Neural response to emotional faces with and without awareness: event-related fMRI in a parietal patient with visual extinction and spatial neglect

This study examined whether differential neural responses are evoked by emotional stimuli with and without conscious perception, in a patient with visual neglect and extinction. Stimuli were briefly shown in either right, left, or both fields during event-related fMRI. On bilateral trials, either a fearful or neutral left face appeared with a right house, and it could either be extinguished from awareness or perceived. Seen faces in left visual field (LVF) activated primary visual cortex in the damaged right-hemisphere and bilateral fusiform gyri. Extinguished left faces increased activity in striate and extrastriate cortex, compared with right houses only. Critically, fearful faces activated the left amygdala and extrastriate cortex both when seen and when extinguished; as well as bilateral orbitofrontal and intact right superior parietal areas. Comparison of perceived versus extinguished faces revealed no difference in amygdala for fearful faces. Conscious perception increased activity in fusiform, parietal and prefrontal areas of the left-hemisphere, irrespective of emotional expression; while a differential emotional response to fearful faces occurring specifically with awareness was found in bilateral parietal, temporal, and frontal areas. These results demonstrate that amygdala and orbitofrontal cortex can be activated by emotional stimuli even without awareness after parietal damage; and that substantial unconscious residual processing can occur within spared brain areas well beyond visual cortex, despite neglect and extinction.     

Behavioral and electrophysiological evidence of a right hemisphere bias for the influence of negative emotion on higher cognition

We examined how responses to aversive pictures affected performance and stimulus-locked event-related potentials (ERPs) recorded during a demanding cognitive task. Numeric Stroop stimuli were brief ly presented to either left or right visual hemifield (LVF and RVF, respectively) after a centrally presented aversive or neutral picture from the International Affective Picture System. Subjects indicated whether a quantity value from each Stroop stimulus matched the preceding Stroop stimulus while passively viewing the pictures. After aversive pictures, responses were more accurate for LVF Stroops and less accurate for RVF Stroops. Early-latency extrastriate attention-dependent visual ERPs were enhanced for LVF Stroops. The N2 ERP was enhanced for LVF Stroops over the right frontal and parietal scalp sites. Slow potentials (300-800 msec) recorded over the frontal and parietal regions showed enhanced picture related modulation and amplitude for LVF Stroops. These results suggest that emotional responses to aversive pictures selectively facilitated right hemisphere processing during higher cognitive task performance.     

Negative content enhances stimulus‐specific cerebral activity during free viewing of pictures,faces, and words

Negative visual stimuli have been found to elicit stronger brain activation than do neutral stimuli. Such emotion effects have been shown for pictures, faces, and words alike, but the literature suggests stimulus‐specific differences regarding locus and lateralization of the activity. In the current functional magnetic resonance imaging study, we directly compared brain responses to passively viewed negative and neutral pictures of complex scenes, faces, and words (nouns) in 43 healthy participants (21 males) varying in age and demographic background. Both negative pictures and faces activated the extrastriate visual cortices of both hemispheres more strongly than neutral ones, but effects were larger and extended more dorsally for pictures, whereas negative faces additionally activated the superior temporal sulci. Negative words differentially activated typical higher‐level language processing areas such as the left inferior frontal and angular gyrus. There were small emotion effects in the amygdala for faces and words, which were both lateralized to the left hemisphere. Although pictures elicited overall the strongest amygdala activity, amygdala response to negative pictures was not significantly stronger than to neutral ones. Across stimulus types, emotion effects converged in the left anterior insula. No gender effects were apparent, but age had a small, stimulus‐specific impact on emotion processing. Our study specifies similarities and differences in effects of negative emotional content on the processing of different types of stimuli, indicating that brain response to negative stimuli is specifically enhanced in areas involved in processing of the respective stimulus type in general and converges across stimuli in the left anterior insula.     

Emotional words: what's so different from just words?

