Context influences early perceptual analysis of faces--an electrophysiological study

Electrophysiological and hemodynamic correlates of processing isolated faces have been investigated extensively over the last decade. A question not addressed thus far is whether the visual scene, which normally surrounds a face or a facial expression, has an influence on how the face is processed. Here we investigated this issue by presenting faces in natural contexts and measuring whether the emotional content of the scene influences processing of a facial expression. Event-related potentials were recorded to faces (fearful/neutral) embedded in scene contexts (fearful/neutral) while participants performed an orientation-decision task (face upright or inverted). Two additional experiments were run, one to examine the effects of context that occur without a face and the other to evaluate the effects of faces isolated from contexts. Faces without any context showed the largest N170 amplitudes. The presence of a face in a fearful context enhances the N170 amplitude over a face in neutral contexts, an effect that is strongest for fearful faces on left occipito-temporal sites. This N170 effect, and the corresponding topographic distribution, was not found for contexts-only, indicating that the increased N170 amplitude results from the combination of face and fearful context. These findings suggest that the context in which a face appears may influence how it is encoded.     

Unintentional temporal context-based prediction of emotional faces: an electrophysiological study

The ability to extract sequential regularities embedded in the temporal context or temporal structure of sensory events and to predict upcoming events based on the extracted sequential regularities plays a central role in human cognition. In the present study, we demonstrate that, without any intention, upcoming emotional faces can be predicted based on sequential regularities, by showing that prediction error responses as reflected by visual mismatch negativity (MMN), an event-related brain potential (ERP) component, were evoked in response to emotional faces that violated a regular alternation pattern of 2 emotional faces (fearful and happy faces) under a situation where the emotional faces themselves were unrelated to the participant's task. Face-inversion and negative-bias effects in the visual MMN further indicated the involvement of holistic face representations. In addition, through successive source analyses of the visual MMN, it was revealed that the prediction error responses were composed of activations mainly in the face-responsible visual extrastriate areas and the prefrontal areas. The present results provide primary evidence for the existence of the unintentional temporal context-based prediction of biologically relevant visual stimuli as well as empirical support for the major engagement of the visual and prefrontal areas in unintentional temporal context-based prediction in vision.     

Rapid processing of emotional expressions without conscious awareness

Rapid accurate categorization of the emotional state of our peers is of critical importance and as such many have proposed that facial expressions of emotion can be processed without conscious awareness. Typically, studies focus selectively on fearful expressions due to their evolutionary significance, leaving the subliminal processing of other facial expressions largely unexplored. Here, I investigated the time course of processing of 3 facial expressions (fearful, disgusted, and happy) plus an emotionally neutral face, during objectively unaware and aware perception. Participants completed the challenging "which expression?" task in response to briefly presented backward-masked expressive faces. Although participant's behavioral responses did not differentiate between the emotional content of the stimuli in the unaware condition, activity over frontal and occipitotemporal (OT) brain regions indicated an emotional modulation of the neuronal response. Over frontal regions this was driven by negative facial expressions and was present on all emotional trials independent of later categorization. Whereas the N170 component, recorded on lateral OT electrodes, was enhanced for all facial expressions but only on trials that would later be categorized as emotional. The results indicate that emotional faces, not only fearful, are processed without conscious awareness at an early stage and highlight the critical importance of considering categorization response when studying subliminal perception.     

Target visibility and visual awareness modulate amygdala responses to fearful faces

The goals of the present study were twofold. First, we wished to investigate the neural correlates of aware and unaware emotional face perception after characterizing each subject's behavioral performance via signal detection theory methods. Second, we wished to investigate the extent to which amygdala responses to fearful faces depend on the physical characteristics of the stimulus independently of the percept. We show that amygdala responses depend on visual awareness. Under conditions in which subjects were not aware of fearful faces flashed for 33 ms, no differential activation was observed in the amygdala. On the other hand, differential activation was observed for 67 ms fearful targets that the subjects could reliably detect. When trials were divided into hits, misses, correct rejects, and false alarms, we show that target visibility is an important factor in determining amygdala responses to fearful faces. Taken together, our results further challenge the view that amygdala responses occur automatically.     

