Effects of attention and emotion on repetition priming and their modulation by cholinergic enhancement

We examined whether behavioral and neural effects of repeating faces are modulated by independent factors of selective attention, emotion, and cholinergic enhancement, during functional MRI. Face repetition occurred either between task-relevant (spatially attended) or task-irrelevant (unattended) stimuli; faces could be fearful or neutral; subjects received either placebo or physostigmine. Under placebo, a reaction time advantage occurred with repetition (i.e., priming) that did not differ between levels of attention, but was attenuated with emotion. Inferior temporo-occipital cortex demonstrated repetition decreases to both attended and unattended faces, and showed either equivalent or greater repetition decreases with emotional compared with neutral faces. By contrast, repetition decreases were attenuated for emotional relative to neutral faces in lateral orbitofrontal cortex. These results distinguish automatic repetition effects in sensory cortical regions from repetition effects modulated by emotion in orbitofrontal cortex, which parallel behavioral effects. Under physostigmine, unlike placebo, behavioral repetition effects were seen selectively for attended faces only, whereas emotional faces no longer impaired priming. Physostigmine enhanced repetition decreases in inferior occipital cortex selectively for attended faces, and reversed the emotional interaction with repetition in lateral orbitofrontal cortex. Thus we show that cholinergic enhancement both augments a neural signature of priming and modulates the effects of attention and emotion on behavioral and neural consequences of repetition.     

Neural basis of redundancy effects in visual object categorization

Bilateral redundant information often leads to improved detection performance compared to only unilateral input. This experiment investigates redundancy effects at the level of object processing in behavioral and functional imaging data. Subjects received different combinations of categorical information presented to both visual hemifields simultaneously. For pictures of faces as well as for pictures of buildings, response latencies were faster when two pictures from the same object category were presented compared to two pictures from different categories. This behavioral advantage was accompanied by increased activation in the respective object-selective areas, i.e. in the Fusiform Face Area (FFA) for pictures of faces and in the Parahippocampal Place Areas (PPAs) for pictures of buildings. These results suggest an involvement of visual object-selective areas in the behavioral redundancy gain.     

Attention bias to faces in Asperger Syndrome: a pictorial emotion Stroop study

BACKGROUND: Emotional Stroop tasks have shown attention biases of clinical populations towards stimuli related to their condition. Asperger Syndrome (AS) is a neuropsychiatric condition with social and communication deficits, repetitive behaviours and narrow interests. Social deficits are particularly striking, including difficulties in understanding others. METHOD: We investigated colour-naming latencies of adults with and without AS to name colours of pictures containing angry facial expressions, neutral expressions or non-social objects. We tested three hypotheses: whether (1) controls show longer colour-naming latencies for angry versus neutral facial expressions with male actors, (2) people with AS show differential latencies across picture types, and (3) differential response latencies persist when photographs contain females. RESULTS: Controls had longer latencies to pictures of male faces with angry compared to neutral expressions. The AS group did not show longer latencies to angry versus neutral expressions in male faces, instead showing slower latencies to pictures containing any facial expression compared to objects. When pictures contained females, controls no longer showed longer latencies for angry versus neutral expressions. However, the AS group still showed longer latencies to all facial picture types, compared to objects, providing further evidence that faces produce interference effects for this clinical group. CONCLUSIONS: The pictorial emotional Stroop paradigm reveals normal attention biases towards threatening emotional faces. The AS group showed Stroop interference effects to all facial stimuli regardless of expression or sex, suggesting that faces cause disproportionate interference in AS.     

Emotional arousal and activation of the visual cortex: An fMRI analysis

Functional activity in the visual cortex was assessed using functional magnetic resonance imaging technology while participants viewed a series of pleasant, neutral, or unpleasant pictures. Coronal images at four different locations in the occipital cortex were acquired during each of eight 12-s picture presentation periods (on) and 12-s interpicture interval (off). The extent of functional activation was larger in the right than the left hemisphere and larger in the occipital than in the occipitoparietal regions during processing of all picture contents compared with the interpicture intervals. More importantly, functional activity was significantly greater in all sampled brain regions when processing emotional (pleasant or unpleasant) pictures than when processing neutral stimuli. In Experiment 2, a hypothesis that these differences were an artifact of differential eye movements was ruled out. Whereas both emotional and neutral pictures produced activity centered on the calcarine fissure (Area 17), only emotional pictures also produced sizable clusters bilaterally in the occipital gyrus, in the right fusiform gyrus, and in the right inferior and superior parietal lobules.     

