Differential neurodynamics and connectivity in the dorsal and ventral visual pathways during perception of emotional crowds and individuals: a MEG study.

Reading the prevailing emotion of groups of people ("crowd emotion") is critical to understanding their overall intention and disposition. It alerts us to potential dangers, such as angry mobs or panicked crowds, giving us time to escape. A critical aspect of processing crowd emotion is that it must occur rapidly, because delays often are costly. Although knowing the timing of neural events is crucial for understanding how the brain guides behaviors using coherent signals from a glimpse of multiple faces, this information is currently lacking in the literature on face ensemble coding. Therefore, we used magnetoencephalography to examine the neurodynamics in the dorsal and ventral visual streams and the periamygdaloid cortex to compare perception of groups of faces versus individual faces. Forty-six participants compared two groups of four faces or two individual faces with varying emotional expressions and chose which group or individual they would avoid. We found that the dorsal stream was activated as early as 68 msec after the onset of stimuli containing groups of faces. In contrast, the ventral stream was activated later and predominantly for individual face stimuli. The latencies of the dorsal stream activation peaks correlated with participants' response times for facial crowds. We also found enhanced connectivity earlier between the periamygdaloid cortex and the dorsal stream regions for crowd emotion perception. Our findings suggest that ensemble coding of facial crowds proceeds rapidly and in parallel by engaging the dorsal stream to mediate adaptive social behaviors, via a distinct route from single face perception.

Fast saccadic and manual responses to faces presented to the koniocellular visual pathway.

The parallel pathways of the human visual system differ in their tuning to luminance, color, and spatial frequency. These attunements recently have been shown to propagate to differential processing of higher-order stimuli, facial threat cues, in the magnocellular (M) and parvocellular (P) pathways, with greater sensitivity to clear and ambiguous threat, respectively. The role of the third, koniocellular (K) pathway in facial threat processing, however, remains unknown. To address this gap in knowledge, we briefly presented peripheral face stimuli psychophysically biased towards M, P, or K pathways. Observers were instructed to report via a key-press whether the face was angry or neutral while their eye movements and manual responses were recorded. We found that short-latency saccades were made more frequently to faces presented in the K channel than to P or M channels. Saccade latencies were not significantly modulated by expressive and identity cues. In contrast, manual response latencies and accuracy were modulated by both pathway biasing and by interactions of facial expression with facial masculinity, such that angry male faces elicited the fastest, and angry female faces, the least accurate, responses. We conclude that face stimuli can evoke fast saccadic and manual responses when projected to the K pathway.

Spatial and feature-based attention to expressive faces.

Facial emotion is an important cue for deciding whether an individual is potentially helpful or harmful. However, facial expressions are inherently ambiguous and observers typically employ other cues to categorize emotion expressed on the face, such as race, sex, and context. Here, we explored the effect of increasing or reducing different types of uncertainty associated with a facial expression that is to be categorized. On each trial, observers responded according to the emotion and location of a peripherally presented face stimulus and were provided with either: (1) no information about the upcoming face; (2) its location; (3) its expressed emotion; or (4) both its location and emotion. While cueing emotion or location resulted in faster response times than cueing unpredictive information, cueing face emotion alone resulted in faster responses than cueing face location alone. Moreover, cueing both stimulus location and emotion resulted in a superadditive reduction of response times compared with cueing location or emotion alone, suggesting that feature-based attention to emotion and spatially selective attention interact to facilitate perception of face stimuli. While categorization of facial expressions was significantly affected by stable identity cues (sex and race) in the face, we found that these interactions were eliminated when uncertainty about facial expression, but not spatial uncertainty about stimulus location, was reduced by predictive cueing. This demonstrates that feature-based attention to facial expression greatly attenuates the need to rely on stable identity cues to interpret facial emotion.

Sex-related differences in behavioral and amygdalar responses to compound facial threat cues.

During face perception, we integrate facial expression and eye gaze to take advantage of their shared signals. For example, fear with averted gaze provides a congruent avoidance cue, signaling both threat presence and its location, whereas fear with direct gaze sends an incongruent cue, leaving threat location ambiguous. It has been proposed that the processing of different combinations of threat cues is mediated by dual processing routes: reflexive processing via magnocellular (M) pathway and reflective processing via parvocellular (P) pathway. Because growing evidence has identified a variety of sex differences in emotional perception, here we also investigated how M and P processing of fear and eye gaze might be modulated by observer's sex, focusing on the amygdala, a structure important to threat perception and affective appraisal. We adjusted luminance and color of face stimuli to selectively engage M or P processing and asked observers to identify emotion of the face. Female observers showed more accurate behavioral responses to faces with averted gaze and greater left amygdala reactivity both to fearful and neutral faces. Conversely, males showed greater right amygdala activation only for M-biased averted-gaze fear faces. In addition to functional reactivity differences, females had proportionately greater bilateral amygdala volumes, which positively correlated with behavioral accuracy for M-biased fear. Conversely, in males only the right amygdala volume was positively correlated with accuracy for M-biased fear faces. Our findings suggest that M and P processing of facial threat cues is modulated by functional and structural differences in the amygdalae associated with observer's sex.

