An extremely fast neural mechanism to detect emotional visual stimuli: A two-experiment study.

Defining the brain mechanisms underlying initial emotional evaluation is a key but unexplored clue to understanding affective processing. Event-related potentials (ERPs), especially suited for investigating this issue, were recorded in two experiments (n = 36 and n = 35). We presented emotionally negative (spiders) and neutral (wheels) silhouettes homogenized regarding their visual parameters. In Experiment 1, stimuli appeared at fixation or in the periphery (200 trials per condition and location), the former eliciting a N40 (39 milliseconds) and a P80 (or C1: 80 milliseconds) component, and the latter only a P80. In Experiment 2, stimuli were presented only at fixation (500 trials per condition). Again, an N40 (45 milliseconds) was observed, followed by a P100 (or P1: 105 milliseconds). Analyses revealed significantly greater N40-C1P1 peak-to-peak amplitudes for spiders in both experiments, and ANCOVAs showed that these effects were not explained by C1P1 alone, but that processes underlying N40 significantly contributed. Source analyses pointed to V1 as an N40 focus (more clearly in Experiment 2). Sources for C1P1 included V1 (P80) and V2/LOC (P80 and P100). These results and their timing point to low-order structures (such as visual thalamic nuclei or superior colliculi) or the visual cortex itself, as candidates for initial evaluation structures.

"I heard it before or not": time-course of ERP response and behavioural correlates associated with false recognition memory.

Electrophysiological and behavioural correlates of true and false memories were examined in the Deese/Roediger-McDermont (DRM) paradigm. A mass univariate approach for analysing event-related potentials (ERP) in the temporal domain was used to examine the electrophysiological effects associated with this paradigm precisely (point-by-point) and without bias (data-driven). Behaviourally, true and false recognition did not differ, and the predicted DRM effect was observed, as false recognition of critical lures (i.e., new words semantically related to studied words) was higher than false alarms of new (unrelated) words. Neurally, an expected old/new effect was observed during the time-range of the late positive component (LPC) over left centro-parietal scalp electrodes. Furthermore, true recognition also evoked larger LPC amplitudes than false recognition over both left centro-parietal and fronto-central scalp electrodes. However, we did not observe LPC-related differences between critical lures and new words, nor between correct rejections of critical lures and new words. In contrast, correct rejections of critical lures were accompanied by higher activation of a sustained positive slow wave (SPSW) in right fronto-central electrodes beyond 1200 ms. This result reveals a key role of post-retrieval processes in recognition. Results are discussed in light of theoretical approaches to false memory in the DRM paradigm.

Pain E-motion Faces Database (PEMF): Pain-related micro-clips for emotion research.

A large number of publications have focused on the study of pain expressions. Despite the growing knowledge, the availability of pain-related face databases is still very scarce compared with other emotional facial expressions. The Pain E-Motion Faces Database (PEMF) is a new open-access database currently consisting of 272 micro-clips of 68 different identities. Each model displays one neutral expression and three pain-related facial expressions: posed, spontaneous-algometer and spontaneous-CO2 laser. Normative ratings of pain intensity, valence and arousal were provided by students of three different European universities. Six independent coders carried out a coding process on the facial stimuli based on the Facial Action Coding System (FACS), in which ratings of intensity of pain, valence and arousal were computed for each type of facial expression. Gender and age effects of models across each type of micro-clip were also analysed. Additionally, participants' ability to discriminate the veracity of pain-related facial expressions (i.e., spontaneous vs posed) was explored. Finally, a series of ANOVAs were carried out to test the presence of other basic emotions and common facial action unit (AU) patterns. The main results revealed that posed facial expressions received higher ratings of pain intensity, more negative valence and higher arousal compared with spontaneous pain-related and neutral faces. No differential effects of model gender were found. Participants were unable to accurately discriminate whether a given pain-related face represented spontaneous or posed pain. PEMF thus constitutes a large open-source and reliable set of dynamic pain expressions useful for designing experimental studies focused on pain processes.

Tensor factorization approach for ERP-based assessment of schizotypy in a novel auditory oddball task on perceived family stress.