Emotional interference under low versus high executive control

Previous research has demonstrated that task‐irrelevant emotional distractors interfere with task performance especially under low phasic executive control (i.e., in nonconflict trials). In the present study, we measured medio‐frontal ERPs (N2 and correct‐related negativity, CRN) to elucidate which aspects of task performance are affected by emotional interference in a flanker task. To create emotional interference, negative and neutral pictures were presented during the flanker stimuli. N2 and CRN were reduced after negative pictures, indicating that conflict processing and performance monitoring are both affected by emotional interference. On the behavioral level, prolonged response times after negative pictures were observed under low phasic executive control (i.e., in compatible trials). Additionally, we explored whether emotional interference is modulated not only by phasic changes in executive control (i.e., conflict vs. nonconflict trials) but also by tonic changes in executive control (i.e., low vs. high overall conflict frequency). To this end, the flanker task consisted of two blocks with 25% versus 75% incompatible trials. Prolonged response times after negative pictures in compatible trials were observed only under low tonic executive control but not under high executive control.     

Fearful faces evoke a larger C1 than happy faces in executive attention task: An event-related potential study

Neural responses to negatively valenced stimuli such as fear are enhanced relative to positive or neutral stimuli, reflecting an emotional negativity bias. In the present study, high time resolution event related potential (ERP) techniques were used, to investigate whether C1, the earliest visually evoked potential, is modulated by emotional valence in the executive attention network. Subjects were instructed to respond to the expression of the face, while ignoring the content of word, in an emotional face-word Stroop task. We demonstrated modulation of C1 in response to fearful faces versus happy faces. The differentiation between detection of fearful and happy faces emerged at 60-90ms after the stimulus onset at the posterior electrode sites, and this early differentiation occurred regardless of whether the subject had viewed a congruent or incongruent trials (i.e., happy face with fear label or vice versa). The present results indicate that faces with a fearful expression capture processing resources at an early sensory processing stage.     

Distant influences of amygdala lesion on visual cortical activation during emotional face processing

Emotional visual stimuli evoke enhanced responses in the visual cortex. To test whether this reflects modulatory influences from the amygdala on sensory processing, we used event-related functional magnetic resonance imaging (fMRI) in human patients with medial temporal lobe sclerosis. Twenty-six patients with lesions in the amygdala, the hippocampus or both, plus 13 matched healthy controls, were shown pictures of fearful or neutral faces in task-releant or task-irrelevant positions on the display. All subjects showed increased fusiform cortex activation when the faces were in task-relevant positions. Both healthy individuals and those with hippocampal damage showed increased activation in the fusiform and occipital cortex when they were shown fearful faces, but this was not the case for individuals with damage to the amygdala, even though visual areas were structurally intact. The distant influence of the amygdala was also evidenced by the parametric relationship between amygdala damage and the level of emotional activation in the fusiform cortex. Our data show that combining the fMRI and lesion approaches can help reveal the source of functional modulatory influences between distant but interconnected brain regions.     

Relationship between trait anxiety, prefrontal cortex, and attention bias to angry faces in children and adolescents

Using event-related functional magnetic resonance imaging (fMRI) with a visual-probe task that assesses attention to threat, we investigated the cognitive and neurophysiological correlates of trait anxiety in youth. During fMRI acquisition, 16 healthy children and adolescents viewed angry-neutral face pairs and responded to a probe that was on the same (angry-congruent) or opposite (angry-incongruent) side as the angry face. Attention bias scores were calculated by subtracting participants' mean reaction time for angry-congruent trials from angry-incongruent trials. Trait anxiety was positively associated with attention bias towards angry faces. Neurophysiologically, trait anxiety was positively associated with right dorsolateral prefrontal cortex (PFC) activation on a contrast of trials that reflect the attention bias for angry faces (i.e. angry-incongruent versus angry-congruent trials). Trait anxiety was also positively associated with right ventrolateral PFC activation on trials with face stimuli (vesus baseline), irrespective of their emotional content.     