Aphasic patients, in particular global aphasics, may still swear and produce emotional utterances with ease. Based on these clinical observations we investigated emotional word "reading" in a series of different experiments over 25 years, not only in aphasic patients, but also in the left (LVF) and right (RVF) visual fields of healthy subjects, and in a depth-recorded epileptic patient. Across these experiments we found: i) behaviorally a strong emotional word effect in the left visual field (right hemisphere - RH) of normals, correlating well with the emotional word performance of aphasic patients, pointing to a specific role of the right hemisphere; ii) electro-physiologically a specific early (100-140 msec) brain response to emotional words during scalp recordings in healthy subjects subsequent to right visual field (left hemisphere - LH) stimulation, that source localization procedures project to posterior areas of the right hemisphere; iii) preliminary data of a very early (60 msec) activation of the left amygdala in a depth-recorded epileptic patient when the same emotional words were presented to the right visual field (left hemisphere); and iv) a consistent gender difference showing that the above findings might be relevant for men only. Both hemispheres therefore appear to be implicated in emotional word "reading" but in different ways. We propose that the left amygdala via extrastriate connections acts as a detector of emotional word content at a very early stage of processing; that this amygdala response subsequently modulates the cortical response to emotional words asymmetrically, rendering the left visual cortex less sensitive to emotional words than that of the right hemisphere; and that this modulation is gender dependent.     

Emotional facial expressions capture attention

OBJECTIVE: To determine whether the emotional significance of stimuli can influence spatial attention. BACKGROUND: Motivational and emotional factors may affect attention toward stimuli. However, this has never been examined in brain-damaged patients who present with unilateral inattention due to left spatial neglect. METHODS: The authors studied three patients with chronic left neglect and visual extinction after right parietal stroke. Shapes or faces with neutral, happy, or angry expressions were briefly presented in the right, left, or both visual fields. On unilateral trials, the patients detected all stimuli equally on both sides. On bilateral trials, they extinguished faces in the contralesional field much less often than shapes, and faces with happy or angry facial expressions much less than faces with a neutral expression. CONCLUSION: Facial features and emotional expressions can be analyzed despite lying on the unattended side, and may influence the spatial distribution of attention. These findings support the view that attention is controlled by neural mechanisms involving not only frontoparietal areas but also limbic components in cingulate cortex and amygdala, which may interact with ventral visual areas in the temporal lobe to detect affective value and prioritize attention to salient stimuli.     

Brain activity during expectancy of emotional stimuli: an fMRI study

We studied the neural activation associated with the expectancy of emotional stimuli using whole brain fMRI. Fifteen healthy subjects underwent fMRI scanning during which they performed a warned reaction task using emotional pictures carrying pleasant, unpleasant, or neutral content. The task involved an expected or unexpected condition. Data were analyzed by comparing the images acquired under the different conditions. In the expected condition, compared with the unexpected condition, significant activation was observed in the medial, inferior and dorsolateral prefrontal cortex. Whereas the expectancy of pleasant stimuli produced activation in the left dorsolateral and left medial prefrontal cortex as well as in the right cerebellum, the expectancy of unpleasant stimuli produced activation in the right inferior and right medial prefrontal cortex, the right amygdala, the left anterior cingulate cortex, and bilaterally in the visual cortex. These results suggest that the expectancy of emotional stimuli is mediated by the prefrontal area including the medial, inferior, and dorsolateral prefrontal cortex. Furthermore, our data suggest that left frontal activation is associated with the expectancy of pleasant stimuli and that right frontal activation is associated with the expectancy of unpleasant stimuli. Finally, our findings suggest that the amygdala and anterior cingulate cortex may play an important role in the expectancy of unpleasant stimuli and that the input of this negative information is modulated by these specific brain areas.     