Predictions penetrate perception: Converging insights from brain, behaviour and disorder.

It is argued that during ongoing visual perception, the brain is generating top-down predictions to facilitate, guide and constrain the processing of incoming sensory input. Here we demonstrate that these predictions are drawn from a diverse range of cognitive processes, in order to generate the richest and most informative prediction signals. This is consistent with a central role for cognitive penetrability in visual perception. We review behavioural and mechanistic evidence that indicate a wide spectrum of domains-including object recognition, contextual associations, cognitive biases and affective state-that can directly influence visual perception. We combine these insights from the healthy brain with novel observations from neuropsychiatric disorders involving visual hallucinations, which highlight the consequences of imbalance between top-down signals and incoming sensory information. Together, these lines of evidence converge to indicate that predictive penetration, be it cognitive, social or emotional, should be considered a fundamental framework that supports visual perception.

Convergent evidence for top-down effects from the "predictive brain".

Modern conceptions of brain function consider the brain as a "predictive organ," where learned regularities about the world are utilised to facilitate perception of incoming sensory input. Critically, this process hinges on a role for cognitive penetrability. We review a mechanism to explain this process and expand our previous proposals of cognitive penetrability in visual recognition to social vision and visual hallucinations.

Visual predictions in the orbitofrontal cortex rely on associative content.

Predicting upcoming events from incomplete information is an essential brain function. The orbitofrontal cortex (OFC) plays a critical role in this process by facilitating recognition of sensory inputs via predictive feedback to sensory cortices. In the visual domain, the OFC is engaged by low spatial frequency (LSF) and magnocellular-biased inputs, but beyond this, we know little about the information content required to activate it. Is the OFC automatically engaged to analyze any LSF information for meaning? Or is it engaged only when LSF information matches preexisting memory associations? We tested these hypotheses and show that only LSF information that could be linked to memory associations engages the OFC. Specifically, LSF stimuli activated the OFC in 2 distinct medial and lateral regions only if they resembled known visual objects. More identifiable objects increased activity in the medial OFC, known for its function in affective responses. Furthermore, these objects also increased the connectivity of the lateral OFC with the ventral visual cortex, a crucial region for object identification. At the interface between sensory, memory, and affective processing, the OFC thus appears to be attuned to the associative content of visual information and to play a central role in visuo-affective prediction.

Early onset of neural synchronization in the contextual associations network.

Objects are more easily recognized in their typical context. However, is contextual information activated early enough to facilitate the perception of individual objects, or is contextual facilitation caused by postperceptual mechanisms? To elucidate this issue, we first need to study the temporal dynamics and neural interactions associated with contextual processing. Studies have shown that the contextual network consists of the parahippocampal, retrosplenial, and medial prefrontal cortices. We used functional MRI, magnetoencephalography, and phase synchrony analyses to compare the neural response to stimuli with strong or weak contextual associations. The context network was activated in functional MRI and preferentially synchronized in magnetoencephalography (MEG) for stimuli with strong contextual associations. Phase synchrony increased early (150-250 ms) only when it involved the parahippocampal cortex, whereas retrosplenial-medial prefrontal cortices synchrony was enhanced later (300-400 ms). These results describe the neural dynamics of context processing and suggest that context is activated early during object perception.

The Influence of Preoperative Physical Activity on Intraoperative Brain Function in Cardiac Surgical patients.

Background Preoperative physical activity and intraoperative brain health are recognized to influence postoperative delirium (POD). Electroencephalogram (EEG) burst suppression and cerebral desaturation are indicators of abnormal intraoperative brain health. Our study aimed to investigate the associations between preoperative physical activity and intraoperative EEG burst suppression and cerebral desaturation. Methods We retrospectively analyzed data from 67 patients from one of the institutions participating in a multisite randomized controlled trial, PANDORA, involving patients undergoing cardiac surgery. The preoperative PCS12 score calculated using the SF12 questionnaire was used as an indicator of preoperative physical activity. Intraoperative EEG and cerebral oximetry data (not the current standard of care in this facility) were collected, and the anesthesiologists were blinded to the information. We analyzed the following associations between the PCS12 score and i) burst suppression duration, ii) the number of cerebral desaturations, and iii) the number of observations with concurrent cerebral desaturation and burst suppression using a generalized linear model. The results are presented as percentage changes in outcomes, and a 95% C.I. p value < 0.05 was considered to indicate statistical significance. Results Each unit increase in the PCS12 score was associated with a 3.3% decrease in the duration of burst suppression (-3.3 [-5.3, -1.2], p value = 0.002). The duration of burst suppression decreased by 29.2% with each successive quartile increase in the PCS-12 score, indicating a dose‒response relationship (-29.2 [-41.6, -16], p < 0.001). Specifically, the patients in the last three quartiles exhibited a 55.4% reduction in BSD compared to those in the first quartile (-55.4 [-74.4, -24.6], p = 0.002) (Fig. 2). We did not observe any significant association between the PCS12 score and cerebral desaturation. Conclusion Decreased preoperative physical activity, as measured by the SF-12 questionnaire, is significantly associated with increased EEG burst suppression duration. Preoperative physical activity did not show any association with cerebral desaturations and concurrent cerebral desaturation and burst suppression. Clinical Trial information ClinicalTrials.gov Identifier- NCT04093219 https://clinicaltrials.gov/ct2/show/NCT04093219 Principal Investigator - Balachundhar Subramaniam Date of registration - September 13, 2019.