Objective. Schizotypy, a potential phenotype for schizophrenia, is a personality trait that depicts psychosis-like signs in the normal range of psychosis continuum. Family communication may affect the social functioning of people with schizotypy. Greater family stress, such as irritability, criticism and less praise, is perceived at a higher level of schizotypy. This study aims to determine the differences between people with high and low levels of schizotypy using electroencephalography (EEG) during criticism, praise and neutral comments. EEGs were recorded from 29 participants in the general community who varied from low schizotypy to high schizotypy (HS) during a novel emotional auditory oddball task.Approach. We consider the difference in event-related potential parameters, namely the amplitude and latency of P300 subcomponents (P3a and P3b), between pairs of target words (standard, positive, negative and neutral). A model based on tensor factorization is then proposed to detect these components from the EEG using the CANDECOMP/PARAFAC decomposition technique. Finally, we employ the mutual information estimation method to select influential features for classification.Main results.The highest classification accuracy, sensitivity, and specificity of 93.1%, 94.73%, and 90% are obtained via leave-one-out cross validation.Significance. This is the first attempt to investigate the identification of individuals with psychometrically-defined HS from brain responses that are specifically associated with perceiving family stress and schizotypy. By measuring these brain responses to social stress, we achieve the goal of improving the accuracy in detection of early episodes of psychosis.

Menstrual cycle and exogenous attention toward emotional expressions.

Several studies suggest that the menstrual cycle affects emotional processing. However, these results may be biased by including women with premenstrual syndrome (PMS) in the samples. PMS is characterized by negative emotional symptomatology, such as depression and/or anxiety, during the luteal phase. This study aimed to explore the modulation of exogenous attention to emotional facial expressions as a function of the menstrual cycle in women without PMS. For this purpose, 55 women were selected (from an original volunteer sample of 790) according to rigorous exclusion criteria. Happy, angry, and neutral faces were presented as distractors, while both behavioral performance in a perceptual task and event-related potentials (ERPs) were recorded. This task was applied during both phases of the menstrual cycle (luteal and follicular, counterbalanced), and premenstrual symptomatology was monitored daily. Traditional and Bayesian ANOVAs on behavioral data (reaction times and errors in the task) and ERP indices (P1, N170, N2, and LPP amplitudes) confirmed the expected lack of an interaction of phase and emotion. Taken together, these results indicate that women free of PMS present steady exogenous attention levels to emotionally positive and negative stimuli regardless of the menstrual phase.

Exogenous Attention to Emotional Stimuli Presenting Realistic (3D) Looming Motion.

Previous research shows that dynamic stimuli, on the one hand, and emotional stimuli, on the other, capture exogenous attention due to their biological relevance. Through neural (ERPs) and behavioral measures (reaction times and errors), the present study explored the combined effect of looming motion and emotional content on attentional capture. To this end, 3D-recreated static and dynamic animals assessed as emotional (positive or negative) or neutral were presented as distractors while 71 volunteers performed a line orientation task. We observed a two-phase effect: firstly (before 300 ms), early components of ERPs (P1p and N2po) showed enhanced exogenous attentional capture by looming positive distractors and static threatening animals. Thereafter, dynamic and static threatening distractors received enhanced endogenous attention as revealed by both late ERP activity (LPC) and behavioral (errors) responses. These effects are likely explained by both the emotional valence and the distance of the stimulus at each moment.

Suppression of alpha-band power underlies exogenous attention to emotional distractors.

Alpha-band oscillations (8-14 Hz) are essential for attention and perception processes by facilitating the selection of relevant information. Directing visuospatial endogenous (voluntary) attention to a given location consistently results in a power suppression of alpha activity over occipito-parietal areas contralateral to the attended visual field. In contrast, the neural oscillatory dynamics underlying the involuntary capture of attention, or exogenous attention, are currently under debate. By exploiting the inherent capacity of emotionally salient visual stimuli to capture attention, we aimed to investigate whether exogenous attention is characterized by either a reduction or an increase in alpha-band activity. Electroencephalographic activity was recorded while participants completed a Posner visuospatial cueing task, in which a lateralized image with either positive, negative, or neutral emotional content competed with a target stimulus presented in the opposite hemifield. Compared with trials with no distractors, alpha power was reduced over occipital regions contralateral to distracting images. This reduction of alpha activity turned out to be functionally relevant, as it correlated with impaired behavioral performance on the ongoing task and was enhanced for distractors with negative valence. Taken together, our results demonstrate that visuospatial exogenous attention is characterized by a suppression of alpha-band activity contralateral to distractor location, similar to the oscillatory underpinnings of endogenous attention. Further, these results highlight the key role of exogenous attention as an adaptive mechanism for the efficient detection of biologically salient stimuli.

