Modulation of the error-related negativity by induction of short-term negative affect

Abstract

The present study investigates whether performance monitoring and its electrophysiological indices in a choice reaction time task are modulated by affective information presented briefly prior to the critical stimuli. A flanker task known to elicit a sufficient number of performance errors was used and prior to each flanker stimulus a neutral, pleasant or unpleasant picture from the International Affective Picture System (IAPS) was shown. While behavioral performance to the flanker stimuli was hardly affected by the preceding affective information, the error-related negativity (ERN) of the event-related potential was modulated by affective information: Unpleasant IAPS pictures preceding a performance error led to an increased ERN amplitude compared to trials with neutral and pleasant IAPS pictures. These trial-by-trial modulations of electrophysiological markers of performance monitoring are discussed in terms of the possible influence of affective stimuli on monaminergic neuromodulatory transmitter systems.

Introduction

Affect influences how we perceive and act upon our environment. It has been shown that positive affect increases problem solving (Isen, 2001, Isen et al., 1987), memory performance (Lee, & Sternthal, 1999), executive attention (Ashby, Valentin, & Turken, 2002), decision making (Isen, 2001) and a variety of other cognitive tasks, while the influence of negative affect is more diffuse and difficult to predict (Ashby, Isen, & Turken, 1999; Mitchell, & Phillips, 2007). The present investigation is concerned with the affective modulation of action monitoring. In particular, we are interested in the affective modulation of a specific component in the event-related brain potential (ERP), the error-related negativity (ERN or Ne) (Falkenstein, Hohnsbein, Hoormann, & Blanke, 1991; Gehring, Goss, Coles, Meyer, & Donchin, 1993). It is observed with a frontocentral distribution and a peak-latency between 50 and 100 ms after the commission of an error. Electrophysiological (e.g., van Veen and Carter, 2002a, van Veen and Carter, 2002b) and brain imaging techniques (Marco-Pallares, Müller, & Münte, 2007; Ridderinkhof, Ullsperger, Crone, & Nieuwenhuis, 2004) agree that the ERN emerges in the anterior cingulate cortex (ACC).

Long-lasting emotional and motivational factors have also been shown previously to modulate ERN amplitude: It is increased in subjects suffering from increased anxiety and negative affect (Hajcak et al., 2003a, Hajcak et al., 2004). In an early study Luu, Collins, and Tucker (2000) similarly found that college students who were high on negative affect and negative emotionality displayed larger ERN amplitudes compared to participants who displayed low negative affect and emotionality. This effect decreased, however, over the course of the experiment, which was interpreted as signifying disengagement of the high negative affect participants from the task. More globally, the results were interpreted as evidence for an interaction between affect and associated behavioral patterns with frontal lobe executive functions. In patients suffering from obsessive-compulsive disorder who likewise display a high negative affect, several studies have reported an increased ERN amplitude (Gehring, Himle, & Nisenson, 2000; Hajcak, & Simons, 2002; Johannes et al., 2001a, Johannes et al., 2001b; Münte et al., 2008). There are also some indirect indications that long-lasting positive affect modulates ERN amplitude: Alcohol, which induces pleasant feelings, and oxazepam, a benzodiazepine derivative with anxiolytic properties reduce ERN amplitude (Johannes et al., 2001a, Johannes et al., 2001b, Riba et al., 2005a, Riba et al., 2005b; Ridderinkhof et al., 2002). These pharmacological studies have to be interpreted with caution, however, as a direct action of these agents (e.g., by enhancing the activity of cortical interneurons) on the ERP amplitudes rather than an indirect action via their influence on affective factors is a possibility. To summarize, stable and replicable influences of negative and – to a lesser degree – positive affect on action monitoring indexed by the ERN have been shown.

The influence of short lasting affective modulations has been less intensively studied and has led to contradictory and counterintuitive results. Larson, Perlstein, Stigge Kaufman, Kelly, and Dotson (2006) presented a flanker stimulus superimposed on neutral, unpleasant or pleasant pictures taken from the International Affective Picture System (IAPS) and, in contrast to what has been observed with longer lasting affective states (see above), observed an increase in ERN amplitude for pleasant compared to neutral and unpleasant background pictures. The authors interpreted this finding as possibly indicating a mismatch between the positive affect induced by the background picture and the negative event constituted by the error response. Because of the long presentation of the IAPS pictures and the fact that the flanker stimuli were presented during the presentation of background pictures, an alternative explanation might be that the unpleasant background pictures might have drawn attention away from the flanker stimulus and thus might have precluded an increase of ERN amplitude. Anxiety induced by a tarantula spider close to the phobic subject did not alter ERN amplitude (Moser, Hajcak, & Simons, 2005). However, if negative affect is induced by external stimuli, subjects allocate attentional resources towards the threatening cue. This might decrease error significance and counteract fear-induced effects.

In the present study we reexamined this issue by presenting pleasant, unpleasant and neutral IAPS pictures immediately prior to flanker stimuli for which the subjects had to perform a choice reaction time task¹.

In light of the previous studies on the influence of longer lasting negative (Hajcak et al., 2003a, Hajcak et al., 2004, Luu et al., 2000) and positive (Johannes et al., 2001a, Johannes et al., 2001b, Riba et al., 2005a, Riba et al., 2005b, Ridderinkhof et al., 2002) affect on ERN and action monitoring, we formulated two hypotheses:

The first hypothesis stated that ERN amplitude to performance errors should be increased following the presentation of unpleasant IAPS pictures. The second hypothesis stated that ERN amplitude should be decreased after the presentation of pleasant IAPS pictures.

The primary focus of the experiment is thus on the (possible) influence of the valence of the preceding IAPS picture on the amplitude of the ERN. A second prominent effect in the flanker task is the so-called N2 component present in stimulus-locked averages that differentiates incongruent (HHSHH, SSHSS) from congruent (SSSSS, HHHHH) stimuli and has been interpreted as an index of response conflict (van Veen and Carter, 2002a, van Veen and Carter, 2002b; but see Wendt, Heldmann, Münte, & Kluwe, 2007). Like the ERN, this component has been attributed to the medial prefrontal cortex. Therefore it was of interest whether any valence-induced changes in the ERN might also be found for the N2 component.

Since the response to emotional stimuli has been shown to vary as a function of participants’ gender and to be weaker in men (Campbell et al., 2002, Kemp et al., 2004; Wrase et al., 2003), only women were enrolled in the present experiment.