Attentional capture by emotional stimuli is preserved in patients with amygdala lesions

Piech, Richard M.; McHugo, Maureen; Smith, Stephen D.; Dukic, Mildred S.; Meer, Joost van der; Abou‐Khalil, Bassel; Most, Steven B.; Zald, David H.

doi:10.1016/j.neuropsychologia.2011.08.004

Cited by 35 publications

(37 citation statements)

References 49 publications

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“…It is also worth noting that compensatory circuits may account for the intact social attention in amygdala lesion patients (Becker et al, 2012) and a recent finding has also shown that amygdala lesion patients have intact preferred attention towards animals (Wang et al, 2014a), even though these findings would not be expected on the basis of neuronal responses observed in the amygdala to animals (Mormann et al, 2011). Our finding is also consistent with preserved attentional capture by emotional stimuli and intact emotion-guided visual search in patients with acute amygdala lesions due to neurosurgical resection (Piech et al, 2010, 2011). Taken together, there are now numerous examples of a discrepancy between engagement of the amygdala (e.g., in functional neuroimaging studies) in tasks for which there is no obvious corresponding behavioral impairment when the amygdala is lesioned.…”

Section: Discussionsupporting

confidence: 87%

Autism spectrum disorder, but not amygdala lesions, impairs social attention in visual search

Wang¹,

Xu²,

Jiang³

et al. 2014

Neuropsychologia

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People with autism spectrum disorders (ASD) have pervasive impairments in social interactions, a diagnostic component that may have its roots in atypical social motivation and attention. One of the brain structures implicated in the social abnormalities seen in ASD is the amygdala. To further characterize the impairment of people with ASD in social attention, and to explore the possible role of the amygdala, we employed a series of visual search tasks with both social (faces and people with different postures, emotions, ages, and genders) and non-social stimuli (e.g., electronics, food, and utensils). We first conducted trial-wise analyses of fixation properties and elucidated visual search mechanisms. We found that an attentional mechanism of initial orientation could explain the detection advantage of non-social targets. We then zoomed into fixation-wise analyses. We defined target-relevant effects as the difference in the percentage of fixations that fell on target-congruent vs. target-incongruent items in the array. In Experiment 1, we tested 8 high-functioning adults with ASD, 3 adults with focal bilateral amygdala lesions, and 19 controls. Controls rapidly oriented to target-congruent items and showed a strong and sustained preference for fixating them. Strikingly, people with ASD oriented significantly less and more slowly to target-congruent items, an attentional deficit especially with social targets. By contrast, patients with amygdala lesions performed indistinguishably from controls. In Experiment 2, we recruited a different sample of 13 people with ASD and 8 healthy controls, and tested them on the same search arrays but with all array items equalized for low-level saliency. The results replicated those of Experiment 1. In Experiment 3, we recruited 13 people with ASD, 8 healthy controls, 3 amygdala lesion patients and another group of 11 controls and tested them on a simpler array. Here our group effect for ASD strongly diminished and all four subject groups showed similar target-relevant effects. These findings argue for an attentional deficit in ASD that is disproportionate for social stimuli, cannot be explained by low-level visual properties of the stimuli, and is more severe with high-load top-down task demands. Furthermore, this deficit appears to be independent of the amygdala, and not evident from general social bias independent of the target-directed search.

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Section: Discussionsupporting

confidence: 87%

Autism spectrum disorder, but not amygdala lesions, impairs social attention in visual search

Wang¹,

Xu²,

Jiang³

et al. 2014

Neuropsychologia

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“…In an effort to better understand the dynamics of attention capture by pleasant images as a category, we have included non-erotic imagery within the pleasant category. This contrasts with other studies that have relied exclusively on erotic or romantic scenes as examples of highly arousing, pleasant pictures (Most et al, 2007;Ciesielski et al, 2010;Piech et al, 2011). We expected that since this experiment used only one target per RSVP stream, no competition between emotional pictures would occur on a single trial.…”

Section: Methodsmentioning

confidence: 84%

“…While such an attentional set improved performance on trials with negative and neutral emotional distractors, attention to the sexually arousing distractors was unaffected (Most, Smith, Cooter, Levy & Zald, 2007). In other studies using pleasant, unpleasant, and neutral distractors, emotional distractors impaired later detection of neutral targets more than neutral distractors, but erotic pictures were more distracting than unpleasant pictures of violence and injury (Piech et al, 2011;Ciesielski et al, 2010). One possible explanation is that sexually arousing images are especially capable of attention capture due to their relevance for reproduction.…”

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confidence: 93%

Emotional Modulation of the Attentional Blink by Pleasant and Unpleasant Pictures

Villa

Cervantes

et al. 2012

The Journal of General Psychology

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When shown a rapid series of images, attention to a second target that follows in short proximity to a first is diminished--a phenomenon sometimes called an "attentional blink." Three experiments compared detection of motivationally relevant pleasant, unpleasant, and neutral pictures when they appeared as the second target following a neutral (Experiment 1), unpleasant (Experiment 2) and pleasant (Experiment 3) picture target. The second target followed at lags of 2, 3 or 8 pictures. In all three experiments, detection of neutral pictures was reduced at lags 2 and 3, indicative of an attentional blink. In contrast, unpleasant pictures were detected more than neutral pictures at lags 2 and 3. Unexpectedly, pleasant pictures not only resisted the attentional blink, but they were detected substantially more than other pictures at all lags in all three experiments. Overall, the experiments support the idea that motivationally relevant stimuli preferentially capture attention more than motivationally neutral stimuli.

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“…However, other brain structures may be involved as well. Rapid detection of emotional stimuli takes place even when the amygdala is lesioned (54)(55)(56). In humans (57) and in monkeys (58), OT has been shown to reduce responses to negative facial expressions not only in the amygdala, but also in inferior temporal cortex and prefrontal cortex (58).…”

Section: Discussionmentioning

confidence: 99%

Effect of distracting faces on visual selective attention in the monkey

Landman

Sharma

Sur

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

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In primates, visual stimuli with social and emotional content tend to attract attention. Attention might be captured through rapid, automatic, subcortical processing or guided by slower, more voluntary cortical processing. Here we examined whether irrelevant faces with varied emotional expressions interfere with a covert attention task in macaque monkeys. In the task, the monkeys monitored a target grating in the periphery for a subtle color change while ignoring distracters that included faces appearing elsewhere on the screen. The onset time of distracter faces before the target change, as well as their spatial proximity to the target, was varied from trial to trial. The presence of faces, especially faces with emotional expressions interfered with the task, indicating a competition for attentional resources between the task and the face stimuli. However, this interference was significant only when faces were presented for greater than 200 ms. Emotional faces also affected saccade velocity and reduced pupillary reflex. Our results indicate that the attraction of attention by emotional faces in the monkey takes a considerable amount of processing time, possibly involving cortical-subcortical interactions. Intranasal application of the hormone oxytocin ameliorated the interfering effects of faces. Together these results provide evidence for slow modulation of attention by emotional distracters, which likely involves oxytocinergic brain circuits.attention | faces | oxytocin | social | vision

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Attentional capture by emotional stimuli is preserved in patients with amygdala lesions

Cited by 35 publications

References 49 publications

Autism spectrum disorder, but not amygdala lesions, impairs social attention in visual search

Autism spectrum disorder, but not amygdala lesions, impairs social attention in visual search

Emotional Modulation of the Attentional Blink by Pleasant and Unpleasant Pictures

Effect of distracting faces on visual selective attention in the monkey

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