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.

Behavioral correlates of temporal attention biases during emotional prosody perception.

Emotional prosody perception (EPP) unfolds in time given the intrinsic temporal nature of auditory stimuli, and has been shown to be modulated by spatial attention. Yet, the influence of temporal attention (TA) on EPP remains largely unexplored. TA studies manipulate subject's motor preparedness according to an upcoming event, with targets to discriminate during short attended trials arriving quickly, and, targets to discriminate during long unattended trials arriving at a later time point. We used here a classic paradigm manipulating TA to investigate its influence on behavioral responses to EPP (n = 100) and we found that TA bias was associated with slower reaction times (RT) for angry but not neutral prosodies and only during short trials. Importantly, TA biases were observed for accuracy measures only for angry voices and especially during short trials, suggesting that neutral stimuli are less subject to TA biases. Importantly, emotional facilitation, with faster RTs for angry voices in comparison to neutral voices, was observed when the stimuli were temporally attended and during short trials, suggesting an influential role of TA during EPP. Together, these results demonstrate for the first time the major influence of TA in RTs and behavioral performance while discriminating emotional prosody.

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.

Expectancies influence attention to neutral but not necessarily to threatening stimuli: An fMRI study.

Recent behavioral observations suggest an influence of prior expectancies on attention to neutral targets, whereas the detection of threatening targets remains comparably immune to these expectancies. The origin of this asymmetry, however, remains unclear. Here, therefore, we investigated its neural basis by using fMRI. Specifically, we tested whether, in accordance with the idea of a resetting attentional system during phylogenetic threat detection, neural responses for threatening compared with neutral targets would remain largely unaffected by prior expectancies. Alternatively, neural responses could reflect equally strong expectancy influences on both types of targets, with the respective patterns differing, thereby producing the asymmetric effect observed in behavior. Predictive cues in our study evoked specific behavioral and neural expectancy states and effectively modulated response latencies to detect neutral (bird) targets in a 3 × 3 visual search matrix: When threat-related (spider) rather than neutral targets were expected, bird detection was considerably slowed, and the neural response to expected birds differed from that to unexpected birds. Conversely, and in line with the hypothesis of a resetting attentional system for phylogenetic threat, expectancy cues had no impact on RTs or neural responses for spider targets-either in spider phobic participants or in non-spider-fearful control participants. Our data support the idea of bottom-up enhancement of threat-related information through processing pathways unaffected by top-down modulatory influences such as expectancy. These pathways may subserve rapid and comparably automatic responding to threat stimuli by safeguarding independence from more controlled and explicit expectancies, consequently promoting adaptive behavior and survival. (PsycINFO Database Record (c) 2019 APA, all rights reserved).

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.

Influence of Temporal Expectations on Response Priming by Subliminal Faces.

Unconscious processes are often assumed immune from attention influence. Recent behavioral studies suggest however that the processing of subliminal information can be influenced by temporal attention. To examine the neural mechanisms underlying these effects, we used a stringent masking paradigm together with fMRI to investigate how temporal attention modulates the processing of unseen (masked) faces. Participants performed a gender decision task on a visible neutral target face, preceded by a masked prime face that could vary in gender (same or different than target) and emotion expression (neutral or fearful). We manipulated temporal attention by instructing participants to expect targets to appear either early or late during the stimulus sequence. Orienting temporal attention to subliminal primes influenced response priming by masked faces, even when gender was incongruent. In addition, gender-congruent primes facilitated responses regardless of attention while gender-incongruent primes reduced accuracy when attended. Emotion produced no differential effects. At the neural level, incongruent and temporally unexpected primes increased brain response in regions of the fronto-parietal attention network, reflecting greater recruitment of executive control and reorienting processes. Congruent and expected primes produced higher activations in fusiform cortex, presumably reflecting facilitation of perceptual processing. These results indicate that temporal attention can influence subliminal processing of face features, and thus facilitate information integration according to task-relevance regardless of conscious awareness. They also suggest that task-congruent information between prime and target may facilitate response priming even when temporal attention is not selectively oriented to the prime onset time.

Expectancy influences on attention to threat are only weak and transient: Behavioral and physiological evidence.

