Frequency-specific gaze modulation of emotional face processing in the human amygdala.

Determining the social significance of emotional face expression is of major importance for adaptive behavior, and gaze direction provides critical information in this process. The amygdala is implicated in both emotion and gaze processing, but how and when it integrates expression and gaze cues remains unresolved. We tackled this question using intracranial electroencephalography in epileptic patients to assess both amygdala (n = 12) and orbitofrontal cortex (OFC; n = 11) time-frequency evoked responses to faces with different emotional expressions and different gaze directions. As predicted, self-relevant threat signals (averted fearful and directed angry faces) elicited stronger amygdala activity than self-irrelevant threat (directed fearful and averted angry faces). Fear effects started at early latencies in both amygdala and OFC (~110 and 160 ms, respectively), while gaze direction effects and their interaction with emotion occurred at later latencies. Critically, the amygdala showed differential gamma band increases to fearful averted gaze (starting ~550 ms) and to angry directed gaze (~470 ms). Moreover, when comparing the 2 self-relevant threat conditions among them, we found higher gamma amygdala activity for averted fearful faces and higher beta OFC activity for angry directed faces. Together, these results reveal for the first time frequency-specific effects of emotion and gaze on amygdala and OFC neural activity.

Prestimulus amygdala spectral activity is associated with visual face awareness.

Alpha cortical oscillations have been proposed to suppress sensory processing in the visual, auditory, and tactile domains, influencing conscious stimulus perception. However, it is unknown whether oscillatory neural activity in the amygdala, a subcortical structure involved in salience detection, has a similar impact on stimulus awareness. Recording intracranial electroencephalography (EEG) from 9 human amygdalae during face detection in a continuous flash suppression task, we found increased spectral prestimulus power and phase coherence, with most consistent effects in the alpha band, when faces were undetected relative to detected, similarly as previously observed in cortex with this task using scalp-EEG. Moreover, selective decreases in the alpha and gamma bands preceded face detection, with individual prestimulus alpha power correlating negatively with detection rate in patients. These findings reveal for the first time that prestimulus subcortical oscillations localized in human amygdala may contribute to perceptual gating mechanisms governing subsequent face detection and offer promising insights on the role of this structure in visual awareness.

Fear Spreading Across Senses: Visual Emotional Events Alter Cortical Responses to Touch, Audition, and Vision.

Attention and perception are potentiated for emotionally significant stimuli, promoting efficient reactivity and survival. But does such enhancement extend to stimuli simultaneously presented across different sensory modalities? We used functional magnetic resonance imaging in humans to examine the effects of visual emotional signals on concomitant sensory inputs in auditory, somatosensory, and visual modalities. First, we identified sensory areas responsive to task-irrelevant tones, touches, or flickers, presented bilaterally while participants attended to either a neutral or a fearful face. Then, we measured whether these responses were modulated by the emotional content of the face. Sensory responses in primary cortices were enhanced for auditory and tactile stimuli when these appeared with fearful faces, compared with neutral, but striate cortex responses to the visual stimuli were reduced in the left hemisphere, plausibly as a consequence of sensory competition. Finally, conjunction and functional connectivity analyses identified 2 distinct networks presumably responsible for these emotional modulatory processes, involving cingulate, insular, and orbitofrontal cortices for the increased sensory responses, and ventrolateral prefrontal cortex for the decreased sensory responses. These results suggest that emotion tunes the excitability of sensory systems across multiple modalities simultaneously, allowing the individual to adaptively process incoming inputs in a potentially threatening environment.

Amygdala function in emotion, cognition, and behavior.

The amygdala is a core structure in the anterior medial temporal lobe, with an important role in several brain functions involving memory, emotion, perception, social cognition, and even awareness. As a key brain structure for saliency detection, it triggers and controls widespread modulatory signals onto multiple areas of the brain, with a great impact on numerous aspects of adaptive behavior. Here we discuss the neural mechanisms underlying these functions, as established by animal and human research, including insights provided in both healthy and pathological conditions.

Brain reactivity to emotion persists in NREM sleep and is associated with individual dream recall.

