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Open Access 01-07-2019 | Original Article

Enhanced insular/prefrontal connectivity when resisting from emotional distraction during visual search

Authors: Tiziana Pedale, Emiliano Macaluso, Valerio Santangelo

Published in: Brain Structure and Function | Issue 6/2019

Abstract

Previous literature demonstrated that the processing of emotional stimuli can interfere with goal-directed behavior. This has been shown primarily in the context of working memory tasks, but “emotional distraction” may affect also other processes, such as the orienting of visuo-spatial attention. During fMRI, we presented human subjects with emotional stimuli embedded within complex everyday life visual scenes. Emotional stimuli could be either the current target to be searched for or task-irrelevant distractors. Behavioral and eye-movement data revealed faster detection of emotional than neutral targets. Emotional distractors were found to be fixated later and for a shorter duration than emotional targets, suggesting efficient top-down control in avoiding emotional distraction. The fMRI data demonstrated that negative (but not positive) stimuli were mandatorily processed by limbic/para-limbic regions (namely, the right amygdala and the left insula), irrespective of current task relevance: that is, these regions activated for both emotional targets and distractors. However, analyses of inter-regional connectivity revealed a functional coupling between the left insula and the right prefrontal cortex that increased specifically during search in the presence of emotional distractors. This indicates that increased functional coupling between affective limbic/para-limbic regions and control regions in the frontal cortex can attenuate emotional distraction, permitting the allocation of spatial attentional resources toward task-relevant neutral targets in the presence of distracting emotional signals.

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It is worth noting that, despite our set of stimuli included emotional stimuli clearly distinguishable from the neutral stimuli in terms of valence and arousal, the absolute difference in valence and in arousal ratings between neutral and positive scenes was lower than the difference between neutral and negative scenes. This potential limitation is a consequence of the fact that we used a limited set of emotional categories. Stimuli eliciting highly arousing positive emotions typically represent social interactions (e.g., families, sexual stimuli, romantic couples; see the IAPS database, Lang et al. 1999). Conversely, the scenes used for the current task did not include any human subject, which might result to be more salient than other objects, and then, attentional capturing per se.

Note that for the two latter conditions in which the emotional object was a distractor we did not compute the f-fix-RT index: given that here we analyzed fixations related to task-irrelevant objects that did not require any responses, it was pointless to report for these conditions the interval between the first fixation and response button press (i.e., the f-fix-RT index), which is related to a different object in the scene (i.e., the current to-be-searched neutral target).

For completeness, we conducted two one-way ANOVAs on the main conditions (negS_negT, negS_neuT, neuS_neuT, posS_posT, posS_neuT) for the accuracy and RT data. These revealed overall coherent results with the IES. Both analyses were significant: ACC [F(4, 84) = 6.16, p < 0.001] and RTs [F(4, 84) = 21.5, p < 0.001]. Planned comparisons revealed higher accuracy when the current target was an emotional (negS_negT or posS_posT) compared to a neutral object (negS_neuT or posS_neuT): t(21) = 2.75; p = 0.006 and t(21) = 3.76; p < 0.001, respectively. Moreover, planned comparisons revealed faster RT for positive targets (posS_posT) compared to neutral targets in the presence of positive distraction (posS_neuT): t(21) = 10.17; p < 0.001. As concerns the baseline condition (neuS_neuT), the planned comparisons revealed faster RT and higher accuracy when searching for positive targets (posS_posT): t(21) = 7.43; p < 0.001 and t(21) = 3.36; p = 0.001, respectively; and only higher accuracy when searching for negative targets (negS_negT): t(21) = 1.77; p = 0.046.

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Title: Enhanced insular/prefrontal connectivity when resisting from emotional distraction during visual search
Authors: Tiziana Pedale
Emiliano Macaluso
Valerio Santangelo
Publication date: 01-07-2019
Publisher: Springer Berlin Heidelberg
Published in: Brain Structure and Function / Issue 6/2019
Print ISSN: 1863-2653
Electronic ISSN: 1863-2661
DOI: https://doi.org/10.1007/s00429-019-01873-1

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Enhanced insular/prefrontal connectivity when resisting from emotional distraction during visual search

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