The processing of anticipated and unanticipated fearful faces: An ERP study

This study examined the processing of fearful and neutral expressions, which could either be anticipated or not from a prime word (i.e., 'fear' or 'neutral') with or without predictive value. In total, data from 17 participants (i.e., reaction times; ERP waveforms) were analyzed. ERP data showed that the expression effect (fearful vs. neutral faces) was different between predictable and unpredictable trials in early components (N1, N170 and P2) after face onset. However, the expression effect was essentially the same between predictable and unpredictable trials in late components (N300 and P3) after face onset. These results revealed that emotion processing of anticipated vs. non-anticipated stimuli differs mainly in the early stage of neural activity after face onset.     

Selective attention to threatening faces in delusion‐prone individuals

Introduction. Selective attention to threat‐related information has been associated with clinical delusions in schizophrenia and nonclinical delusional ideation in healthy individuals. However, it is unclear whether biased attention for threat reflects early engagement effects on selective attention, or later difficulties in disengaging attention from perceived threat. The present study examined which of these processes operate in nonclinical delusion‐prone individuals.

Methods. A total of 100 psychologically healthy participants completed the Peters et al. () Delusions Inventory (PDI). Twenty‐two scoring in the upper quartile (high‐PDI group) and 22 scoring in the lower quartile (low‐PDI group) completed a modified dot‐probe task. Participants detected dot‐probes appearing 200, 500, or 1250 ms after an angry‐neutral face pair or a happy‐neutral face pair.

Results. High‐PDI individuals responded faster to dot‐probes presented in the same location as angry compared to happy faces at the short 200 ms stimulus onset asynchrony (SOA), but only when the emotional faces were presented to the left visual field. At the two longer SOAs (500 ms, 1250 ms), the high‐PDI group were also faster to respond to dot‐probes presented in the same location as angry compared to happy faces and slower to respond to dot‐probes presented in different spatial locations to angry (vs. happy) faces. The latter effects were seen whether emotional faces were presented to the left or the right visual field.

Conclusions. Results support the operation of emotion‐selective engagement and defective disengagement for threat‐related facial expressions (i.e., anger) in delusion‐prone individuals.     

Is a neutral expression also a neutral stimulus? A study with functional magnetic resonance

Although neutral faces do not initially convey an explicit emotional message, it has been found that individuals tend to assign them an affective content. Moreover, previous research has shown that affective judgments are mediated by the task they have to perform. Using functional magnetic resonance imaging in 21 healthy participants, we focus this study on the cerebral activity patterns triggered by neutral and emotional faces in two different tasks (social or gender judgments). Results obtained, using conjunction analyses, indicated that viewing both emotional and neutral faces evokes activity in several similar brain areas indicating a common neural substrate. Moreover, neutral faces specifically elicit activation of cerebellum, frontal and temporal areas, while emotional faces involve the cuneus, anterior cingulated gyrus, medial orbitofrontal cortex, posterior superior temporal gyrus, precentral/postcentral gyrus and insula. The task selected was also found to influence brain activity, in that the social task recruited frontal areas while the gender task involved the posterior cingulated, inferior parietal lobule and middle temporal gyrus to a greater extent. Specifically, in the social task viewing neutral faces was associated with longer reaction times and increased activity of left dorsolateral frontal cortex compared with viewing facial expressions of emotions. In contrast, in the same task emotional expressions distinctively activated the left amygdale. The results are discussed taking into consideration the fact that, like other facial expressions, neutral expressions are usually assigned some emotional significance. However, neutral faces evoke a greater activation of circuits probably involved in more elaborate cognitive processing.     

Emotion Processing in the Visual Brain: A MEG Analysis

Recent functional magnetic resonance imaging (fMRI) and event-related brain potential (ERP) studies provide empirical support for the notion that emotional cues guide selective attention. Extending this line of research, whole head magneto-encephalogram (MEG) was measured while participants viewed in separate experimental blocks a continuous stream of either pleasant and neutral or unpleasant and neutral pictures, presented for 330 ms each. Event-related magnetic fields (ERF) were analyzed after intersubject sensor coregistration, complemented by minimum norm estimates (MNE) to explore neural generator sources. Both streams of analysis converge by demonstrating the selective emotion processing in an early (120–170 ms) and a late time interval (220–310 ms). ERF analysis revealed that the polarity of the emotion difference fields was reversed across early and late intervals suggesting distinct patterns of activation in the visual processing stream. Source analysis revealed the amplified processing of emotional pictures in visual processing areas with more pronounced occipito-parieto-temporal activation in the early time interval, and a stronger engagement of more anterior, temporal, regions in the later interval. Confirming previous ERP studies showing facilitated emotion processing, the present data suggest that MEG provides a complementary look at the spread of activation in the visual processing stream.     