The waking brain efficiently detects emotional signals to promote survival. However, emotion detection during sleep is poorly understood and may be influenced by individual sleep characteristics or neural reactivity. Notably, dream recall frequency has been associated with stimulus reactivity during sleep, with enhanced stimulus-driven responses in high vs. low recallers. Using electroencephalography (EEG), we characterized the neural responses of healthy individuals to emotional, neutral voices, and control stimuli, both during wakefulness and NREM sleep. Then, we tested how these responses varied with individual dream recall frequency. Event-related potentials (ERPs) differed for emotional vs. neutral voices, both in wakefulness and NREM. Likewise, EEG arousals (sleep perturbations) increased selectively after the emotional voices, indicating emotion reactivity. Interestingly, sleep ERP amplitude and arousals after emotional voices increased linearly with participants' dream recall frequency. Similar correlations with dream recall were observed for beta and sigma responses, but not for theta. In contrast, dream recall correlations were absent for neutral or control stimuli. Our results reveal that brain reactivity to affective salience is preserved during NREM and is selectively associated to individual memory for dreams. Our findings also suggest that emotion-specific reactivity during sleep, and not generalized alertness, may contribute to the encoding/retrieval of dreams.

Tuning the brain for novelty detection under emotional threat: the role of increasing gamma phase-synchronization.

Effective orienting of attention towards novel events is crucial for survival, particularly if they occur in a dangerous situation. This is why stimuli with emotional value are more efficient in capturing attention than neutral stimuli, and why the processing of unexpected novel stimuli is enhanced under a negative emotional context. Here we measured the phase-synchronization (PS) of gamma-band responses (GBR) from human EEG scalp-recordings during performance of a visual discrimination task in which task-irrelevant standard and novel sounds were presented in either a neutral or a negative emotional context, in order to elucidate the brain mechanisms by which emotion tunes the processing of novel events. Visual task performance was distracted by novel sounds, and this distraction was enhanced by the negative emotional context. Similarly, gamma PS was enhanced after novel as compared to standard sounds and it was also larger to auditory stimuli in the negative than in the neutral emotional context, reflecting the synchronization of neural networks for increasing of attentional processing. Remarkably, the larger PS increase of GBR after novel sounds in the negative as compared to the neutral emotional context over midline and right frontal regions reveals that a negative emotional context tunes novelty processing by means of the PS of brain activity in the gamma frequency band around 40 Hz in specific neural networks.

Emotional context enhances auditory novelty processing in superior temporal gyrus.

Visualizing emotionally loaded pictures intensifies peripheral reflexes toward sudden auditory stimuli, suggesting that the emotional context may potentiate responses elicited by novel events in the acoustic environment. However, psychophysiological results have reported that attentional resources available to sounds become depleted, as attention allocation to emotional pictures increases. These findings have raised the challenging question of whether an emotional context actually enhances or attenuates auditory novelty processing at a central level in the brain. To solve this issue, we used functional magnetic resonance imaging to first identify brain activations induced by novel sounds (NOV) when participants made a color decision on visual stimuli containing both negative (NEG) and neutral (NEU) facial expressions. We then measured modulation of these auditory responses by the emotional load of the task. Contrary to what was assumed, activation induced by NOV in superior temporal gyrus (STG) was enhanced when subjects responded to faces with a NEG emotional expression compared with NEU ones. Accordingly, NOV yielded stronger behavioral disruption on subjects' performance in the NEG context. These results demonstrate that the emotional context modulates the excitability of auditory and possibly multimodal novelty cerebral regions, enhancing acoustic novelty processing in a potentially harming environment.

Temporal dynamics of amygdala response to emotion- and action-relevance.

It has been proposed that the human amygdala may not only encode the emotional value of sensory events, but more generally mediate the appraisal of their relevance for the individual's goals, including relevance for action or task-based needs. However, emotional and non-emotional/action-relevance might drive amygdala activity through distinct neural signals, and the relative timing of both kinds of responses remains undetermined. Here, we recorded intracranial event-related potentials from nine amygdalae of patients undergoing epilepsy surgery, while they performed variants of a Go/NoGo task with faces and abstract shapes, where emotion- and action-relevance were orthogonally manipulated. Our results revealed early amygdala responses to emotion facial expressions starting ~ 130 ms after stimulus-onset. Importantly, the amygdala responded to action-relevance not only with face stimuli but also with abstract shapes (squares), and these relevance effects consistently occurred in later time-windows (starting ~ 220 ms) for both faces and squares. A similar dissociation was observed in gamma activity. Furthermore, whereas emotional responses habituated over time, the action-relevance effect increased during the course of the experiment, suggesting progressive learning based on the task needs. Our results support the hypothesis that the human amygdala mediates a broader relevance appraisal function, with the processing of emotion-relevance preceding temporally that of action-relevance.

