Temporal-Spatial Neural Activation Patterns Linked to Perceptual Encoding of Emotional Salience

et al. (2014) Temporal-Spatial Neural Activation Patterns Linked to Perceptual Encoding of Emotional Salience. PLoS ONE 9(4): e93753. doi:10.1371/journal.pone.0093753 Temporal-Spatial Neural Activation Patterns Linked to Perceptual Encoding of Emotional Salience Rebecca M. Todd 0 Margot J. Taylor 0 Amanda Robertson 0 Daniel B. Cassel 0 Sam M. Doesberg 0 Daniel H. Lee 0 Pang N. Shek 0 Elizabeth W. Pang 0 Jyrki Ahveninen, Harvard Medical School/Massachusetts General Hospital, United States of America 0 1 Department of Psychology, University of British Columbia , Vancouver, British Columbia , Canada , 2 Department of Diagnostic Imaging, Hospital for Sick Children , Toronto, Ontario , Canada , 3 Neurosciences and Mental Health Research Institute, Hospital for Sick Children , Toronto, Ontario , Canada , 4 Department of Psychology, University of Toronto , Toronto, Ontario , Canada , 5 Department of Medical Imaging, University of Toronto , Toronto, Ontario , Canada , 6 Military Medicine Section, Defence Research and Development , Toronto, Ontario , Canada , 7 Division of Neurology, Hospital for Sick Children , Toronto, Ontario , Canada It is well known that we continuously filter incoming sensory information, selectively allocating attention to what is important while suppressing distracting or irrelevant information. Yet questions remain about spatiotemporal patterns of neural processes underlying attentional biases toward emotionally significant aspects of the world. One index of affectively biased attention is an emotional variant of an attentional blink (AB) paradigm, which reveals enhanced perceptual encoding for emotionally salient over neutral stimuli under conditions of limited executive attention. The present study took advantage of the high spatial and temporal resolution of magnetoencephalography (MEG) to investigate neural activation related to emotional and neutral targets in an AB task. MEG data were collected while participants performed a rapid stimulus visual presentation task in which two target stimuli were embedded in a stream of distractor words. The first target (T1) was a number and the second (T2) either an emotionally salient or neutral word. Behavioural results replicated previous findings of greater accuracy for emotionally salient than neutral T2 words. MEG source analyses showed that activation in orbitofrontal cortex, characterized by greater power in the theta and alpha bands, and dorsolateral prefrontal activation were associated with successful perceptual encoding of emotionally salient relative to neutral words. These effects were observed between 250 and 550 ms, latencies associated with discrimination of perceived from unperceived stimuli. These data suggest that important nodes of both emotional salience and frontoparietal executive systems are associated with the emotional modulation of the attentional blink. - Competing Interests: Sam Doesberg is currently a PLOS ONE editorial board member. This does not alter the authors adherence to all the PLOS ONE policies on sharing data and materials. Emotionally important events are perceived more vividly than mundane ones [1], and emotionally compelling objects in the environment capture the eye as we navigate the world [2,3]. It is well known that we continuously filter incoming sensory information, selectively allocating attention to what is important to us and suppressing distracting or irrelevant information (for review see [4]). Yet questions remain about spatio-temporal patterns of neural processes underlying attentional biases toward emotionally significant aspects of the world. A wide body of research indicates that enhanced visual processing of goal-relevant stimuli is modulated by executive attentional processes in the service of explicit goals [5,6,7]. Evidence from affective science suggests that selective visual attention is also modulated by emotional or motivational salience linked to longer-term subjective goals of increasing pleasure and avoiding pain [8,9]. Such long-term goals can tune visual attention habitually to emotionally salient stimuli such as a prized possession, a facial expression, or a gruesome scene [8,10,11]. Convergent data suggest that the amygdalae, orbitofrontal cortices, and other brain regions key in tagging emotional salience may underlie deployment of affect-biased attention by modulating visual cortical activation in much the same way as frontoparietal regions do during task-based control [12,13,14,15]. Convergent evidence suggests that, at a latency sufficiently late to allow awareness and explicit evaluation of stimuli, both executive and emotional salience systems contribute to enhanced processing of emotional stimuli. ERP studies have identified a late positive component, the late positive potential (LPP), between 400 and 600 ms after stimulus onset, which is enhanced for emotionally salient over neutral stimuli (e.g., [16]). A recent study found that LPP amplitude for emotionally evocative images can be modulated by both task relevance (executive top-down attention) as well as by the emotional salience of an image when it is not task relevant [17]. This finding suggests that, at that latency, executive and emotional salience systems interact to modulate cortical activation. Building on this finding, one magnetoencephalography (MEG) study found that in the 400500 ms time window, frontal and occipitoparietal regions showed greater bidirectional activation for more emotionally salient stimuli [18]. Again, this finding was interpreted as reflecting interaction between perceptual and reflective processes. These studies suggest that executive and emotional attention systems may work in an additive manner for later stage processing. A further question concerns whether similar patterns of co-activation between executive and affect-biased attention can be observed for rapid attentional capture by emotional stimuli. A behavioural index of affect-biased attention that may tap more directly the deployment of emotional control settings is an emotional variant of an attentional blink (AB) paradigm. The AB [19] is a well-documented experimental manipulation that effectively measures biases in perceptual encoding and resulting awareness. The AB task is a rapid serial visual presentation (RSVP) task in which target stimuli are embedded in a stream of very rapidly presented stimuli. The blink itself is a phenomenon where participants are typically unable to report a target stimulus (T2) when it is presented within ,500 ms of a previous target (T1) within the stream of distractors. ERP research has shown that, whereas perceptual components in the first 150200 ms of stimulus onset are identical for both perceived and unperceived targets, an unperceived T2 stimulus fails to elicit a P3 component [20,21], which is measured at a similar latency to the LPP reported in emotional studies. fMRI studies implicate frontoparietal networks in the AB, likely functioning (...truncated)