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.

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.

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.

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: 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.

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.

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.