Neurophysiological evidence for early modulation of amygdala activity by emotional reappraisal.

How emotions unfold through time in the brain, and how fast they can be regulated by voluntary control, remain unresolved. Psychological accounts of emotion regulation posit cognitive reappraisal mechanisms may alter early emotion generative processes directly, whereas suppression impacts only later processing stages, after emotion has arisen. However, to date, there is no neurophysiological data concerning the precise latency of emotion regulation effects on the amygdala, a major emotion processing relay in the brain. Here we record amygdala activity from six patients undergoing surgery for pharmaco-resistant epilepsy during both reappraisal and suppression. We find that emotion reappraisal strategy, but not suppression, modulates early neural responses to emotional scenes during an extended period of time, starting 130 ms post-stimulus onset. Further, reappraisal produced earlier impact on amygdala responses to positive compared to negative scenes. Our results provide the first neurophysiological support for theoretical accounts of emotion regulation that postulate an early modulation of emotion generative processes by reappraisal.

Human amygdala response to unisensory and multisensory emotion input: No evidence for superadditivity from intracranial recordings.

The amygdala is crucially implicated in processing emotional information from various sensory modalities. However, there is dearth of knowledge concerning the integration and relative time-course of its responses across different channels, i.e., for auditory, visual, and audiovisual input. Functional neuroimaging data in humans point to a possible role of this region in the multimodal integration of emotional signals, but direct evidence for anatomical and temporal overlap of unisensory and multisensory-evoked responses in amygdala is still lacking. We recorded event-related potentials (ERPs) and oscillatory activity from 9 amygdalae using intracranial electroencephalography (iEEG) in patients prior to epilepsy surgery, and compared electrophysiological responses to fearful, happy, or neutral stimuli presented either in voices alone, faces alone, or voices and faces simultaneously delivered. Results showed differential amygdala responses to fearful stimuli, in comparison to neutral, reaching significance 100-200 ms post-onset for auditory, visual and audiovisual stimuli. At later latencies, ∼400 ms post-onset, amygdala response to audiovisual information was also amplified in comparison to auditory or visual stimuli alone. Importantly, however, we found no evidence for either super- or subadditivity effects in any of the bimodal responses. These results suggest, first, that emotion processing in amygdala occurs at globally similar early stages of perceptual processing for auditory, visual, and audiovisual inputs; second, that overall larger responses to multisensory information occur at later stages only; and third, that the underlying mechanisms of this multisensory gain may reflect a purely additive response to concomitant visual and auditory inputs. Our findings provide novel insights on emotion processing across the sensory pathways, and their convergence within the limbic system.

Emotional context enhances auditory novelty processing: behavioural and electrophysiological evidence.

Viewing emotionally negative pictures has been proposed to attenuate brain responses towards sudden auditory events, as more attentional resources are allocated to the affective visual stimuli. However, peripheral reflexes have been shown intensified. These observations have raised the question of whether an emotional context actually facilitates or attenuates processing in the auditory novelty system. Using scalp event-related potentials we measured brain responses induced by novel sounds when participants responded to visual stimuli displaying either threatening or neutral sceneries. We then tested the modulatory effect of the emotional task conditions on auditory responses. Novel sounds yielded a stronger behavioural disruption on subjects' visual task performance when responding to negative pictures compared with when responding to the neutral ones. Accordingly, very early novelty-P3 responses to novel sounds were enhanced in negative context. These results provide strong evidence that the emotional context enhances the activation of neural networks in the auditory novelty system, gating acoustic novelty processing under potentially threatening conditions.

Negative emotional context enhances auditory novelty processing.

We used an auditory-visual distraction task to investigate the functional relationship between distraction elicited by auditory novel events and a context of negative emotional processing, both at behavioural and electrophysiological (event-related brain potentials) levels in humans. Participants performed a decision task on pictures disclosing sceneries with a task-irrelevant emotional load or neutral, whereas ignoring sounds presented concomitantly. Our data showed that novel sounds yielded stronger behavioural disruption on participants' visual task performance in negative context compared to the neutral one. Accordingly, late novelty P3 responses to novel sounds were enhanced. These results demonstrate that the negative emotional context enhances the activation of neural networks in the auditory novelty system, enhancing auditory novelty processing under potentially threatening conditions.

Phasic boosting of auditory perception by visual emotion.