Unilateral amygdala lesions hamper attentional orienting triggered by gaze direction

The newly discovered deficit in a bilateral amygdala-damaged case, of not being able to allocate attention to the critical feature of a face (Adolphs R, Gosselin F, Buchanan TW, Tranel D, Schyns P, Damasio AR. 2005. A mechanism for impaired fear recognition after amygdala damage. Nature. 433:68--72.), has opened a new window into the function of the amygdala. This case implies that the amygdala might be essential in detecting potentially relevant social stimuli, and directing attention accordingly. In this study, we have sought to test this implication by investigating the behavioral performance of 5 unilateral amygdala-damaged subjects on spatial cueing tasks. The tasks employed central gaze and arrow direction as cues to trigger attentional orienting in peripheral target detection. Although age-matched normal controls demonstrated a significant congruency effect such that targets presented congruently to cue direction elicited faster detection, amygdala subjects demonstrated no such congruency effect for gaze cues in the face of a significant congruency effect for arrow cues. The results suggest that the social valence of a stimulus is critical for amygdala involvement in visual processing. The results also support the implicated role of the amygdala in detecting and analyzing relevant social stimuli, and orienting attention accordingly.     

Enhanced processing of threat stimuli under limited attentional resources

The ability to process stimuli that convey potential threat, under conditions of limited attentional resources, confers adaptive advantages. This study examined the neurobiology underpinnings of this capacity. Employing an attentional blink paradigm, in conjunction with functional magnetic resonance imaging, we manipulated the salience of the second of 2 face target stimuli (T2), by varying emotionality. Behaviorally, fearful T2 faces were identified significantly more than neutral faces. Activity in fusiform face area increased with correct identification of T2 faces. Enhanced activity in rostral anterior cingulate cortex (rACC) accounted for the benefit in detection of fearful stimuli reflected in a significant interaction between target valence and correct identification. Thus, under conditions of limited attention resources activation in rACC correlated with enhanced processing of emotional stimuli. We suggest that these data support a model in which a prefrontal "gate" mechanism controls conscious access of emotional information under conditions of limited attentional resources.     

Dynamic perception of facial affect and identity in the human brain

Functional magnetic resonance imaging (fMRI) was used to compare brain activation to static facial displays versus dynamic changes in facial identity or emotional expression. Static images depicted prototypical fearful, angry and neutral expressions. Identity morphs depicted identity changes from one person to another, always with neutral expressions. Emotion morphs depicted expression changes from neutral to fear or anger, creating the illusion that the actor was 'getting scared' or 'getting angry' in real-time. Brain regions implicated in processing facial affect, including the amygdala and fusiform gyrus, showed greater responses to dynamic versus static emotional expressions, especially for fear. Identity morphs activated a dorsal fronto-cingulo-parietal circuit and additional ventral areas, including the amygdala, that also responded to the emotion morphs. Activity in the superior temporal sulcus discriminated emotion morphs from identity morphs, extending its known role in processing biologically relevant motion. The results highlight the importance of temporal cues in the neural coding of facial displays.     

Cognitive response profile of the human fusiform face area as determined by MEG

Activation in or near the fusiform gyrus was estimated to faces and control stimuli. Activation peaked at 165 ms and was strongest to digitized photographs of human faces, regardless of whether they were presented in color or grayscale, suggesting that face- and color-specific areas are functionally separate. Schematic sketche evoked approximately 30% less activation than did face photographs. Scrambling the locations of facial features reduced the response by approximately 25% in either hemisphere, suggesting that configurational versus analytic processing is not lateralized at this latency. Animal faces evoked approximately 50% less activity, and common objects, animal bodies or sensory controls evoked approximately 80% less activity than human faces. The (small) responses evoked by meaningless control images were stronger when they included surfaces and shading, suggesting that the fusiform gyrus may use these features in constructing its face-specific response. Putative fusiform activation was not significantly related to stimulus repetition, gender or emotional expression. A midline occipital source significantly distinguished between faces and control images as early as 110 ms, but was more sensitive to sensory qualities. This source significantly distinguished happy and sad faces from those with neutral expressions. We conclude that the fusiform gyrus may selectively encode faces at 165 ms, transforming sensory input for further processing.     

Cognitive coping style modulates neural responses to emotional faces in healthy humans: a 3-T FMRI study

Repression designates coping strategies that aim to shield the organism from distressing stimuli by disregarding their aversive characteristics. In contrast, sensitization comprises coping strategies that are employed to reduce situational uncertainty such as analyzing the environment. Functional magnetic resonance imaging was used to study neural correlates of coping styles during the perception of threatening and nonthreatening socially relevant information. Pictures of human faces bearing fearful (ambiguously threatening), angry (unambiguously threatening), happy (nonthreatening), and neutral expressions were presented masked and unmasked. Two groups of subjects were examined who were defined as consistent repressors versus consistent sensitizers with the Mainz Coping Inventory. Sensitizers tended to exhibit stronger neural responses in the amygdala to unmasked fearful faces compared with repressors. Overall, repressors were cortically more responsive to fearful (ambiguously threatening) and happy (nonthreatening) facial expressions than sensitizers, whereas sensitizers presented an enhanced responsivity to angry faces in several prefrontal areas, that is, unambiguously threatening expressions. Results from time series analyses suggest that sensitizers could exhibit less top-down cortical regulation of the amygdala than repressors in the processing of fearful faces. An increased responsivity of the amygdala to ambiguously threatening stimuli may represent a biological determinant of sensitizers' feelings of uncertainty.     