Fast unconscious processing of emotional stimuli in early stages of the visual cortex.

Several cortical and subcortical brain areas have been reported to be sensitive to the emotional content of subliminal stimuli. However, the timing of these activations remains unclear. Our scope was to detect the earliest cortical traces of emotional unconscious processing of visual stimuli by recording event-related potentials (ERPs) from 43 participants. Subliminal spiders (emotional) and wheels (neutral), sharing similar low-level visual parameters, were presented at two different locations (fixation and periphery). The differential (peak-to-peak) amplitude from CP1 (77 ms from stimulus onset) to C2 (100 ms), two early visual ERP components originated in V1/V2 according to source localization analyses, was analyzed via Bayesian and traditional frequentist analyses. Spiders elicited greater CP1-C2 amplitudes than wheels when presented at fixation. This fast effect of subliminal stimulation-not reported previously to the best of our knowledge-has implications in several debates: 1) The amygdala cannot be mediating these effects, 2) latency of other evaluative structures recently proposed, such as the visual thalamus, is compatible with these results, 3) the absence of peripheral stimuli effects points to a relevant role of the parvocellular visual system in unconscious processing.

Realistic (3D) looming of emotional visual stimuli: Attentional effects at neural and behavioral levels.

Previous research shows that endogenous attention (the controlled selection of certain aspects of our environment) is enhanced toward emotional stimuli due to its biological relevance. Although looming affective stimuli such as threat seem even more critical for survival, little is known about their effect on endogenous attention. Here, we recorded neural (event-related potentials, ERPs) and behavioral responses (errors and reaction times) to explore the combined effect of emotion and looming motion. 3D-recreated static and moving animals assessed as emotionally positive, negative, and neutral, were presented to participants (n = 71), who performed an indirect categorization task (vertebrate vs. invertebrate). Behavioral results showed better task performance, as reflected by lower number of errors and reaction times, in response to threatening stimuli. Neural indices revealed significant early (P1p, 150 milliseconds), intermediate (P2p, 240), and late (LPP, 450) effects, the latter being more intensely associated with behavior, as revealed by regression analyses. In general, neural indexes of attention to both static and dynamic stimuli showed a positivity offset in early stages and a negativity bias in subsequent phases. However, and importantly, the progressive inclusion of negative stimuli in the attentional focus is produced earlier in the case of dynamic (at P2p latency) than in static versions (at LPP). These results point to an enhancement of attention, particularly in temporal terms, toward stimuli combining motion and biological significance.

Stimulus-response learning and expected reward value enhance stimulus cognitive processing: An ERP study.

Reward affects our attention to stimuli, prioritizing those that lead to high-value outcomes. Recently, it has been suggested that such reward-related cognitive prioritization might be associated with the process of learning new stimulus-response (S-R) associations, because both are acquired through extended reward training, and once established, they are hard to overcome. We used event-related potentials (ERP) to analyze the contribution of S-R links to the formation of reward-related cognitive prioritization during reinforcement learning. Reward-related cognitive prioritization was measured by comparing the ERP signals for stimuli predicting high-value and low-value outcomes. In addition, we compared a strong S-R link (same stimulus, same response), with a weak S-R link condition (same stimulus, two different responses). The participants' performance was more accurate and faster when the procedure allowed for establishing strong S-R links and for high-value outcomes. Furthermore, those stimuli associated with strong S-R links showed a larger P3 amplitude at parietal sites. Value effects (larger ERP activity for those stimuli predicting a high-value outcome) were obtained at parietal and occipital sites in the P3 time window. However, value effects did not benefit from strong S-R links in either the P1 or the P3 components. These results suggest that strong S-R learning is not necessary to develop reward-related modulations of ERP activity.