Emotionally negative stimuli boost perceptual processes. There is little known, however, about the timing of this modulation. The present study aims at elucidating the phasic effects of, emotional processing on auditory processing within subsequent time-windows of visual emotional, processing in humans. We recorded the electroencephalogram (EEG) while participants responded to a, discrimination task of faces with neutral or fearful expressions. A brief complex tone, which subjects, were instructed to ignore, was displayed concomitantly, but with different asynchronies respective to, the image onset. Analyses of the N1 auditory event-related potential (ERP) revealed enhanced brain, responses in presence of fearful faces. Importantly, this effect occurred at picture-tone asynchronies of, 100 and 150ms, but not when these were displayed simultaneously, or at 50ms or 200ms asynchrony. These results confirm the existence of a fast-operating crossmodal effect of visual emotion on auditory, processing, suggesting a phasic variation according to the time-course of emotional processing.

Partial recovery of visual extinction by pavlovian conditioning in a patient with hemispatial neglect.

Patients with parietal lesions and unilateral spatial neglect (USN) are unable to detect or respond to information in the contralesional side of space. However, some residual sensory processing may still occur and overcome inattention symptoms when contralesional stimuli are perceptually or biologically salient, as shown for emotional faces or voices. These effects have been attributed to enhanced neural responses of sensory regions to emotional stimuli, presumably driven by feedback signals from limbic regions such as the amygdala. However, because emotional faces and voices also differ from neutral stimuli in terms of physical features, the affective nature of these effects still remains to be confirmed. Here we report data from a right parietal patient in whom left visual extinction was reduced for contralesional visual stimuli following pavlovian aversive conditioning, relative to the same stimulus before conditioning, and relative to similar but non-conditioned stimuli. This reduction of visual extinction was thus mediated by the emotional meaning of stimuli acquired through implicit learning. Functional magnetic resonance imaging also showed that conditioned visual stimuli elicited greater activation in right visual cortex, relative to the non-conditioned stimuli, together with differential activations in amygdala. These results support the hypothesis that emotional appraisal, not only the processing of perceptual features, may partly restore attention to salient information in contralesional space. These findings open new perspectives to improve rehabilitation strategies in neglect, based on affective and motivational signals.

The perception of dynamic and static facial expressions of happiness and disgust investigated by ERPs and fMRI constrained source analysis.

A recent functional magnetic resonance imaging (fMRI) study by our group demonstrated that dynamic emotional faces are more accurately recognized and evoked more widespread patterns of hemodynamic brain responses than static emotional faces. Based on this experimental design, the present study aimed at investigating the spatio-temporal processing of static and dynamic emotional facial expressions in 19 healthy women by means of multi-channel electroencephalography (EEG), event-related potentials (ERP) and fMRI-constrained regional source analyses. ERP analysis showed an increased amplitude of the LPP (late posterior positivity) over centro-parietal regions for static facial expressions of disgust compared to neutral faces. In addition, the LPP was more widespread and temporally prolonged for dynamic compared to static faces of disgust and happiness. fMRI constrained source analysis on static emotional face stimuli indicated the spatio-temporal modulation of predominantly posterior regional brain activation related to the visual processing stream for both emotional valences when compared to the neutral condition in the fusiform gyrus. The spatio-temporal processing of dynamic stimuli yielded enhanced source activity for emotional compared to neutral conditions in temporal (e.g., fusiform gyrus), and frontal regions (e.g., ventromedial prefrontal cortex, medial and inferior frontal cortex) in early and again in later time windows. The present data support the view that dynamic facial displays trigger more information reflected in complex neural networks, in particular because of their changing features potentially triggering sustained activation related to a continuing evaluation of those faces. A combined fMRI and EEG approach thus provides an advanced insight to the spatio-temporal characteristics of emotional face processing, by also revealing additional neural generators, not identifiable by the only use of an fMRI approach.

Emotional processing and its impact on unilateral neglect and extinction.