Affective engagement for facial expressions and emotional scenes: the influence of social anxiety

Pictures of emotional facial expressions or natural scenes are often used as cues in emotion research. We examined the extent to which these different stimuli engage emotion and attention, and whether the presence of social anxiety symptoms influences responding to facial cues. Sixty participants reporting high or low social anxiety viewed pictures of angry, neutral, and happy faces, as well as violent, neutral, and erotic scenes, while skin conductance and event-related potentials were recorded. Acoustic startle probes were presented throughout picture viewing, and blink magnitude, probe P3 and reaction time to the startle probe also were measured. Results indicated that viewing emotional scenes prompted strong reactions in autonomic, central, and reflex measures, whereas pictures of faces were generally weak elicitors of measurable emotional response. However, higher social anxiety was associated with modest electrodermal changes when viewing angry faces and mild startle potentiation when viewing either angry or smiling faces, compared to neutral. Taken together, pictures of facial expressions do not strongly engage fundamental affective reactions, but these cues appeared to be effective in distinguishing between high and low social anxiety participants, supporting their use in anxiety research.     

Trait anger predicts relative left frontal cortical activation to anger-inducing stimuli.

Building on past research that has suggested that relatively greater left frontal cortical activity is associated with approach-related anger and that individuals who are high in trait anger are more likely to evidence angry responses, the present research tested whether individuals high in trait anger would be more likely to evidence relatively greater left frontal cortical activity in response to anger-eliciting pictorial stimuli. In the experiment, participants were exposed to pictures intended to evoke anger, fear/disgust, positive, or neutral affective reactions. Electroencephalographic (EEG) activity was recorded continuously, and alpha power was derived from the EEG to measure cortical activity. Trait anger was measured using the Buss and Perry Aggression Questionnaire [Buss, A.H., Perry, M., 1992. The aggression questionnaire. Journal of Personality and Social Psychology, 63, 452-459]. Results revealed that trait anger was positively related to greater relative left frontal cortical activity to anger-evoking pictures but not to other types of pictures.     

A freezing-like posture to pictures of mutilation

Postural sway and heart rate were recorded in young men viewing emotionally engaging pictures. It was hypothesized that they would show a human analog of "freezing" behavior (i.e., immobility and heart rate deceleration) when confronted with a sustained block of unpleasant (mutilation) images, relative to their response to pleasant/arousing (sport action) or neutral (objects) pictures. Volunteers stood on a stabilometric platform during picture viewing. Significantly reduced body sway was recorded during the unpleasant pictures, along with increased mean power frequency (indexing muscle stiffness). Heart rate during unpleasant pictures also showed the expected greater deceleration. This pattern resembles the "freezing" and "fear bradycardia" seen in many species when confronted with threatening stimuli, mediated by neural circuits that promote defensive survival.     

Negative expectations influence behavioral and ERP responses in the subsequent recognition of expectancy-incongruent neutral events

Previous studies have shown that expectancy incongruence in emotional stimuli influences the encoding (i.e., the first stage of memory processing) of the stimuli. However, it is unknown about whether expectancy incongruence influences later stages of memory processing, such as recognition. To this end, expectancy cues were presented prior to emotional pictures. Most often, the cues accurately indicated the emotional consequences of the pictures, but in some cases the consequence was incongruent with the expectations, and a picture from another emotional category was presented. Afterward, participants completed an unexpected recognition task in which old and novel pictures were not preceded by expectancy cues. The results showed that, in the encoding phase, expectancy incongruence reduced response accuracy when categorizing pictorial emotions, and the effect was smaller for neutral pictures than for negative pictures. ERP results showed stronger and weaker responses to expectancy incongruent pictures compared to congruent pictures in time ranges related to the encoding-related early and middle late positive potential (LPP), respectively. In the subsequent recognition phase, d′ scores were higher for incongruent neutral pictures than for congruent ones. Expectancy incongruence enlarged the P2 response but reduced the recognition-related early LPP response for neutral pictures. However, effects of expectancy incongruence were not seen for negative pictures. Therefore, the findings in the present study indicate that negative expectations influence the later recognition of expectancy incongruent neutral events, whereas negative events are more resistant to the effects of expectation incongruence.     

