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.
BackgroundAttention-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 FindingsWe 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/SignificanceOur 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.
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.
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.
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 actionrelevance 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. The amygdala is a crucial component of brain circuits allowing swift reaction to threatening stimuli, an ability critical for adaptive behavior and survival 1,2. Fast and efficient discrimination of potentially harmful events is a hallmark of the fear response, associated with a well-established sensitivity of the amygdala to threat information, and extensive connectivity with multiple other brain regions that act to facilitate attention, enhance memory, and promote actions 3. It has recently been questioned, however, whether the amygdala is dedicated to fear processing 1 or whether instead it may serve a broader function for the appraisal of behaviorally relevant events (see 4 for a review). There is abundant evidence that the human amygdala responds to other emotionally significant stimuli beyond threat 5 , including positive or reward information 6,7 , but also novelty 8 and non-emotional salient stimuli with personal impact or goal-related significance 9,10. This diversity of response patterns has led to recent theoretical accounts proposing that the amygdala may actually encode the "relevance" of events, which is determined by the goals,
Recent behavioral observations suggest an influence of prior expectancies on attention to neutral targets, while 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 reaction times or neural responses for spider targetseither in spider phobics or in non-spider-fearful controls. Our data support the idea of bottom-up enhancement of threat-related information through processing pathways unaffected by topdown 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.
BackgroundAdults 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 FindingsWe 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/SignificanceThis is the first report of euthymic BD exhibiting abnormal N170 emotional discrimination associated with theory of mind impairments.
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