Unilateral spatial neglect is a neurological disorder characterized by impaired orienting of attention to stimuli located in the contralesional space, typically following right-hemisphere damage. Neuropsychological investigations in the past two decades have demonstrated that neglect is caused by deficits affecting a widespread cortico-subcortical fronto-parietal network controlling spatial attention, but usually sparing early sensory pathways. As a consequence, certain residual abilities in sensory processing remain intact and still take place for stimuli in the neglected space, such as the extraction and organization of coherent or meaningful object features. Moreover, these residual abilities can alleviate inattention symptoms when contralesional stimuli are perceptually or biologically salient. Here we review recent studies suggesting that the emotional content of stimuli may also be processed despite impaired attention towards contralesional space, and that such processing may act to enhance attention and partly reduce neglect for these stimuli, relative to similar but emotionally neutral stimuli. For example, faces with emotional expressions, voices with emotional prosody, as well as pictures of scenes or even spiders have been found to be less severely extinguished from awareness in conditions of bilateral stimulations, and/or lead to fewer omissions in search tasks with multiple distracters. Gaze cues and reward learning might also produce similar effects. Altogether, these findings suggest that emotionally significant information is not only extracted from stimuli at neglected locations through spared pathways, but can also induce emotional biases in attention that partly counteract the abnormal spatial biases caused by fronto-parietal damage. We discuss results from neuropsychology and neuroimaging research suggesting that specific mechanisms for emotional attention might exist, centered on the amygdala and other limbic regions, and that these mechanisms can operate partly independent from other circuits controlling spatial and object-based attention. Although we are only beginning to understand these interactive effects of emotion and attention and to identify their neuroanatomical substrates, we believe that a deeper knowledge of such mechanisms and their conditions of optimal operation will help develop or improve therapeutic strategies in neglect patients.

Phase re-setting of gamma neural oscillations during novelty processing in an appetitive context.

Based on the previous study where phase-synchronization (PS) of gamma-band responses (GBRs) proved a reliable cerebral correlate of involuntary attention and its enhancement under threat, we measured gamma-PS elicited by novel sounds from human electroencephalogram (EEG) scalp-recordings when participants responded to visual stimuli displaying either highly motivational or neutral sceneries. We then tested the modulatory effect of the emotional conditions on auditory responses. Novel distractor sounds did not affect behavioural accuracy on subjects' visual task performance in neutral context but markedly decreased hit rate in the appetitive one. Similarly, gamma-PS to novel sounds remained intact in neutral context, whereas it showed an increase, within the 35-Hz sub-range, in the appetitive context. These results suggest that a context of processing positive emotional stimuli results into an enhanced processing of task-irrelevant novel auditory events, and, furthermore, that gamma-PS is tuned under conditions that could promote long-term survival.

Dopamine transporter regulates the enhancement of novelty processing by a negative emotional context.

The dopaminergic (DA) system has been recently related the emotional modulation of cognitive processes. Moreover, patients with midbrain DA depletion, such as Parkinson's Disease (PD), have shown diminished reactivity during unpleasant events. Here, we examined the role of DA in the enhancement of novelty processing during negative emotion. Forty healthy volunteers were genotyped for the dopamine transporter (DAT) gene SLC6A3 or DAT1 and performed an auditory-visual distraction paradigm in negative and neutral emotional context conditions. 9R- individuals, associated to a lesser striatal DA display, failed to show increased distraction during negative emotion, but experienced an enhancement of the early phase of the novelty-P3 brain response, associated to the evaluation of novel events, in the negative relative to the neutral context. However, 9R+ individuals (associated to larger striatal DA display) showed larger distraction during negative emotion and larger amplitudes of the novelty-P3, irrespective of the condition. These results suggest a blunted reactivity to novelty during negative emotion in 9R- individuals due to a lesser DA display and stronger activation of the representation of novel events in the 9R+ group, due to a larger DA availability, thus reaching a ceiling effect in the neutral context condition with no further enhancement during negative emotion. The present results might help to understand the functional implications of dopamine in some neuropsychiatric disorders.

Electrophysiological and behavioral evidence of gender differences in the modulation of distraction by the emotional context.

Gender differences in brain activity while processing emotional stimuli have been demonstrated by neuroimaging and electrophysiological studies. However, the possible differential effects of emotion on attentional mechanisms between women and men are less understood. The present study aims to elucidate any gender differences in the modulation of unexpected auditory stimulus processing using an emotional context elicited by aversive images. Fourteen men and fourteen women performed a well-established auditory-visual distraction paradigm in which distraction was elicited by novel stimuli within a neutral or negative emotional context induced by images from the IAPS. Response time increased after unexpected novel sounds as a behavioral effect of distraction, and this increase was larger for women, but not for men, within the negative emotional context. Novelty-P3 was also modulated by the emotional context for women but not for men. These results reveal stronger novelty processing in women than in men during a threatening situation.