Enhanced N170 to outgroup faces: Perceptual novelty or prejudice?

Habituation to ethnic ingroup members has been reported to be greater than to ethnic outgroup members. This pattern could be due to the lack of perceptive experience (familiarity) with outgroup facial morphs or, alternatively, to the prejudice held toward that outgroup. We explored this disjunctive in 71 participants, all Spanish, who were experimentally habituated to faces from their Ingroup and to faces from two unfamiliar outgroups, one for which there is low probability of prejudice in this population (Non-prejudiced Outgroup), and one for which the probability of prejudice is higher (Prejudiced Outgroup). We indexed habituation through event-related potentials, concretely as the differential amplitude of the face-sensitive N170 component from Initial to Final trials of each group. Afterward, participants completed several prejudice measures. N170 showed significant habituation to all faces, though it did not differ among groups. However, a regression analysis revealed that individual habituation to the Outgroup faces was inversely related to implicit prejudice scores. Importantly, N170 amplitudes were maximal for the Prejudiced Outgroup in both Initial and Final trials. We conclude that these effects are explained by the prejudice held toward a specific outgroup rather than perceptive experience.

Prejudice drives exogenous attention to outgroups.

Exogenous attention allows the automatic detection of relevant stimuli and the reorientation of our current focus of attention towards them. Faces from an ethnic outgroup tend to capture exogenous attention to a greater extent than faces from an ethnic ingroup. We explored whether prejudice toward the outgroup, rather than lack of familiarity, is driving this effect. Participants (N = 76) performed a digit categorization task while distractor faces were presented. Faces belonged to (i) a prejudiced outgroup, (ii) a non-prejudiced outgroup and (iii) their ingroup. Half of the faces were previously habituated in order to increase their familiarity. Reaction times, accuracy and event-related potentials (ERPs) were recorded to index exogenous attention to distractor faces. Additionally, different indexes of explicit and implicit prejudice were measured, the latter being significantly greater towards prejudiced outgroup. N170 amplitude was greater to prejudiced outgroup-regardless of their habituation status-than to both non-prejudiced outgroup and ingroup faces and was associated with implicit prejudice measures. No effects were observed at the behavioral level. Our results show that implicit prejudice, rather than familiarity, is under the observed attention-related N170 effects and that this ERP component may be more sensitive to prejudice than behavioral measures under certain circumstances.

Retinotopy of emotion: Perception of negatively valenced stimuli presented at different spatial locations as revealed by event-related potentials.

Scarce previous data on how the location where an emotional stimulus appears in the visual scene modulates its perception suggest that, for functional reasons, a perceptual advantage may exist, vertically, for stimuli presented at the lower visual field (LoVF) and, horizontally, for stimuli presented at the left visual field (LeVF). However, this issue has been explored through a limited number of spatial locations, usually in a single spatial dimension (e.g., horizontal) and invariant eccentricities. Event-related potentials (ERPs) were recorded from 39 participants perceiving brief neutral (wheels) and emotional stimuli (spiders) presented at 17 different locations, one foveal and 16 at different peripheral coordinates. As a secondary scope, we explored the role of the magnocellular (M) and the parvocellular (P) visual pathways by presenting an isoluminant/heterochromatic (P-biased) and a heteroluminant/isochromatic version (M-biased) of each stimulus. Emo > Neu effects were observed in PN1 (120 ms) for stimuli located at fovea, and in PN2 (215 ms) for stimuli located both at fovea and diverse peripheral regions. A factorial approach to these effects further revealed that: (a) emotional stimuli presented in the periphery are efficiently perceived, without evident decrease from para- to perifovea; (b) peripheral Emo > Neu effects are reflected 95 ms later than foveal Emo > Neu effects in ERPs; (c) LoVF is more involved than UVF in these effects; (d) our data fail to support the LeVF advantage previously reported, and (e) Emo > Neu effects were significant for both M and P stimuli.

Binocular rivalry and emotion: Implications for neural correlates of consciousness and emotional biases in conscious perception.