Electrophysiological evidence for temporal dissociation between spatial attention and sensory competition during human face processing

Scalp event-related potential (ERP) studies in humans indicate that face processes taking place between 130 and 170 ms after stimulus onset at posterior sites (N170) are strongly reduced when another face stimulus is processed concurrently or has been presented shortly before for a prolonged period. These observations suggest that neural representations of individual faces compete in the occipitotemporal cortex as early as 130 ms. Here, we tested the respective role of spatial attention and sensory competition in accounting for the amplitude reduction of the N170 during concurrent face stimulation. ERPs time locked to a lateralized face stimulus were recorded while subjects were fixating either a face or a controlled scrambled-face stimulus (context factor) and were engaged in either a high- or a low-attentional load task at fixation (task factor). The N170 amplitude to the lateralized face stimulus was reduced both when the central stimulus was a face compared with a scrambled face and when the attentional load at fixation was high. However, these effects of context and task factors were largely additive. Most importantly, spatial attention modulated visual processes as early as 80 ms after stimulus onset, whereas sensory competition effects started at about 130 ms. These results provide strong evidence that the N170 in response to faces is modulated by spatial attention, and also that spatial attention and sensory competition do not reflect the same mechanisms of early selection of visual information in the extrastriate cortex.     

Stimulation modalities in the study of visual evoked potentials

An evoked potentials (EPs) is an electrical manifestation of the brain's reception of and response to an external stimulus. The classification of visual evoked potentials (VEPs) depend primarily on stimulus characteristics. The visual content of a stimulus can be divided into two types: patterned and diffuse. VEPs to patterned stimuli are due mainly to the density of light and dark contrast borders; VEPs to diffuse light flashes are due to change in luminance only. Transitions between light and dark pattern elements have sharp borders in checkerboard patterns and in bar gratings. Those transitions can be represented by a spatial square wave. In sine wave gratings the change of luminance between light and dark stripes is gradual. The visual angle describes the size of the image of one light or dark element. The spatial frequency equals the number of repetitions of one light plus one dark element.     

Rapid face-selective adaptation of an early extrastriate component in MEG

Adaptation paradigms are becoming increasingly popular for characterizing visual areas in neuroimaging, but the relation of these results to perception is unclear. Neurophysiological studies have generally reported effects of stimulus repetition starting at 250-300 ms after stimulus onset, well beyond the latencies of components associated with perception (100-200 ms). Here we demonstrate adaptation for earlier evoked components when 2 stimuli (S1 and S2) are presented in close succession. Using magnetoencephalography, we examined the M170, a "face-selective" response at 170 ms after stimulus onset that shows a larger response to faces than to other stimuli. Adaptation of the M170 occurred only when stimuli were presented with relatively short stimulus onset asynchronies (< 800 ms) and was larger for faces preceded by faces than by houses. This face-selective adaptation is not merely low-level habituation to physical stimulus attributes, as photographic, line-drawing, and 2-tone face images produced similar levels of adaptation. Nor does it depend on the amplitude of the S1 response: adaptation remained greater for faces than houses even when the amplitude of the S1 face response was reduced by visual noise. These results indicate that rapid adaptation of early, short-latency responses not only exists but also can be category selective.     

Time-locked brain activity associated with emotion: a pilot MEG study

Objective: To examine the time course of brain activation in response to emotionally evocative pictures.

Methods and procedures: Regions of the brain involved in the processing of affective stimuli in response to picture sets rated unpleasant, pleasant and affectively neutral, as well as the order of activation of each region, were investigated using magnetoencephalography in 10 normal adult volunteers.

Results: Spatiotemporal maps were found consisting of two basic components. The first involving activation in the occipital and basal aspects of the temporal cortex- lasted, on average, 270 ms post-stimulus. The second component involving activation in the mesial temporal lobes (MTL) extended from 270 to 850 ms post-stimulus. After (serial) activating the mesial temporal lobe structures or simultaneous (parallel) to it, activation is also observed in the frontal structures.

