Emotional modulation of the attentional blink: The neural structures involved in capturing and holding attention☆
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.
References (51)
- et al.
Cognitive and emotional influences in anterior cingulate cortex
Trends in Cognitive Sciences
(2000) - et al.
Amygdala circuitry in attentional and representational processes
Trends in Cognitive Sciences
(1999) - et al.
A global optimisation method for robust affine registration of brain images
Medical Image Analysis
(2001) - et al.
Neural correlates of conscious perception in the attentional blink
NeuroImage
(2005) - et al.
Neural correlates of dual task interference in visual streams: An fMRI study
Brain and Cognition
(2003) - et al.
Neural correlates of the attentional blink
Neuron
(2000) - et al.
The neural fate of consciously perceived and missed events in the attentional blink
Neuron
(2004) - et al.
Are you always on my mind? A review of how face perception and attention interact
Neuropsychologia
(2007) - et al.
Subcortical discrimination of unperceived objects during binocular rivalry
Neuron
(2004) - et al.
The attentional blink
Trends in Cognitive Sciences
(1997)
The interaction of attention and emotion
Neural Networks
How brains beware: Neural mechanisms of emotional attention
Trends in Cognitive Sciences
Multi level linear modelling for fMRI group analysis using Bayesian inference
NeuroImage
Temporal autocorrelation in univariate linear modelling of fMRI data
NeuroImage
Affective influences on the attentional dynamics supporting awareness
Journal of Experimental Psychology: General
Lesions of the human amygdala impair enhanced perception of emotionally salient events
Nature
Blinded by emotion: Target misses follow attention capture by arousing distractors in RSVP
Emotion
Emotion, decision making and the orbitofrontal cortex
Cerebral Cortex
General multi-level linear modelling for group analysis in fMRI
NeuroImage
State anxiety modulation of the amygdala response to unattended threat-related stimuli
The Journal of Neuroscience
From detection to identification: Response to multiple targets in rapid serial visual presentation
Perception & Psychophysics
Anterior cingulate cortex, error detection, and the online monitoring of performance
Science
The anatomical connections of the macaque monkey orbitofrontal cortex. A review
Cerebral Cortex
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The study was carried out at the Bender Institute of Neuroimaging, University of Giessen, Germany.