Hemispheric differences in neural systems for face working memory: A PET-rCBF study

Neural systems that participate in working memory for faces were investigated in an experiment designed to distinguish face perception areas from working memory areas. Regional cerebral blood flow (rCBF) was measured using positron emission tomography (PET) while subjects performed a sensorimotor control task, a face perception control task, and five working memory tasks with parametrically varied retention intervals, ranging from 1 to 21 sec. Striate and ventral occipitotemporal extrastriate areas demonstrated a simple negative correlation between rCBF and retention delay, indicating that these areas participate principally in perceptual operations performed during visual stimulation. By contrast, right and left frontal areas demonstrated rCBF increases that were significantly more sustained across delays than were increases in ventral extrastriate areas, but the relation between rCBF and retention interval differed significantly by hemisphere. Whereas right frontal rCBF showed a nonsignificant tendency to diminish at longer delays, left inferior frontal, middle frontal, and anterior cingulate cortex, as well as left parietal and inferior temporal cortex, demonstrated their largest rCBF increases at the longest delays. These results indicate that right frontal and left frontal, parietal, and temporal areas all participate in face working memory, but that left hemisphere areas are associated with a more durable working memory representation or strategy that subjects rely on increasingly with longer retention intervals. One possible explanation for this hemispheric difference is that left hemisphere activity is associated with a face representation that embodies the result of more analysis and elaboration, whereas right frontal activity is associated with a simpler, icon-like image of a face that is harder to maintain in working memory. © 1995 Wiley-Liss, Inc.     

Transient interference of right hemispheric function due to automatic emotional processing

We examined the effects of emotional stimuli on right and left hemisphere detection performance in a hemifield visual discrimination task. A group of 18 healthy subjects were asked to discriminate between upright and inverted triangles (target). Targets were randomly presented in the left or right visual hemifield (150 ms target duration). A brief emotional picture (pleasant or unpleasant; 150 ms stimulus duration) or neutral picture selected from the International Affective Picture System was randomly presented either in the same (47%) or the opposite (47%) spatial location to the subsequent target. Emotional or neutral stimuli offset 150 ms prior to the subsequent target. Subjects were instructed to ignore the pictures and respond to the targets as quickly and accurately as possible. Independent of field of presentation, emotional stimuli prolonged reaction times (P < 0.01) to LVF targets, with unpleasant stimuli showing a greater effect than pleasant stimuli. The current study shows that brief emotional stimuli selectively impair right hemispheric visual discrimination capacity. The findings suggest automatic processing of emotional stimuli captures right hemispheric processing resources and transiently interferes with other right hemispheric functions.     

Cortical responses to self and others

The extrastriate body area (EBA) is one among the multiple, functionally specialized regions of the human visual cortex exhibiting modulation by body-related stimuli. Here we investigate whether activation patterns differ for the perception of one's own body and the bodies of others. We used functional magnetic resonance imaging to identify body-related brain areas and to see how these areas differentiate between images of one's own body and those of others in the absence of facial or motion cues. Whole brain explorative group-level analysis identified body-related blood oxygen level dependent (BOLD) signal enhancement in five regions of the right and in one region of the left hemisphere (right: in the extrastriate visual and parietal cortex and in the precentral gyrus, left: in the extrastriate visual cortex). General linear model group-level random effects analysis of the self-other contrast revealed self-related responses in the extrastriate and parietal regions in the right hemisphere but also in the right middle frontal gyrus. These results suggest the existence of a cortical network for the extraction of body-related information and another cortical network for the extraction of self-related body information. The two networks partially overlap in the right superior and inferior parietal cortices, but are clearly segregated in the extrastriate visual cortex and in the middle frontal gyrus. In addition, we report that the classical EBA is only involved in the analysis of body-related information but not in the assignment of body identity. The latter appears to be accomplished by a network in right hemisphere comprising the fusiform body area, regions of the superior parietal lobe, the inferior parietal cortex, and the middle frontal gyrus.     