Conclusions: The temporal organization in the brain of an emotional stimulus requires the serial and alternating engagement of frontal and posterior cortices. It is suggested that lesions to the brain may disrupt this temporal course, altering the emotional response commonly observed in patients with brain injury.     

Spatio temporal dynamics of face recognition

To better understand face recognition, it is necessary to identify not only which brain structures are implicated but also the dynamics of the neuronal activity in these structures. Latencies can then be compared to unravel the temporal dynamics of information processing at the distributed network level. To achieve high spatial and temporal resolution, we used intracerebral recordings in epileptic subjects while they performed a famous/unfamiliar face recognition task. The first components peaked at 110 ms in the fusiform gyrus (FG) and simultaneously in the inferior frontal gyrus, suggesting the early establishment of a large-scale network. This was followed by components peaking at 160 ms in 2 areas along the FG. Important stages of distributed parallel processes ensued at 240 and 360 ms involving up to 6 regions along the ventral visual pathway. The final components peaked at 480 ms in the hippocampus. These stages largely overlapped. Importantly, event-related potentials to famous faces differed from unfamiliar faces and control stimuli in all medial temporal lobe structures. The network was bilateral but more right sided. Thus, recognition of famous faces takes place through the establishment of a complex set of local and distributed processes that interact dynamically and may be an emergent property of these interactions.     

The noradrenergic alpha2 agonist clonidine modulates behavioural and neuroanatomical correlates of human attentional orienting and alerting

We examined whether the known noradrenergic attenuation of the alerting effect (the beneficial effect of a warning cue) results from an underlying effect of noradrenaline on temporal orienting (orienting toward a particular moment in time). Following a within-subjects, counterbalanced design, 10 healthy human volunteers received placebo, 200 microg clonidine or 1 mg guanfacine (alpha2 agonists) in three separate testing sessions. Subjects were scanned by fMRI while performing attentional orienting tasks containing spatially informative, temporally informative, non-informative or no cues. The alerting effect primarily activated left-lateralized prefrontal, premotor and parietal regions. Clonidine, but not guanfacine, impaired behavioural measures of the alerting effect while attenuating activity in the left temporo-parietal junction. Replicating previous results, the temporal orienting task activated left parietal and frontal cortex, while parietal cortex was activated bilaterally during spatial orienting. Of these networks, clonidine, but not guanfacine, attenuated left prefrontal cortex and insula activity during temporal orienting and attenuated right superior parietal cortex activity during spatial orienting,. To complement these neuroanatomical changes, clonidine produced selective behavioural effects on both temporal and spatial orienting. The anatomical dissociation between the effects of clonidine during temporal orienting versus alerting suggests that noradrenergic modulation of the alerting effect does not result only from an underlying effect on temporal orienting. Furthermore, we have demonstrated lateralized neuroanatomical substrates for the noradrenergic modulation of human attentional orienting in the spatial and temporal domains.     

Unconscious Fearful Priming Followed by a Psychosocial Stress Test Results in Higher Cortisol Levels

Human perception of stress includes an automatic pathway that processes subliminal presented stimuli below the threshold of conscious awareness. Subliminal stimuli can therefore activate the physiologic stress system. Unconscious emotional signals were shown to significantly moderate reactions and responses to subsequent stimuli, an effect called ‘priming’. We hypothesized that subliminal presentation of a fearful signal during the Stroop task compared with an emotionally neutral one will prime stress reactivity in a subsequently applied psychosocial stress task, thereby yielding a significant increase in salivary cortisol. Half of 36 participants were repeatedly presented either a fearful face or a neutral one. After this, all underwent a psychosocial stress task. The fearful group showed a significant increase in cortisol levels (p = 0.022). This change was not affected by sex, age and body mass index, and it also did not change when taking resting cortisol levels into account. Post‐hoc analyses showed that the increase in cortisol in the fearful group started immediately after the psychosocial stress test. Hence, subliminal exposure to a fearful signal in combination with the Stroop and followed by a psychosocial stress test leads to an increase in stress reactivity. Copyright © 2012 John Wiley & Sons, Ltd.     

