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Biomedical subjects

Luiz Pessoa

Publications and source records attributed to Luiz Pessoa.

At least 19 recordsLinked to original sources

Reducing state anxiety with alpha-frequency transcranial alternating current stimulation.

BACKGROUND: Anxiety reactivity to acute stress is a transdiagnostic vulnerability factor. We tested whether a single session of alpha-frequency transcranial alternating current stimulation (tACS) targeting the frontoparietal control network reduces stress-evoked state anxiety in healthy adults. METHODS: In a randomized, blinded, sham-controlled study, 42 participants (mean age 58.9 years) completed an acute stress task before and after stimulation. The task was an adapted moving-circles paradigm in which circle collisions triggered a brief aversive event (mild electric shock plus unpleasant noise and a white flash). Active stimulation consisted of 20 min of 10-Hz tACS (2.0 mA/channel; 30-s ramp up/down) delivered via electrodes at F3, P3, Cz, and T7 (0° phase at F3/P3; 180° at Cz/T7). Sham stimulation used the same montage and ramp periods but no sustained current. RESULTS: State anxiety showed a significant Time × Protocol interaction (F(1,35) = 4.22, p = .047): STAI-S decreased after active tACS (Δ = -3.16) but increased slightly after sham (Δ = +1.17). Perceived stress appraisal (SAAS) did not change. Resting-state alpha power at F3/P3 showed no reliable pre-post effects. During the task, left-frontal relative alpha differed by protocol and showed a trend toward larger increases following active tACS. Electrodermal and pupil indices changed across sessions in both groups, with no differential stimulation effects. CONCLUSIONS: A single alpha-tACS session produced a modest, selective reduction in stress-evoked state anxiety, supporting oscillatory neuromodulation as a scalable approach to dampen anxiety reactivity.

Humans↗

Decoding near-threshold perception of fear from distributed single-trial brain activation.

Instead of contrasting functional magnetic resonance imaging (fMRI) signals associated with 2 conditions, as customarily done in neuroimaging, we reversed the direction of analysis and probed whether brain signals could be used to "predict" perceptual states. We probed the neural correlates of perceptual decisions by "decoding" brain states during near-threshold fear detection. Decoding was attempted by using support vector machines and other related techniques. Although previous decoding studies have employed relatively "blocked" data, our objective was to probe how the "moment-to-moment" fluctuation in fMRI signals across a population of voxels reflected the participant's perceptual decision. Accuracy increased from when 1 region was considered (approximately 64%) to when 10 regions were used (approximately 78%). When the best classifications per subject were averaged, accuracy levels ranged between 74% and 86% correct. An information theoretic analysis revealed that the information carried by pairs of regions reliably exceeded the sum of the information carried by individual regions, suggesting that information was combined "synergistically" across regions. Our results indicate that the representation of behavioral choice is "distributed" across several brain regions. Such distributed encoding may help prepare the organism to appropriately handle emotional stimuli and regulate the associated emotional response upon the conscious decision that a fearful face is present. In addition, the results show that challenging brain states can be decoded with high accuracy even when "single-trial" data are employed and suggest that multivariate analysis strategies have considerable potential in helping to elucidate the neural correlates of visual awareness and the encoding of perceptual decisions.

Adult↗

Sustained and transient modulation of performance induced by emotional picture viewing.

We investigated how viewing task-irrelevant emotional pictures affects the performance of a subsequent nonemotional visual detection task. Subjects performed target-detection trials following the offset of individual unpleasant, pleasant, and neutral pictures. Sustained interference occurred when subjects viewed unpleasant pictures (mutilated bodies) in a sequential, "blocked" fashion. Such slowing down of reaction time appeared to build up with time, consistent with the instatement of a defensive emotional state. With a randomized picture presentation, only a transient interference effect was observed, consistent with increased attentional demands during the processing of unpleasant pictures. During blocked presentation of affiliative pleasant pictures, reaction times were faster, suggesting the activation of appetitive motivational systems. Ultimately, both attentional and motivational systems are intricately tied in the brain and, together, determine behavior.