Semantic category effects modulate visual priming in neglect patients

Previous studies indicate that extinguished stimuli can still be unconsciously processed, leading to implicit priming effects. Here we investigated whether these implicit effects might be modulated by the semantic nature of the stimuli. Five neglect patients and ten controls performed an identification task of items belonging to living and non-living categories. In the study phase photographs of animals and artifacts were presented either to the left visual field (LVF) or to the right visual field (RVF). In the identification phase, each stimulus was displayed centrally and was revealed in a sequence of frames where the item was represented by an increasingly less and less filtered image up to a complete version. The results showed that lateralized stimuli differentially affected controls’ and neglect patients’ memory retrieval. In controls memory traces from the study phase served as efficient primes, thereby reducing the amount of information necessary for the identification of both stimulus categories. Moreover, hemispheric differences emerged with an advantage of the RVF/left hemisphere for artifact items, while no difference was found for living things. Neglect patients showed a priming effect for artifact items presented either to the RVF/left hemisphere or LVF/right hemisphere, as well as for living items presented to the RVF/left hemisphere, but not for living items presented to the LVF/right hemisphere. The priming effect observed for extinguished artifacts is consistent with the evidence of the existence of a specific mechanism destined to analyze, in an automatic and implicit fashion, motor-relevant information of manipulable objects and tools, which are important for identification process. Results are discussed in relation to current models of organization of conceptual knowledge within the framework of different processes performed by the two hemispheres.     

Abnormal neural responses to emotional visual stimuli in adolescents with conduct disorder.

BACKGROUND: It is widely held that aggression and antisocial behavior arise as a consequence of a deficiency in responding to emotional cues in the social environment. We asked whether neural responses evoked by affect-laden pictures would be abnormal in adolescents with conduct disorder (CD). METHODS: Functional magnetic resonance imaging during passive viewing of pictures with neutral or strong negative affective valence was performed in 13 male adolescents with severe CD aged 9 to 15 years and in 14 healthy age-matched control subjects. RESULTS: Main effects for negative-neutral affective valence included activations in the amygdala and hippocampus, ventral extrastriate visual cortex, and intraparietal sulcus bilaterally. There was a significant group-by-condition interaction in the right dorsal anterior cingulate cortex that was due to a pronounced deactivation in the patient group during viewing of negative pictures. When correcting for anxiety and depressive symptoms, we additionally found a reduced responsiveness of the left amygdala to negative pictures in patients compared with control subjects. CONCLUSIONS: We suggest that these findings reflect an impairment of both the recognition of emotional stimuli and the cognitive control of emotional behavior in patients with CD, resulting in a propensity for aggressive behavior.     

Now you see it, now you don't: variable hemineglect in a commissurotomized man

We describe the case of a callosotomized man, D.D.V., who shows unusual neglect of stimuli in the left visual field (LVF). This is manifest in simple reaction time (RT) to stimuli flashed in the LVF and in judging whether pairs of filled circles in the LVF are of the same or different color. It may reflect strong left-hemispheric control and consequent attention restricted to the right side of space. It is not evident in simple RT when there are continuous markers in the visual fields to indicate the locations of the stimuli. In this condition, his RTs are actually faster to LVF than to right visual field (RVF) stimuli, suggesting a switch to right-hemispheric control that eliminates the hemineglect. Neglect is also not evident when D.D.V. responds by pointing to or touching the locations of the stimuli, perhaps because these responses are controlled by the dorsal rather than the ventral visual system. Despite his atypical manifestations of hemineglect, D.D.V. showed evidence of functional disconnection typical of split-brained subjects, including prolonged crossed-uncrossed different in simple reaction time, inability to match colors between visual fields, and enhanced redundancy gain in simple RT to bilateral stimuli even when the stimulus in the LVF was neglected.     

Right hemispheric dysfunction in schizophrenia

This study uses the Poffenberger (1912) paradigm, which compares the difference between "crossed" (stimuli and motor response areas are contralateral) and "uncrossed" (stimuli and motor response areas are ipsilateral) conditions to estimate interhemispheric transfer time. Simple reaction time (RT) was recorded to stimuli presented to the left visual field (LVF), right visual field (RVF), or bilaterally (BVF) in individuals with schizophrenia (n = 10) and controls (n = 14), who responded using either the left or right hand. While the results provide no evidence for differences between the groups in information transfer between the hemispheres, the schizophrenia group were significantly slower to respond to LVF stimuli, suggesting right hemisphere dysfunction.     