Attentional selectivity for emotional faces: Evidence from human electrophysiology

This study investigated the temporal course of attentional biases for threat-related (angry) and positive (happy) facial expressions. Electrophysiological (event-related potential) and behavioral (reaction time [RT]) data were recorded while participants viewed pairs of faces (e.g., angry face paired with neutral face) shown for 500 ms and followed by a probe. Behavioral results indicated that RTs were faster to probes replacing emotional versus neutral faces, consistent with an attentional bias for emotional information. Electrophysiological results revealed that attentional orienting to threatening faces emerged earlier (early N2pc time window; 180–250 ms) than orienting to positive faces (after 250 ms), and that attention was sustained toward emotional faces during the 250–500-ms time window (late N2pc and SPCN components). These findings are consistent with models of attention and emotion that posit rapid attentional prioritization of threat.     

Threat sensitivity as assessed by automatic amygdala response to fearful faces predicts speed of visual search for facial expression

It has been argued that the amygdala represents an integral component of a vigilance system that is primarily involved in the perception of ambiguous stimuli of biological relevance. The present investigation was conducted to examine the relationship between automatic amygdala responsivity to fearful faces which may be interpreted as an index of trait-like threat sensitivity and spatial processing characteristics of facial emotions. During 3T fMRI scanning, pictures of human faces bearing fearful, angry, and happy expressions were presented to 20 healthy volunteers using a backward masking procedure based on neutral facial expressions. Subsequently, a computer-based face-in-the-crowd task using schematic face stimuli was administered. The neural response of the (right) amygdala to masked fearful faces correlated consistently with response speed to negative and neutral faces. Neither amygdala activation during the masked presentation of angry faces nor amygdala activation during the presentation of happy faces was correlated with any of the response latencies in the face-in-the-crowd task. Our results suggest that amygdala responsivity to masked facial expression is differentially related to the general visual search speed for facial expression. Neurobiologically defined threat sensitivity seems to represent an important determinant of visual scanning behaviour.     

State anxiety and affective physiology: effects of sustained exposure to affective pictures

Effects of sustained exposure to emotional stimuli on affective reactions and their recovery were examined to determine whether increasing exposure to a specific emotional content (e.g., unpleasant) cumulatively affects physiological responses; and whether motivational activation persists following sustained exposure. Participants viewed pleasant, neutral, and unpleasant IAPS pictures, presented in blocks separated by an inter-block interval. With increasing exposure to unpleasant pictures, startle magnitude showed greater potentiation, and corrugator EMG activity increased. Both affective startle and corrugator modulation persisted following exposure to unpleasant pictures. The cumulative effects of sustained exposure to unpleasant pictures were enhanced for those reporting higher state anxiety, consistent with the hypothesis that sustained aversive exposure leads to increased defensive activation. These findings suggest sustained exposure to unpleasant pictures may induce a short-term mood state, and may be a useful paradigm to study individuals who vary in symptoms of anxiety.     

Stimulus type and design influence hemodynamic responses towards visual disgust and fear elicitors.

The question to what extent emotion-related brain activation depends upon the presentation design (block design vs. event-related design) and the stimulus type (scene pictures vs. pictures with facial mimic) has hardly been addressed in previous functional magnetic resonance imaging (fMRI) research. In the present fMRI experiment, 40 right-handed subjects viewed pictures with fear-inducing and disgust-inducing content as well as facial expressions of fear and disgust. Pictures of neutral objects and neutral facial mimic were used as control stimuli. The pictures were presented in a block design for half of the subjects; the other half viewed the same stimuli as singular events in randomized sequence. The participants had been instructed to passively view the pictures. Disgust-evoking scenes provoked activation in the amygdala, the insula and the orbitofrontal cortex (OFC). This applied to the blocked as well as to the event-related design. Fear-relevant scenes were associated with activity in the insula, the OFC and the middle temporal gyri in the event-related design. The presentation in a block design only led to activation in the middle temporal gyri. Facial expressions of disgust and fear did not trigger significant activation neither in the blocked nor event-related design. This surprising outcome may be a result of context and task effects. The face stimuli which were presented together with the more complex scenes in a passive viewing paradigm possibly were not salient enough to trigger emotional processing.