Can prior expectancies shape attention to threat? To answer this question, we manipulated the expectancies of spider phobics and nonfearful controls regarding the appearance of spider and bird targets in a visual search task. We observed robust evidence for expectancy influences on attention to birds, reflected in error rates, reaction times, pupil diameter, and heart rate (HR). We found no solid effect, however, of the same expectancies on attention to spiders; only HR revealed a weak and transient impact of prior expectancies on the orientation of attention to threat. Moreover, these asymmetric effects for spiders versus birds were observed in both phobics and controls. Our results are thus consistent with the notion of a threat detection mechanism that is only partially permeable to current expectancies, thereby increasing chances of survival in situations that are mistakenly perceived as safe.

Varying expectancies and attention bias in phobic and non-phobic individuals.

Phobic individuals display an attention bias to phobia-related information and biased expectancies regarding the likelihood of being faced with such stimuli. Notably, although attention and expectancy biases are core features in phobia and anxiety disorders, these biases have mostly been investigated separately and their causal impact has not been examined. We hypothesized that these biases might be causally related. Spider phobic and low spider fearful control participants performed a visual search task in which they specified whether the deviant animal in a search array was a spider or a bird. Shorter reaction times (RTs) for spiders than for birds in this task reflect an attention bias toward spiders. Participants' expectancies regarding the likelihood of these animals being the deviant in the search array were manipulated by presenting verbal cues. Phobics were characterized by a pronounced and persistent attention bias toward spiders; controls displayed slower RTs for birds than for spiders only when spider cues had been presented. More important, we found RTs for spider detections to be virtually unaffected by the expectancy cues in both groups, whereas RTs for bird detections showed a clear influence of the cues. Our results speak to the possibility that evolution has formed attentional systems that are specific to the detection of phylogenetically salient stimuli such as threatening animals; these systems may not be as penetrable to variations in (experimentally induced) expectancies as those systems that are used for the detection of non-threatening stimuli. In sum, our findings highlight the relation between expectancies and attention engagement in general. However, expectancies may play a greater role in attention engagement in safe environments than in threatening environments.

Neural processing of emotional facial and semantic expressions in euthymic bipolar disorder (BD) and its association with theory of mind (ToM).

BACKGROUND: Adults with bipolar disorder (BD) have cognitive impairments that affect face processing and social cognition. However, it remains unknown whether these deficits in euthymic BD have impaired brain markers of emotional processing. METHODOLOGY/PRINCIPAL FINDINGS: We recruited twenty six participants, 13 controls subjects with an equal number of euthymic BD participants. We used an event-related potential (ERP) assessment of a dual valence task (DVT), in which faces (angry and happy), words (pleasant and unpleasant), and face-word simultaneous combinations are presented to test the effects of the stimulus type (face vs word) and valence (positive vs. negative). All participants received clinical, neuropsychological and social cognition evaluations. ERP analysis revealed that both groups showed N170 modulation of stimulus type effects (face > word). BD patients exhibited reduced and enhanced N170 to facial and semantic valence, respectively. The neural source estimation of N170 was a posterior section of the fusiform gyrus (FG), including the face fusiform area (FFA). Neural generators of N170 for faces (FG and FFA) were reduced in BD. In these patients, N170 modulation was associated with social cognition (theory of mind). CONCLUSIONS/SIGNIFICANCE: This is the first report of euthymic BD exhibiting abnormal N170 emotional discrimination associated with theory of mind impairments.

The neural basis of decision-making and reward processing in adults with euthymic bipolar disorder or attention-deficit/hyperactivity disorder (ADHD).

