Affective Bias without Hemispheric Competition: Evidence for Independent Processing Resources in Each Cortical Hemisphere.

We assessed the extent of neural competition for attentional processing resources in early visual cortex between foveally presented task stimuli and peripheral emotional distracter images. Task-relevant and distracting stimuli were shown in rapid serial visual presentation (RSVP) streams to elicit the steady-state visual evoked potential, which serves as an electrophysiological marker of attentional resource allocation in early visual cortex. A task-related RSVP stream of symbolic letters was presented centrally at 15 Hz while distracting RSVP streams were displayed at 4 or 6 Hz in the left and right visual hemifields. These image streams always had neutral content in one visual field and would unpredictably switch from neutral to unpleasant content in the opposite visual field. We found that the steady-state visual evoked potential amplitude was consistently modulated as a function of change in emotional valence in peripheral RSVPs, indicating sensory gain in response to distracting affective content. Importantly, the facilitated processing for emotional content shown in one visual hemifield was not paralleled by any perceptual costs in response to the task-related processing in the center or the neutral image stream in the other visual hemifield. Together, our data provide further evidence for sustained sensory facilitation in favor of emotional distracters. Furthermore, these results are in line with previous reports of a "different hemifield advantage" with low-level visual stimuli and are suggestive of independent processing resources in each cortical hemisphere that operate beyond low-level visual cues, that is, with complex images that impact early stages of visual processing via reentrant feedback loops from higher order processing areas.

Rapid sensory gain with emotional distracters precedes attentional deployment from a foreground task.

The steady-state visual evoked potential (SSVEP), an electrophysiological marker of attentional resource allocation, has recently been demonstrated to serve as a neural signature of emotional content extraction from a rapid serial visual presentation (RSVP). SSVEP amplitude was reduced for streams of emotional relative to neutral scenes passively viewed at 6 Hz (~167 ms per image), but it was enhanced for emotional relative to neutral scenes when viewed as 4 Hz RSVP (250 ms per image). Here, we investigated whether these seemingly contradictory observations may be related to different dynamics in the allocation of attentional resources as a consequence of stimulation frequency. To this end, we advanced our distraction paradigm by presenting a visual foreground task consisting of randomly moving squares flickering at 15 Hz superimposed on task-irrelevant RSVP streams shown at 6 or 4 Hz, which could unpredictably switch from neutral to unpleasant content during the trial or remained neutral. Critically, our findings demonstrate that affective distractors captured attentional resources more strongly than their neutral counterparts, irrespective of whether they were presented at 6 or 4 Hz rate. Moreover, the emotion-dependent attentional deployment from the foreground task was temporally preceded by sustained sensory facilitation in response to emotional background images. Together, present findings provide evidence for rapid sustained visual facilitation but a rather slow attentional bias in favor of emotional distractors in early visual areas.

Bringing color to emotion: The influence of color on attentional bias to briefly presented emotional images.

Is color a critical feature in emotional content extraction and involuntary attentional orienting toward affective stimuli? Here we used briefly presented emotional distractors to investigate the extent to which color information can influence the time course of attentional bias in early visual cortex. While participants performed a demanding visual foreground task, complex unpleasant and neutral background images were displayed in color or grayscale format for a short period of 133 ms and were immediately masked. Such a short presentation poses a challenge for visual processing. In the visual detection task, participants attended to flickering squares that elicited the steady-state visual evoked potential (SSVEP), allowing us to analyze the temporal dynamics of the competition for processing resources in early visual cortex. Concurrently we measured the visual event-related potentials (ERPs) evoked by the unpleasant and neutral background scenes. The results showed (a) that the distraction effect was greater with color than with grayscale images and (b) that it lasted longer with colored unpleasant distractor images. Furthermore, classical and mass-univariate ERP analyses indicated that, when presented in color, emotional scenes elicited more pronounced early negativities (N1-EPN) relative to neutral scenes, than when the scenes were presented in grayscale. Consistent with neural data, unpleasant scenes were rated as being more emotionally negative and received slightly higher arousal values when they were shown in color than when they were presented in grayscale. Taken together, these findings provide evidence for the modulatory role of picture color on a cascade of coordinated perceptual processes: by facilitating the higher-level extraction of emotional content, color influences the duration of the attentional bias to briefly presented affective scenes in lower-tier visual areas.

Attentional bias to affective faces and complex IAPS images in early visual cortex follows emotional cue extraction.

Emotionally arousing stimuli are known to rapidly draw the brain's processing resources, even when they are task-irrelevant. The steady-state visual evoked potential (SSVEP) response, a neural response to a flickering stimulus which effectively allows measurement of the processing resources devoted to that stimulus, has been used to examine this process of attentional shifting. Previous studies have used a task in which participants detected periods of coherent motion in flickering random dot kinematograms (RDKs) which generate an SSVEP, and found that task-irrelevant emotional stimuli withdraw more attentional resources from the task-relevant RDKs than task-irrelevant neutral stimuli. However, it is not clear whether the emotion-related differences in the SSVEP response are conditional on higher-level extraction of emotional cues as indexed by well-known event-related potential (ERPs) components (N170, early posterior negativity, EPN), or if affective bias in competition for visual attention resources is a consequence of a time-invariant shifting process. In the present study, we used two different types of emotional distractors - IAPS pictures and facial expressions - for which emotional cue extraction occurs at different speeds, being typically earlier for faces (at ~170ms, as indexed by the N170) than for IAPS images (~220-280ms, EPN). We found that emotional modulation of attentional resources as measured by the SSVEP occurred earlier for faces (around 180ms) than for IAPS pictures (around 550ms), after the extraction of emotional cues as indexed by visual ERP components. This is consistent with emotion related re-allocation of attentional resources occurring after emotional cue extraction rather than being linked to a time-fixed shifting process.

