Elsevier

Neuropsychologia

Volume 49, Issue 3, February 2011, Pages 416-425
Neuropsychologia

Emotional modulation of the attentional blink: The neural structures involved in capturing and holding attention

https://doi.org/10.1016/j.neuropsychologia.2010.12.037Get rights and content

Abstract

Perceiving a first target stimulus (T1) in a rapid serial visual presentation stream results in a transient impairment in detecting a second target (T2). This “attentional blink” is modulated by the emotional relevance of T1 and T2. The present experiment examined the neural underpinnings of the emotional modulation of the attentional blink. Behaviorally, the attentional blink was reduced for emotional T2 while emotional T1 led to a prolonged attentional blink. Using functional magnetic resonance imaging, we observed amygdala activation associated with the reduced attentional blink for emotional T2 in the face of neutral T1. The prolonged attentional blink following emotional T1 was correlated with enhanced activity in a cortical network including the anterior cingulate cortex, the insula and the orbitofrontal cortex. These results suggest that brain areas previously implicated in rather reflexive emotional reactions are responsible for the reduced attentional blink for emotional T2 whereas neural structures previously related to higher level processing of emotional information mediate the prolonged attentional blink following emotional T1.

Research highlights

▶ Emotional stimuli can reduce or extend the attentional blink. ▶ The reduction of the attentional blink is associated with amygdala activity. ▶ Its extension is associated with circuits involved in higher level processing.

Introduction

Our ability to process sequentially presented stimuli is limited. A prominent example is the attentional blink which describes the severe impairment in detecting the second of two targets presented rapidly (i.e., within 500 ms) one after another among a stream of distractor items (Broadbent and Broadbent, 1987, Raymond et al., 1992). This blink occurs when attentional resources are consumed by the processing of the first target (T1), leaving only few attentional resources available for allocation to the second target (T2; Chun and Potter, 1995, Jolicoeur, 1999, Shapiro et al., 1997). Studies using functional magnetic resonance imaging (fMRI) identified a fronto-parietal network as a locus of the attentional blink in the brain (Hein et al., 2008, Kranczioch et al., 2005, Marcantoni et al., 2003, Marois et al., 2000, Marois et al., 2004, Shapiro et al., 2007).

There is compelling evidence that emotionally arousing stimuli can overcome, at least partly, the attentional limitations underlying the attentional blink. T2s that are emotionally arousing are significantly better detected than neutral T2s and thus reduce the attentional blink (Anderson, 2005, Anderson and Phelps, 2001, De Martino et al., 2009, Keil and Ihssen, 2004, Schwabe and Wolf, 2010). This might reflect faster orienting towards emotional stimuli, prolonged holding of attention for emotional stimuli or both (Vuilleumier, 2005). Bilateral amygdala damage abolishes the enhanced detection of emotionally arousing T2s suggesting that this brain area is critical for the reduced attentional blink for emotionally arousing stimuli (Anderson & Phelps, 2001). To date, there is only one study that examined the neural correlates of the enhanced detection of emotional T2s in healthy humans (De Martino et al., 2009). This fMRI study showed enhanced activity in the rostral part of the anterior cingulate cortex (ACC), an area that shares reciprocal connectivity with the amygdala, that was related to the improved detection of fearful compared to neutral faces.

Recent evidence demonstrates that emotionally arousing stimuli do not always reduce the attentional blink but may also lead to a prolonged attentional blink. In particular, emotionally arousing T1s or emotionally arousing to-be-ignored distractor items decrease the report accuracy for subsequently presented neutral T2s (Arnell et al., 2007, Mathewson et al., 2008, Most et al., 2005, Stein et al., 2009). Moreover, emotionally arousing T1s reduce the benefit in detection of emotional T2s (Schwabe & Wolf, 2010). Emotional stimuli are preferentially processed and attract substantial attentional resources (Dijksterhuis and Aarts, 2003, Vuilleumier, 2005). The enhanced processing demands associated with emotional T1s leave less attentional capacities for the identification of T2s and thus result in a prolonged attentional blink (Mathewson et al., 2008). The neural circuitry underlying the attentional blink extension by emotionally arousing T1s is still unknown.

In the present experiment, we therefore examined whether the brain structures mediating the prolonged attentional blink following emotional T1s are the same as those involved in the reduced attentional blink for emotional T2s (De Martino et al., 2009). Participants viewed a rapid sequence of 15 words and had to identify two targets (T1 and T2) that were either neutral or emotionally arousing. Based on previous studies (Anderson, 2005, Keil and Ihssen, 2004, Mathewson et al., 2008, Schwabe and Wolf, 2010), we predicted a reduced attentional blink for emotional T2s and a prolonged attentional blink following emotional T1s. At the neural level, we expected that the amygdala would be involved in the enhanced detection of emotional T2s (Anderson & Phelps, 2001). Given that the prolonged attentional blink after emotionally arousing T1s appears to be primarily owing to the extended processing of the emotionally arousing T1s, it is tempting to speculate that prefrontal areas involved in the processing of emotional information (Damasio, 1996, Rolls et al., 1994) might be associated with the failure to identify the T2 in the presence of emotional T1s.

Section snippets

Participants

Thirty-eight right-handed, healthy native speakers of German with normal or corrected to normal vision participated in this experiment (19 men, 19 women; mean age: 24.3 years, range: 20–35 years). Participants were prescreened to exclude those with a previous history of psychiatric or neurological illness. All subjects provided written informed consent, and the study was approved by the local ethics committee.

General procedure

At the beginning of the experiment, participants practiced the rapid serial visual

Pre-scan session: emotional modulation of the attentional blink

In the pre-scan session, participants showed a robust attentional blink as expressed by a significant increase in T2 detection accuracy from the early to the late lag (58 percent vs. 93 percent, chance: 25 percent; main effect lag: F(1,37) = 205.3, p < .001; Fig. 2). Emotionally arousing T1s and T2s had opposite effects on the attentional blink. Detection of T2s in the attentional blink period (i.e., at the early lag) was impaired by emotionally arousing T1s (T1 × lag interaction effect: F(1,37) = 

Discussion

Our behavioral findings replicate previous reports in showing that individuals have considerable difficulties to identify a T2 presented rapidly after a T1 (Broadbent and Broadbent, 1987, Raymond et al., 1992) and that this attentional blink is modulated by the emotionality of T1 and T2 (Anderson, 2005, Anderson and Phelps, 2001, Mathewson et al., 2008, Schwabe and Wolf, 2010). Emotionally arousing T2s reduced the attentional blink whereas emotionally arousing T1s led to a prolonged attentional

Acknowledgement

This work was supported by a grant of the Rektoratsfonds of the Ruhr-University Bochum.

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    The study was carried out at the Bender Institute of Neuroimaging, University of Giessen, Germany.

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