Studies of the neural correlates of consciousness (NCCs) combining MEG/EEG with behavioral data have described two main time ranges relating to conscious perception: 130-320 (the visual awareness negativity; VAN) and 300-500 (P3a) ms after stimulus onset. At the same time, two event-related potential (ERP) peaks have shown an emotional modulation of endogenous attention: the early posterior negativity (EPN; peaking around 250 msec) and the late positive potential (LPP, peaking around 600 msec). Furthermore, an emotional bias on conscious perception has been reported in Binocular Rivalry (BR) studies. Here, we combined an intermittent BR paradigm with neutral and emotional stimuli while recording the behavioral subjective perception and ERPs with two aims: i) to explore the NCCs of emotional content in the time ranges previously described, and ii) to study the emotional bias in conscious perception as first percept when neutral and emotional images rival against each other. First, results revealed a specific ERP emotional modulation (emotional content awareness modulation; ECAM) at the VAN time range. This was the first time window sensitive to the emotional information and showing the strongest modulation in conscious emotional content. Second, results revealed an emotional bias in conscious perception towards the positive valence. This work shows how conscious perception pertaining to emotional content relates to perceptual areas at the VAN latency, which supports the claim of the 130-320 msec time window as the earliest NCC and extends the claim to apply to more than visual perceptual features. Additionally, our findings show that positive and negative content modulates the conscious perception differently.

Response inhibition in borderline personality disorder: Neural and behavioral correlates.

Although response inhibition is thought to be important in borderline personality disorder (BPD), little is known about its neurophysiological basis. This study aimed to provide insight into this issue by capitalizaing on the high temporal resolution of electroencephalography and information provided by source localization methods. To this end, twenty unmedicated patients with BPD and 20 healthy control subjects performed a modified go/no-go task designed to better isolate the brain activity specifically associated with response inhibition. Event-related potentials (ERP) were measured and further analyzed at the scalp and source levels. Patients with BPD made more commission errors (failed inhibitions) than control subjects. Scalp ERP data showed that both groups displayed greater frontocentral P3 amplitude for no-go (response inhbition) than for go trials (response execution). However, source reconstruction data revealed that patients with BPD activated posterior parietal regions (precuneus) to inhibit their responses, whereas controls activated prefrontal regions (presupplementary motor area, preSMA). This dissociation was supported by a significant Region (precuneus, preSMA) x Trial Type (no-go, go) x Group (BPD, control) interaction. These findings extend our understanding of the neurophysiological basis of abnormal response inhibition in BPD, suggesting that patients with BPD recruit different brain regions for inhibiting prepotent responses compared to controls. Future research in larger, medication-naïve samples of patients with BPD is required to confirm and extend these findings.

Effects of social and affective content on exogenous attention as revealed by event-related potentials.

The social content of affective stimuli has been proposed as having an influence on cognitive processing and behaviour. This research was aimed, therefore, at studying whether automatic exogenous attention demanded by affective pictures was related to their social value. We hypothesised that affective social pictures would capture attention to a greater extent than non-social affective stimuli. For this purpose, we recorded event-related potentials in a sample of 24 participants engaged in a digit categorisation task. Distracters were affective pictures varying in social content, in addition to affective valence and arousal, which appeared in the background during the task. Our data revealed that pictures depicting high social content captured greater automatic attention than other pictures, as reflected by the greater amplitude and shorter latency of anterior P2, and anterior and posterior N2 components of the ERPs. In addition, social content also provoked greater allocation of processing resources as manifested by P3 amplitude, likely related to the high arousal they elicited. These results extend data from previous research by showing the relevance of the social value of the affective stimuli on automatic attentional processing.

Haptic recognition memory following short-term visual deprivation: Behavioral and neural correlates from ERPs and alpha band oscillations.