Emotional content overrides spatial attention.

Spatial attention is our capacity to attend to or ignore particular regions of our spatial environment. However, some classes of stimuli may be able to override our efforts to ignore them. Here we assessed the relationship between involuntary attentional capture with emotional images and spatial attention at early stages of perceptual processing. Multiple scenes of unpleasant and neutral content were displayed in rapid serial visual presentation (RSVP) streams that elicited the steady-state visual evoked potential (SSVEP), a neural marker of selective attention at early visual areas. In a spatial cueing task, participants were cued to covertly attend to RSVP streams presented at 4 and 6 Hz presentation rates in the left and right visual hemifields. The task was to detect square targets occasionally displayed within the image streams, responding only to those appearing on the cued side. The RSVP streams were always neutral pictures in one visual hemifield but would unpredictably switch from neutral to aversive content in the other visual hemifield. We found that SSVEP amplitude was consistently modulated by a change in emotional valence of image streams, regardless of whether the change in content occurred in the attended or unattended spatial location, reflecting an automatic sensory amplification for affective stimuli. The present data provide further evidence in support that emotional images can attract visual processing resources independently of spatial attention allocation, and are consistent with sustained sensory facilitation of early visual areas through re-entrant feedback projections from higher-order cortical areas involved in the extraction of affective information.

The neural signature of extracting emotional content from rapid visual streams at multiple presentation rates: A cross-laboratory study.

The steady-state visual evoked potential (SSVEP), a neural signature of attentional resource allocation, is enhanced for affective compared to neutral visual scenes. Recently, it has been demonstrated that modulation of early visual cortex associated with viewing of unpleasant scenes presented in a rapid succession relies on emotional content extraction from each individual image shown in a rapid serial visual presentation (RSVP) at 6 Hz (~167 ms per image). Against expectations, the SSVEP was reduced when viewing visual streams of unpleasant compared to neutral scenes. Here, we investigated to what extent that finding was limited to the 6 Hz rate and whether it generalizes to pleasant pictures. We recorded SSVEPs elicited by RSVP of neutral and emotional scenes presented at 3, 4, 6.67, and 8.57 Hz rates. We demonstrated that SSVEP amplitudes were enhanced for unpleasant compared to neutral images with a presentation rate of 3, 4, and 8.57 Hz. By contrast, SSVEP decreased for both pleasant and unpleasant relative to neutral RSVP streams shown at 6.67 Hz. Our findings suggest that a linear superposition of ERPs evoked by each individual image in an RSVP may lead to SSVEP amplitude patterns that increase or decrease the power at the driving frequency, which in turn might produce the observed differential emotional amplitude modulations. The results provide new methodological considerations for investigating temporal dynamics of early visual cortex modulation during sustained perception of affective scenes with SSVEP using RSVP paradigms.

Affective facilitation of early visual cortex during rapid picture presentation at 6 and 15 Hz.

The steady-state visual evoked potential (SSVEP), a neurophysiological marker of attentional resource allocation with its generators in early visual cortex, exhibits enhanced amplitude for emotional compared to neutral complex pictures. Emotional cue extraction for complex images is linked to the N1-EPN complex with a peak latency of ∼140-160 ms. We tested whether neural facilitation in early visual cortex with affective pictures requires emotional cue extraction of individual images, even when a stream of images of the same valence category is presented. Images were shown at either 6 Hz (167 ms, allowing for extraction) or 15 Hz (67 ms per image, causing disruption of processing by the following image). Results showed SSVEP amplitude enhancement for emotional compared to neutral images at a presentation rate of 6 Hz but no differences at 15 Hz. This was not due to featural differences between the two valence categories. Results strongly suggest that individual images need to be displayed for sufficient time allowing for emotional cue extraction to drive affective neural modulation in early visual cortex.

Effects of EEG-vigilance regulation patterns on early perceptual processes in human visual cortex.

OBJECTIVE: To investigate influences of EEG-vigilance regulation patterns on perceptual processing during sustained visual attention in early visual areas. METHODS: We compared a subject group with stable vigilance regulation to a group with unstable EEG-vigilance regulation. A rapid serial visual presentation stream (RSVP) elicited a 7.5 Hz steady state visual evoked potential (SSVEP), a continuous sinusoidal brain response as a measure of attentional resource allocation during sustained attention in early visual cortex. Subjects performed a target discrimination task. 150 trials were divided into two parts (75 trials each, trial duration: 11 s). RESULTS: A significant interaction vigilance group by experimental part provided significantly greater SSVEP amplitudes for the unstable group in the second compared to the first part of the experiment. Both groups showed training effects with increased hit rates and d'-values in the second part of the experiment. CONCLUSIONS: The unexpected finding of SSVEP amplitude increase for the unstable group might be due to competitive interactions for neural resources between the alpha response and SSVEPs. SIGNIFICANCE: Individual patterns of EEG-vigilance regulation have a moderate impact on early sensory processing during sustained visual attention that is not paralleled in task performance.