Adolescent↗

Fate of unattended fearful faces in the amygdala is determined by both attentional resources and cognitive modulation.

The evidence for amygdala processing of emotional items outside the focus of attention is mixed. We hypothesized that differences in attentional demands may, at least in part, explain prior discrepancies. In the present study, attention was manipulated by parametrically varying the difficulty of a central task, allowing us to compare responses evoked by unattended emotion-laden faces while the attentional load of a central task was varied. Reduced responses to unattended emotional stimuli may also reflect an active suppression of amygdala responses during difficult non-emotional tasks (cognitive modulation). To explicitly assess cognitive modulation, an experimental condition was used in which subjects performed the central task without the presence of irrelevant emotional stimuli. Our findings revealed that amygdala responses were modulated by the focus of attention. Stronger responses were evoked during a sex task (when faces were attended) relative to a bar-orientation task (when faces were unattended). Critically, a valence effect was observed in the right amygdala during low attentional demand conditions, but not during medium or high demand conditions. Moreover, performing a difficult non-emotional task alone was associated with signal decreases in a network of brain regions, including the amygdala. Such robust decreases demonstrate that cognitive modulation comprises a powerful factor in determining amygdala responses. Collectively, our findings reveal that both attentional resources and cognitive modulation govern the fate of unattended fearful faces in the amygdala.

Adult↗

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.

Adaptation, Physiological↗

Quantitative prediction of perceptual decisions during near-threshold fear detection.

A fundamental goal of cognitive neuroscience is to explain how mental decisions originate from basic neural mechanisms. The goal of the present study was to investigate the neural correlates of perceptual decisions in the context of emotional perception. To probe this question, we investigated how fluctuations in functional MRI (fMRI) signals were correlated with behavioral choice during a near-threshold fear detection task. fMRI signals predicted behavioral choice independently of stimulus properties and task accuracy in a network of brain regions linked to emotional processing: posterior cingulate cortex, medial prefrontal cortex, right inferior frontal gyrus, and left insula. We quantified the link between fMRI signals and behavioral choice in a whole-brain analysis by determining choice probabilities by means of signal-detection theory methods. Our results demonstrate that voxel-wise fMRI signals can reliably predict behavioral choice in a quantitative fashion (choice probabilities ranged from 0.63 to 0.78) at levels comparable to neuronal data. We suggest that the conscious decision that a fearful face has been seen is represented across a network of interconnected brain regions that prepare the organism to appropriately handle emotionally challenging stimuli and that regulate the associated emotional response.

Amygdala↗

To what extent are emotional visual stimuli processed without attention and awareness?

In the past few years, important contributions have been made to the study of emotional visual perception. Researchers have reported responses to emotional stimuli in the human amygdala under some unattended conditions (i.e. conditions in which the focus of attention was diverted away from the stimuli due to task instructions), during visual masking and during binocular suppression. Taken together, these results reveal the relative degree of autonomy of emotional processing. At the same time, however, important limitations to the notion of complete automaticity have been revealed. Effects of task context and attention have been shown, as well as large inter-subject differences in sensitivity to the detection of masked fearful faces (whereby briefly presented, target fearful faces are immediately followed by a neutral face that 'masks' the initial face). A better understanding of the neural basis of emotional perception and how it relates to visual attention and awareness is likely to require further refinement of the concepts of automaticity and awareness.

Animals↗

Visual awareness and the detection of fearful faces.