Monetary incentives enhance processing in brain regions mediating top-down control of attention

To evaluate the effect of an abstract motivational incentive on top-down mechanisms of visual spatial attention, 10 subjects engaged in a target detection task and responded to targets preceded by spatially valid (predictive), invalid (misleading) or neutral central cues under three different incentive conditions: win money (WIN), lose money (LOSE), and neutral (neither gain nor lose). Activation in the posterior cingulate cortex was correlated with visual spatial expectancy, defined as the degree to which the valid cue benefited performance as evidenced by faster reaction times compared to non-directional cues. Winning and losing money enhanced this relationship via overlapping but independent limbic mechanisms. In addition, activity in the inferior parietal lobule was correlated with disengagement (the degree to which invalid cues diminished performance). This relationship was also enhanced by monetary incentives. Finally, incentive enhanced the relationship of activation in the visual cortex to visual spatial expectancy and disengagement for both types of incentive (WIN and LOSE). These results show that abstract incentives enhance neural processing within the attention network in a process- and valence-selective manner. They also show that different cognitive and motivational mechanisms may produce a common effect upon unimodal cortices in order to enhance processing to serve the current behavioral goal.     

Dorsal posterior parietal rTMS affects voluntary orienting of visuospatial attention

Patients with lesions in posterior parietal cortex (PPC) are relatively unimpaired in voluntarily directing visual attention to different spatial locations, while many neuroimaging studies in healthy subjects suggest dorsal PPC involvement in this function. We used an offline repetitive transcranial magnetic stimulation (rTMS) protocol to study this issue further. Ten healthy participants performed a cue-target paradigm. Cues prompted covert orienting of spatial attention under voluntary control to either a left or right visual field position. Targets were flashed subsequently at the cued or uncued location, or bilaterally. Following rTMS over right dorsal PPC, (i) the benefit for target detection at cued versus uncued positions was preserved irrespective of cueing direction (left- or rightward), but (ii) leftward cueing was associated with a global impairment in target detection, at all target locations. This reveals that leftward orienting was still possible after right dorsal PPC stimulation, albeit at an increased overall cost for target detection. In addition, rTMS (iii) impaired left, but (iv) enhanced right target detection after rightward cueing. The finding of a global drop in target detection during leftward orienting with a spared, relative detection benefit at the cued (left) location (i-ii) suggests that right dorsal PPC plays a subsidiary rather than pivotal role in voluntary spatial orienting. This finding reconciles seemingly conflicting results from patients and neuroimaging studies. The finding of attentional inhibition and enhancement occurring contra- and ipsilaterally to the stimulation site (iii-iv) supports the view that spatial attention bias can be selectively modulated through rTMS, which has proven useful to transiently reduce visual hemispatial neglect.     

Mechanisms of action of midazolam on expression of contextual fear in rats

Background. Midazolam may suppress conditioned fear after anaversive event by disrupting the memory trace formed duringconditioning, by altering the emotional part of the aversiveevent, or by the combination of both effects. The purpose ofthe present study was to determine whether affective-relatedprocesses contribute to the amnesic-like effects of midazolamon aversive events. Methods. The effects of acute administration of low doses ofmidazolam (0.37–3 mg kg^–1) on fear conditioning(association between a neutral context and an aversive stimulus)and on innate anxiety in fearful surroundings were examinedin rats. The effect of midazolam on the deleterious consequencesof pre-exposure to the context (a non-aversive event) for subsequentfear conditioning was then compared with its effect on fearconditioning. The role of midazolam as an affective contextwas assessed by performing the testing phase under midazolam.Possible locomotor impairment or long-term effects of midazolamwere controlled in additional experiments. Results. Midazolam reduced both contextual fear conditioningand spontaneous fear. The deleterious effect of midazolam onpre-exposure to the context was of the same magnitude as itseffect on the acquisition phase of fear conditioning. The effectsof midazolam on both pre-exposure to the context and fear conditioningwere unchanged when rats received a second injection of midazolambefore the retention phase. Conclusions. Low doses of midazolam that do not impair locomotionsuppress conditioned fear to the context by acting on memoryprocesses rather than on affective or anxiolytic processes. Br J Anaesth 2002; 89: 614–21     

Attentional modulation of object representations in working memory

We investigated the role of object-based attention in modulating the maintenance of faces and scenes held online in working memory (WM). Participants had to remember a face and a scene, while cues presented during the delay instructed them to orient their attention to one or the other item. Event-related functional magnetic resonance imaging revealed that orienting attention in WM modulated the activity in fusiform and parahippocampal gyri, involved in maintaining representations of faces and scenes respectively. Measures from complementary behavioral studies indicated that this increase in activity corresponded to improved WM performance. The results show that directed attention can modulate maintenance of specific representations in WM, and help define the interplay between the domains of attention and WM.