BACKGROUND: Attention-deficit/hyperactivity disorder (ADHD) and bipolar disorder (BD) share DSM-IV criteria in adults and cause problems in decision-making. Nevertheless, no previous report has assessed a decision-making task that includes the examination of the neural correlates of reward and gambling in adults with ADHD and those with BD. METHODOLOGY/PRINCIPAL FINDINGS: We used the Iowa gambling task (IGT), a task of rational decision-making under risk (RDMUR) and a rapid-decision gambling task (RDGT) which elicits behavioral measures as well as event-related potentials (ERPs: fERN and P3) in connection to the motivational impact of events. We did not observe between-group differences for decision-making under risk or ambiguity (RDMUR and IGT); however, there were significant differences for the ERP-assessed RDGT. Compared to controls, the ADHD group showed a pattern of impaired learning by feedback (fERN) and insensitivity to reward magnitude (P3). This ERP pattern (fERN and P3) was associated with impulsivity, hyperactivity, executive function and working memory. Compared to controls, the BD group showed fERN- and P3-enhanced responses to reward magnitude regardless of valence. This ERP pattern (fERN and P3) was associated with mood and inhibitory control. Consistent with the ERP findings, an analysis of source location revealed reduced responses of the cingulate cortex to the valence and magnitude of rewards in patients with ADHD and BD. CONCLUSIONS/SIGNIFICANCE: Our data suggest that neurophysiological (ERPs) paradigms such as the RDGT are well suited to assess subclinical decision-making processes in patients with ADHD and BD as well as for linking the cingulate cortex with action monitoring systems.

The cortical processing of facial emotional expression is associated with social cognition skills and executive functioning: a preliminary study.

Several lines of experimental evidence support an association between facial processing and social cognition, but no direct link between cortical markers of facial processing and complex cognitive processes has been reported until now. In the current study, we tested the hypothesis that cortical electrophysiological markers for the processing of facial emotion are associated with individual differences in executive and social cognition skills. We tested for correlations between the amplitude of event-related potentials (N170) in a dual valence task and participants' scores on three neuropsychological assessments (general neuropsychology, executive functioning, and social cognition). N170 was modulated by the stimulus type (face versus word) and the valence of faces (positive versus negative). The neural source of N170 was estimated to be the fusiform gyrus. Robust correlations were found between neuropsychological markers and measures of facial processing. Social cognition skills (as measured by three tests: the Reading the Mind in the Eyes test, the Faux Pas test, and the Iowa Gambling Task) correlated with cortical measures of emotional discrimination. Executive functioning ability also correlated with the cortical discrimination of complex emotional stimuli. Our findings suggest that the cortical processing of facial emotional expression is associated with social cognition skills.

Cortical deficits of emotional face processing in adults with ADHD: its relation to social cognition and executive function.

Although it has been shown that adults with attention-deficit hyperactivity disorder (ADHD) have impaired social cognition, no previous study has reported the brain correlates of face valence processing. This study looked for behavioral, neuropsychological, and electrophysiological markers of emotion processing for faces (N170) in adult ADHD compared to controls matched by age, gender, educational level, and handedness. We designed an event-related potential (ERP) study based on a dual valence task (DVT), in which faces and words were presented to test the effects of stimulus type (faces, words, or face-word stimuli) and valence (positive versus negative). Individual signatures of cognitive functioning in participants with ADHD and controls were assessed with a comprehensive neuropsychological evaluation, including executive functioning (EF) and theory of mind (ToM). Compared to controls, the adult ADHD group showed deficits in N170 emotion modulation for facial stimuli. These N170 impairments were observed in the absence of any deficit in facial structural processing, suggesting a specific ADHD impairment in early facial emotion modulation. The cortical current density mapping of N170 yielded a main neural source of N170 at posterior section of fusiform gyrus (maximum at left hemisphere for words and right hemisphere for faces and simultaneous stimuli). Neural generators of N170 (fusiform gyrus) were reduced in ADHD. In those patients, N170 emotion processing was associated with performance on an emotional inference ToM task, and N170 from simultaneous stimuli was associated with EF, especially working memory. This is the first report to reveal an adult ADHD-specific impairment in the cortical modulation of emotion for faces and an association between N170 cortical measures and ToM and EF.

Does the PFC model of analogy account for decision making, problem solving, reasoning, flexibility, adaptability, and even creativity?

Abstract From everyday cognition to scientific discovery, analogical processes play an important role: bringing connection, integration, and interrelation of information. Recently, a PFC model of analogy has been proposed to explain many cognitive processes and integrate general functional properties of PFC. We argue here that analogical processes do not suffice to explain the cognitive processes and functions of PFC. Moreover the model does not satisfactorily integrate specific explanatory mechanisms required for the different processes involved. Its relevance would be improved if fewer cognitive phenomena were considered and more specific predictions and explanations about those processes were stated.