A commonly held view is that emotional stimuli are processed independently of awareness. Here, the authors parametrically varied the duration of a fearful face target stimulus that was backward masked by a neutral face. The authors evaluated awareness by characterizing behavioral performance using receiver operating characteristic curves from signal detection theory. Their main finding was that no universal objective awareness threshold exists for fear perception. Although several subjects displayed a behavioral pattern consistent with previous reports (i.e., targets masked at 33 ms), a considerable percentage of their subjects (64%) were capable of reliably detecting 33-ms targets. Their findings suggest that considerable information is available even in briefly presented stimuli (possibly as short as 17 ms) to support masked fear detection.

Adult↗

Load-dependent modulation of affective picture processing.

Because of the biological significance of emotional stimuli, their processing is considered largely automatic. In the study reported herein, we tested the alternative hypothesis-namely, that the processing of emotional stimuli requires some level of attention. Our experiments utilized highly negative and arousing visual stimuli comprising mutilated bodies. All experiments employed a single task, which consisted of determining whether two peripheral bars were like oriented or not, thereby eliminating potential task-difference confounds that may have contaminated prior studies. Our results revealed that task-irrelevant unpleasant images slowed reaction time during the performance of the main task. Such interference was modulated by task difficulty as well as by alcohol consumption, showing that the processing of emotional visual stimuli is not immune to attentional manipulations. These results suggest that it is essential to utilize attentional manipulations that more fully consume attentional resources in order to demonstrate that the processing of emotional stimuli is resource limited.

Adolescent↗

Repetition suppression of faces is modulated by emotion.

Single-unit recordings and functional brain imaging studies have shown reduced neural responses to repeated stimuli in the visual cortex. By using event-related functional MRI, we compared the activation evoked by repetitions of neutral and fearful faces, which were either task relevant (targets) or irrelevant (distracters). We found that within the inferior occipital gyri, lateral fusiform gyri, superior temporal sulci, amygdala, and the inferior frontal gyri/insula, targets evoked stronger responses than distracters and their repetition was associated with significantly reduced responses. Repetition suppression, as manifested by the difference in response amplitude between the first and third repetitions of a target, was stronger for fearful than neutral faces. Distracter faces, regardless of their repetition or valence, evoked negligible activation, indicating top-down attenuation of behaviorally irrelevant stimuli. Our findings demonstrate a three-way interaction between emotional valence, repetition, and task relevance and suggest that repetition suppression is influenced by high-level cognitive processes in the human brain.

Adult↗

Neural correlates of change detection and change blindness in a working memory task.

Detecting changes in an ever-changing environment is highly advantageous, and this ability may be critical for survival. In the present study, we investigated the neural substrates of change detection in the context of a visual working memory task. Subjects maintained a sample visual stimulus in short-term memory for 6 s, and were asked to indicate whether a subsequent, test stimulus matched or did not match the original sample. To study change detection largely uncontaminated by attentional state, we compared correct change and correct no-change trials at test. Our results revealed that correctly detecting a change was associated with activation of a network comprising parietal and frontal brain regions, as well as activation of the pulvinar, cerebellum, and inferior temporal gyrus. Moreover, incorrectly reporting a change when none occurred led to a very similar pattern of activations. Finally, few regions were differentially activated by trials in which a change occurred but subjects failed to detect it (change blindness). Thus, brain activation was correlated with a subject's report of a change, instead of correlated with the physical change per se. We propose that frontal and parietal regions, possibly assisted by the cerebellum and the pulvinar, might be involved in controlling the deployment of attention to the location of a change, thereby allowing further processing of the visual stimulus. Visual processing areas, such as the inferior temporal gyrus, may be the recipients of top-down feedback from fronto-parietal regions that control the reactive deployment of attention, and thus exhibit increased activation when a change is reported (irrespective of whether it occurred or not). Whereas reporting that a change occurred, be it correctly or incorrectly, was associated with strong activation in fronto-parietal sites, change blindness appears to involve very limited territories.

Adaptation, Physiological↗

[Emotional stimuli: sensory processing and motor responses].