How affective information from faces and scenes interacts in the brain

Facial expression perception can be influenced by the natural visual context in which the face is perceived. We performed an fMRI experiment presenting participants with fearful or neutral faces against threatening or neutral background scenes. Triangles and scrambled scenes served as control stimuli. The results showed that the valence of the background influences face selective activity in the right anterior parahippocampal place area (PPA) and subgenual anterior cingulate cortex (sgACC) with higher activation for neutral backgrounds compared to threatening backgrounds (controlled for isolated background effects) and that this effect correlated with trait empathy in the sgACC. In addition, the left fusiform gyrus (FG) responds to the affective congruence between face and background scene. The results show that valence of the background modulates face processing and support the hypothesis that empathic processing in sgACC is inhibited when affective information is present in the background. In addition, the findings reveal a pattern of complex scene perception showing a gradient of functional specialization along the posterior–anterior axis: from sensitivity to the affective content of scenes (extrastriate body area: EBA and posterior PPA), over scene emotion–face emotion interaction (left FG) via category–scene interaction (anterior PPA) to scene–category–personality interaction (sgACC).     

Orbitofrontal cortex biases attention to emotional events

We examined the role of orbitofrontal (OF) cortex in regulating emotion-attention interaction and the balance between involuntary and voluntary attention allocation. We studied patients with OF lesion applying reaction time (RT) and event-related potential (ERP) measures in a lateralized visual discrimination task with novel task-irrelevant affective pictures (unpleasant, pleasant, or neutral) preceding a neutral target. This allowed for comparing the effects of automatic attention allocation to emotional versus neutral stimuli on subsequent voluntary attention allocation to target stimuli. N2-P3a and N2-P3b ERP components served as measures of involuntary and voluntary attention allocation correspondingly. Enhanced N2-P3a amplitudes to emotional distractors and reduced N2-P3b amplitudes to targets preceded by emotional distractors were observed in healthy subjects, suggesting automatic emotional orienting interfered with subsequent voluntary orienting. OF patients showed an opposite pattern with tendency towards reduced N2-P3a responses to emotional distractors, suggesting impaired automatic orienting to emotional stimuli due to orbitofrontal damage. Enhanced N2-P3b responses to targets preceded by any affective distractor were observed in OF patients, suggesting bias towards voluntary target-related attention allocation due to orbitofrontal lesion. Behavioral evidence indicated that left visual field (LVF) attention performance was modulated by emotional stimuli. Specifically, OF patients responded faster to LVF targets subsequent to pleasant emotional distractors. We suggest that damage to the orbitofrontal circuitry leads to dysbalance between voluntary and involuntary attention allocation in the context of affective distractors with predisposition to posterior target-related processing over frontal novelty and affect-related processing. Furthermore, we suggest that orbitofrontal influence on emotion-attention interaction is valence and hemisphere dependent.     

Implicit associative priming in a patient with left visual neglect

Recent studies have suggested that patients with visual neglect may process, even if without awareness, perceptual features of the neglected stimuli. The aim of the current study was to further investigate whether the ignored stimuli are processed at a deeper level. Findings from a patient with damage to the right hemisphere and with left visual neglect (no hemianopia) are reported. He showed an associative priming in the neglected space: response to a word in the right visual field was faster when the word was preceded by the brief presentation of an associated word in the neglected field. When obliged to orient attention to the left side of a computer screen, he was not able to detect the presence of, to read aloud, or to judge the lexical status and semantic content of left-sided stimuli. This patient was able to perform a covert post-perceptual processing of the neglected stimuli, but could not do so when explicitly requested.     

