxiety-related personality traits, such as anxiety sensitivity and trait anxiety, on event-related potentials of response inhibition in a standard Go/Nogo-paradigm. We focused on the Nogo-N2 and Nogo-P3 components, which probably represent different sub-processes of response inhibition. The Nogo-N2 was mainly influenced by trait anxiety, while it was slightly affected by anxiety sensitivity. In contrast, the Nogo-P3 was significantly associated with anxiety sensitivity, but was less affected by trait anxiety. Thus, anxious subjects seem to maintain a higher level of cognitive control to prepare and to monitor the outcome of their actions, which is differentially reflected in Nogo-N2 and Nogo-P3 potentials. Our results show that anxiety-related personality traits modulate electrophysiological responses related to cognitive control processes and should be taken into consideration in studies investigating response inhibition.

Introduction

Executive functions control cognitive processes. According to the theoretical model of Norman and Shallice (1986), the executive system is especially involved in planning, error correction, and the adaptation to novel situations (Norman and Shallice, 1986, Posner and Dehaene, 1994). Response inhibition, another component of this control system (Mostofsky & Simmonds, 2008), is described as the suppression of actions that are inappropriate in a given context. It can be examined experimentally in a Go/Nogo-task using event-related potentials (ERPs). In such a paradigm, subjects should respond to one target stimulus in the Go-condition and withhold responses to the target stimulus in the Nogo-condition.

Two fronto-central event-related potentials (ERPs) have been associated with larger amplitudes in Nogo- than in Go-trials (Eimer, 1993, Falkenstein et al., 1999). These components have been labelled as Nogo-N2 and Nogo-P3, and are considered to represent different sub-processes of response inhibition. The Nogo-N2 is assumed to reflect inhibition or revision of a motor plan prior to motor execution. In contrast, the Nogo-P3 has been associated with motor inhibition (Falkenstein et al., 1999, Smith et al., 2008, Zordan et al., 2008), but due to its long latency it has also been suggested that it reflects the monitoring of the outcome of inhibition (Righi et al., 2009, Schmajuk et al., 2006). Furthermore, both components seem to be differentially modulated by distinct neurobiological systems (Beste et al., 2010a, Beste et al., 2010b) supporting the assumption of different sub-processes of response inhibition.

Response inhibition and cognitive control have been associated with activity within the anterior cingulate cortex (ACC) and other frontal brain areas (Beste et al., 2008, Bokura et al., 2001, Falkenstein, 2006). Furthermore, the ACC is important for the integration of cognitive and emotional processes (Bush, Luu, & Posner, 2000), for the pathophysiology of psychiatric disorders (Damsa, Kosel, & Moussally, 2009), and is a crucial part of the human anxiety circuitry (Sehlmeyer et al., 2009). Patients with anxiety disorders may be characterized by neurocognitive deficits in inhibitory processing and response monitoring. While some studies observed smaller Nogo-N2 amplitudes (Herrmann et al., 2003, Kim et al., 2007), others found hyperactivation of the ACC (Ursu, Stenger, Shear, Jones, & Carter, 2003), enhanced Nogo-N2 and consequently increased response inhibition (Ruchsow et al., 2007).

While patients with anxiety disorders may show some degree of response over-inhibition, the question remains whether personality traits, which are closely related to pathological anxiety (Chambers et al., 2004, Naragon-Gainey, 2010, Schmidt et al., 2008), can also modulate cognitive functions, such as response inhibition, and electrophysiology, such as Nogo-components. There are two major psychological concepts concerning anxiety-related personality traits that may be linked to response inhibition: trait anxiety (TA) and anxiety sensitivity (AS). TA describes the tendency to respond fearfully to a wide variety of unspecific stressors, and the need for both security and cognitive control (Fales et al., 2008). In contrast, AS represents the specific tendency to respond fearfully to one's own bodily sensations and anxiety-related symptoms, which is based on the belief that these symptoms are harmful (McNally, 2002). It has been a matter of controversial debates whether AS and TA represent common or different concepts of anxiety (Lilienfeld, 1996, McNally, 1996, McWilliams and Cox, 2001, Muris et al., 2001). Actually, it is assumed that they both are related to each other and focus each on different facets of anxiety. While TA concentrates on cognitive anxiety symptoms, AS refers to physical and psychological anxiety symptoms.

In general, the interplay of anxiety traits, cognitive individual differences and electrophysiology has been investigated by recent research (Karch et al., 2008, Manly et al., 1999, Roche et al., 2005). For example, it has been shown that subjects with high trait anxiety or anxiety sensitivity display anxiety-related attentional biases (Bar-Haim, Lamy, Pergamin, Bakermans-Kranenburg, & van, 2007) and may thus show modified ERP components, cognitive performances (flanker task: Dennis and Chen, 2009, Moser et al., 2005; n-back: Holmes, Nielsen, Tipper, & Green, 2009; stroop: Taake, Jaspers-Fayer, & Liotti, 2009 or processing of affective information Carretie et al., 2004, Dennis and Chen, 2007, Fox et al., 2008, Li et al., 2005, Mercado et al., 2006, Most et al., 2006, Rossignol et al., 2005). So far, only few studies emphasized the importance of monitoring anxiety traits with regard to response inhibition and Nogo-components (Karch et al., 2008, Righi et al., 2009). In particular, Righi et al. (2009) reported that, during a Go/Nogo-task, the N2-component was increased in trait and state anxious, healthy subjects, while the P3 was decreased in subjects who reported a higher frequency of cognitive failures.

To the best of our knowledge, this is the first study investigating the influence of two different anxiety-related personality constructs, such as TA and AS, on event-related potentials in a Go/Nogo-paradigm in healthy subjects. We hypothesize that individuals with high levels of TA and AS show a specific enhancement of executive control in this response inhibition task. We assume that persons with high anxiety are characterized by increased cognitive control and an enhanced evaluation of their behavioural outcomes, which may be reflected by increased Nogo-N2 and Nogo-P3 responses, and fewer false alarm rates. Moreover, with respect to each anxiety construct (AS, TA), we expect differential effects on Nogo-N2 and -P3 components.