Emotion can be functionally considered as action dispositions preparing the organism for either avoidance- or approach- related behaviors. In order to prepare an appropriate behavioral output, the organism has to be efficient in the encoding of relevant stimuli. We herein present evidence from neuroimaging studies that seeing emotional and arousing pictures leads to greater activation in visual cortex than seeing neutral ones. In addition to this facilitation of sensory processing, emotional stimuli prompt somatic and vegetative reactions. Recordings of postural oscillations and heart rate while participants visualized a block of unpleasant pictures, revealed a significant reduction of body sway and bradycardia. A parallel investigation showed that reaction time also slows down after the visualization of negative pictures. Taken together, immobility, bradycardia and slower reaction time in the laboratory experimental set may reflect the engagement of the defensive system, resembling the defensive reactions to distant threatening stimuli in natural contexts. In summary, the affective system operates at an early level of sensory encoding and at the motor output favoring dispositions for appropriate actions.

Brain Mapping↗

Neuroimaging studies of attention and the processing of emotion-laden stimuli.

Because the processing capacity of the visual system is limited, selective attention to one part of the visual field comes at the cost of neglecting other parts. In this paper, we review evidence from single-cell studies in monkeys and functional magnetic resonance imaging (fMRI) studies in humans for neural competition and how competition is biased by attention. We suggest that, at the neural level, an important consequence of attention is to enhance the influence of behaviorally relevant stimuli at the expense of irrelevant ones, providing a mechanism for the filtering of distracting information in cluttered visual scenes. Psychophysical evidence suggests that processing outside the focus of attention is attenuated and may be even eliminated under some conditions. A major exception to the critical role of attention may be in the neural processing of emotion-laden stimuli, which are reported to be processed automatically, namely, without attention. Contrary to this prevailing view, in a recent study we found that all brain regions responding differentially to faces with emotional content, including the amygdala, did so only when sufficient resources were available to process those faces. After reviewing our findings, we discuss their implications, in particular (1) how emotional stimuli can bias competition for processing resources; (2) the source of the biasing signal for emotional stimuli; (3) how visual information reaches the amygdala; and finally (4) the relationship between attention and awareness.

Amygdala↗

From humble neural beginnings comes knowledge of numbers.

Following a recent report that monkey prefrontal cortex contains cells that represent number concepts, Nieder and Miller investigated the scale used to code numbers. In this issue of Neuron, they report that prefrontal cells use the same scale (Weber's Law) used by sensory neurons to code stimulus intensity, suggesting how abstract cognitive operations may arise from simpler building blocks that humans share with other animals.

Animals↗

Contour integration in the primary visual cortex of the opossum.

To investigate whether contour integration is a generalized mammalian feature we studied single cells in V1 on the South-America opossum ( ), a plesiomorphic animal believed to retain basic characteristics of early mammals. We observed that when a cell's receptive field (RF) was masked (i.e. an artificial scotoma was produced), sweeping a long bar (several times the length of the RF) at the cell's preferred orientation elicited robust responses in many cells (28/103, or 27%). Therefore, some cells in the primary visual cortex of the opossum interpolate under conditions consistent with physical occlusion. The present results indicate that the property of contour integration appears to be a basic property of the mammalian visual system.

Animals↗

Neural correlates of visual working memory: fMRI amplitude predicts task performance.

We used fMRI to investigate how moment-to-moment neural activity contributes to success or failure on individual trials of a visual working memory (WM) task. We found that different nodes of a distributed cortical network were activated to a greater extent for correct compared to incorrect trials during stimulus encoding, memory maintenance during delays, and at test. A logistic regression analysis revealed that the fMRI signal amplitude during the delay interval in a network of frontoparietal regions predicted successful performance on a trial-by-trial basis. Differential delay activity occurred even for only those trials in which BOLD activity during encoding was strong, demonstrating that it was not a simple consequence of effective versus ineffective encoding. Our results indicate that accurate memory depends on strong sustained signals that span the delay interval of WM tasks.

Adult↗