Neural correlates of recognition memory for emotional faces and scenes

We examined the influence of emotional valence and type of item to be remembered on brain activity during recognition, using faces and scenes. We used multivariate analyses of event-related fMRI data to identify whole-brain patterns, or networks of activity. Participants demonstrated better recognition for scenes vs faces and for negative vs neutral and positive items. Activity was increased in extrastriate cortex and inferior frontal gyri for emotional scenes, relative to neutral scenes and all face types. Increased activity in these regions also was seen for negative faces relative to positive faces. Correct recognition of negative faces and scenes (hits vs correct rejections) was associated with increased activity in amygdala, hippocampus, extrastriate, frontal and parietal cortices. Activity specific to correctly recognized emotional faces, but not scenes, was found in sensorimotor areas and rostral prefrontal cortex. These results suggest that emotional valence and type of visual stimulus both modulate brain activity at recognition, and influence multiple networks mediating visual, memory and emotion processing. The contextual information in emotional scenes may facilitate memory via additional visual processing, whereas memory for emotional faces may rely more on cognitive control mediated by rostrolateral prefrontal regions.     

Neural correlates of conscious and unconscious vision in parietal extinction

Brain areas activated by stimuli in the left visual field of a right parietal patient suffering from left visual extinction were identified using event-related functional magnetic resonance imaging. Left visual field stimuli that were extinguished from awareness still activated the ventral visual cortex, including areas in the damaged right hemisphere. An extinguished face stimulus on the left produced robust category-specific activation of the right fusiform face area. On trials where the left visual stimulus was consciously seen rather than extinguished, greater activity was found in the ventral visual cortex of the damaged hemisphere, and also in frontal and parietal areas of the intact hemisphere. These findings extend recent observations on visual extinction, suggesting distinct neural correlates for conscious and unconscious perception.     

Neural Correlates of Conscious and Unconscious Vision in Parietal Extinction

Brain areas activated by stimuli in the left visual field of a right parietal patient suffering from left visual extinction were identified using event-related functional magnetic resonance imaging. Left visual field stimuli that were extinguished from awareness still activated the ventral visual cortex, including areas in the damaged right hemisphere. An extinguished face stimulus on the left produced robust category-specific activation of the right fusiform face area. On trials where the left visual stimulus was consciously seen rather than extinguished, greater activity was found in the ventral visual cortex of the damaged hemisphere, and also in frontal and parietal areas of the intact hemisphere. These findings extend recent observations on visual extinction, suggesting distinct neural correlates for conscious and unconscious perception.     

Neural response patterns in spider,blood-injection-injury and social fearful individuals: new insights from a simultaneous EEG/ECG–fMRI study

In the present simultaneous EEG/ECG-fMRI study we compared the temporal and spatial characteristics of the brain responses and the cardiac activity during fear picture processing between spider, blood-injection-injury (BII) and social fearful as well as healthy (non-fearful) volunteers. All participants were presented with two neutral and six fear-related blocks of pictures: two social, two spider and two blood/injection fear blocks. In a social fear block neutral images were occasionally interspersed with photographs of angry faces and social exposure scenes. In spider and blood/injection fear blocks neutral pictures were interspersed with spider fear-relevant and blood/injection pictures, respectively. When compared to healthy controls the social fear group responded with increased activations in the anterior orbital, middle/anterior cingulate and middle/superior temporal areas for pictures depicting angry faces and with a few elevated superior frontal activations for social exposure scenes. In the blood/injection fear group, heart rate was decreased and the activity in the middle/inferior frontal and visual processing regions was increased for blood/injection pictures. The HR decrease for blood/injection pictures correlated with increased frontal responses. In the spider fear group, spider fear-relevant pictures triggered increased activations within a broad subcortical and cortical neural fear network. The HR response for spider fear-relevant stimuli was increased and correlated with an increased insula and hippocampus activity. When compared to healthy controls, all fear groups showed higher LPP amplitudes for their feared cues and an overall greater P1 hypervigilance effect. Contrasts against the fear control groups showed that the increased responses for fear-specific stimuli are mostly related to specific fears and not to general anxiety proneness. The results suggest different engagement of cognitive evaluation and down-regulation strategies and an overall increased sensitization of the fear system in the three fear groups.