In the current study, we investigated the effects of short-term visual deprivation (2 h) on a haptic recognition memory task with familiar objects. Behavioral data, as well as event-related potentials (ERPs) and induced event-related oscillations (EROs) were analyzed. At the behavioral level, deprived participants showed speeded reaction times to new stimuli. Analyses of ERPs indicated that starting from 1000 ms the recognition of old objects elicited enhanced positive amplitudes only for the visually deprived group. Visual deprivation also influenced EROs. In this sense, we observed reduced power in the lower-1 alpha band for the processing of new compared to old stimuli between 500 and 750 ms. Overall, our data showed improved haptic recognition memory after a short period of visual deprivation. These effects were thought to reflect a compensatory mechanism that might have developed as an adaptive strategy for dealing with the environment when visual information is not available.

The influence of affective state on exogenous attention to emotional distractors: behavioral and electrophysiological correlates.

The interplay between exogenous attention to emotional distractors and the baseline affective state has not been well established yet. The present study aimed to explore this issue through behavioral measures and event-related potentials (ERPs). Participants (N = 30) completed a digit categorization task depicted over negative, positive or neutral distractor background pictures, while they experienced negative, positive and neutral affective states elicited by movie scenes. Behavioral results showed higher error rates and longer reaction times for negative distractors than for neutral and positive ones, irrespective of the current emotional state. Neural indices showed that the participants' affective state modulated N1 amplitudes, irrespective of distractor type, while the emotional charge of distractors modulated N2, irrespective of the emotional state. Importantly, an interaction of state and distractor type was observed in LPP. These results demonstrate that exogenous attention to emotional distractors is independent from modulating effects of the emotional baseline state at early, automatic stages of processing. However, attention to emotional distractors and affective state interact at later latencies.

A dual mechanism underlying alpha lateralization in attentional orienting to mental representation.

Numerous electrophysiological findings support the notion that selective attention modulates alpha oscillatory activity. Specifically, alpha enhancement and suppression can be dissociated in time and space. It is now accepted that selective attention operates in either the perceptual or the representational environments. Lateralized alpha activity resulting from directing attention to mental representations, might arise from a transient alpha desynchronization, as recent proposals hypothesized. However, the contribution of enhancement vs suppression, as well as their neural correlates to the lateralized alpha modulation remain unstudied. To investigate these questions, we recorded magnetoencephalography while participants performed a retrospective cueing paradigm. Time-frequency analysis revealed a larger transient alpha desynchronization for the sensors contralateral to the relevant items which originated from the ventral lateral occipital cortex. Additionally, greater ipsilateral alpha enhancement in the medial occipital cortex occurred later and was maintained until probe presentation. Based on these differences we reasoned that the former would reflect the allocation of selective attention to relevant items, while the later might signal the inhibition of the irrelevant external hemifield instead of irrelevant WM items. Altogether, our results suggest that alpha lateralization does not arise from a unitary phenomenon. Dissociated anatomical and temporal alpha activity might be signaling different functional roles.

Magnocellular Bias in Exogenous Attention to Biologically Salient Stimuli as Revealed by Manipulating Their Luminosity and Color.

Exogenous attention is a set of mechanisms that allow us to detect and reorient toward salient events-such as appetitive or aversive-that appear out of the current focus of attention. The nature of these mechanisms, particularly the involvement of the parvocellular and magnocellular visual processing systems, was explored. Thirty-four participants performed a demanding digit categorization task while salient (spiders or S) and neutral (wheels or W) stimuli were presented as distractors under two figure-ground formats: heterochromatic/isoluminant (exclusively processed by the parvocellular system, Par trials) and isochromatic/heteroluminant (preferentially processed by the magnocellular system, Mag trials). This resulted in four conditions: SPar, SMag, WPar, and WMag. Behavioral (RTs and error rates in the task) and electrophysiological (ERPs) indices of exogenous attention were analyzed. Behavior showed greater attentional capture by SMag than by SPar distractors and enhanced modulation of SMag capture as fear of spiders reported by participants increased. ERPs reflected a sequence from magnocellular dominant (P1p, ≃120 msec) to both magnocellular and parvocellular processing (N2p and P2a, ≃200 msec). Importantly, amplitudes in one N2p subcomponent were greater to SMag than to SPar and WMag distractors, indicating greater magnocellular sensitivity to saliency. Taking together, results support a magnocellular bias in exogenous attention toward distractors of any nature during initial processing, a bias that remains in later stages when biologically salient distractors are present.