Enabling global processing in simultanagnosia by psychophysical biasing of visual pathways.

A fundamental aspect of visual cognition is our disposition to see the 'forest before the trees'. However, damage to the posterior parietal cortex, a critical brain region along the dorsal visual pathway, can produce a neurological disorder called simultanagnosia, characterized by a debilitating inability to perceive the 'forest' but not the 'trees' (i.e. impaired global processing despite intact local processing). This impairment in perceiving the global shape persists even though the ventral visual pathway, the primary recognition pathway, is intact in these patients. Here, we enabled global processing in patients with simultanagnosia using a psychophysical technique, which allowed us to bias stimuli such that they are processed predominantly by the intact ventral visual pathway. Our findings reveal that the impairment in global processing that characterizes simultanagnosia stems from a disruption in the processing of low-spatial frequencies through the dorsal pathway. These findings advance our understanding of the relationship between visuospatial attention and perception and reveal the neural mechanism mediating the disposition to see the 'forest before the trees'.

The shared signal hypothesis: Facial and bodily expressions of emotion mutually inform one another.

Decades of research show that contextual information from the body, visual scene, and voices can facilitate judgments of facial expressions of emotion. To date, most research suggests that bodily expressions of emotion offer context for interpreting facial expressions, but not vice versa. The present research aimed to investigate the conditions under which mutual processing of facial and bodily displays of emotion facilitate and/or interfere with emotion recognition. In the current two studies, we examined whether body and face emotion recognition are enhanced through integration of shared emotion cues, and/or hindered through mixed signals (i.e., interference). We tested whether faces and bodies facilitate or interfere with emotion processing by pairing briefly presented (33 ms), backward-masked presentations of faces with supraliminally presented bodies (Experiment 1) and vice versa (Experiment 2). Both studies revealed strong support for integration effects, but not interference. Integration effects are most pronounced for low-emotional clarity facial and bodily expressions, suggesting that when more information is needed in one channel, the other channel is recruited to disentangle any ambiguity. That this occurs for briefly presented, backward-masked presentations reveals low-level visual integration of shared emotional signal value.

Short Term Effects of Inner Engineering Completion Online Program on Stress and Well-Being Measures.

Introduction: The Covid-19 pandemic has been a major disruptor of routine life, resulting in increased stress and predisposing people to negative outcomes, such as insomnia, anxiety and hopelessness. Mind-body interventions have improved concentration, emotional balance, and positive emotions, with an enhanced sense of productivity, and self-confidence. We therefore hypothesized that exposure to an online mind-body intervention, "Inner Engineering Completion Online (IECO)," would reduce stress and promote well-being. Methods: This prospective cohort study enrolled participants registered for the IECO courses, which for the first time were delivered remotely, online. Participants learned a 21-min meditation practice called Shambhavi Mahamudra Kriya during the course, which incorporates controlled breathing and mediation techniques. Each enrolled participant was asked to complete self-reported electronic surveys at three key time points: at the time of consent, immediately after completing IECO, and 6 weeks after IECO completion. Effects of IECO practice were assessed using four well-validated neuropsychological scales: Perceived Stress Scale (PSS), Positive Emotion/Relationship/Engagement Scale (PERMA) Profiler, Pittsburgh Sleep Quality Index (PSQI), and Mindful Attention Awareness Scale (MAAS). A Signed Rank test was used to analyze the survey data and P-values of < 0.05 were considered statistically significant. Results: Of the 375 participants interested in participation, 164 participants were eligible. Sixty-eight participants completed surveys at all time points and were identified as compliant participants. The baseline median score for PSS in compliant participants (n = 95) was 13.5 (IQR 9, 18); immediate post-IECO median PSS score was 12 (IQR 8, 16) demonstrating a 1.5 unit decrease in PSS scores (p-value = 0.0023). Similarly, comparing PSS scores in compliant participants (n = 68) for immediate Post IECO [11.5 (IQR 8, 15.5)] to PSS scores at six weeks [8 (IQR 4.5, 12.5)] showed a statistically significant 3.5-unit decrease, indicating a reduction in stress upon routine practice of the intervention (p < 0.0001). Conclusion: Incorporating the remotely delivered mind-body intervention Shambhavi Mahamudra Kriya into daily life via the IECO program over as few as 6 weeks produced a significant stress reduction, improvement in sleep quality and mindfulness. Clinical Trial Registration: [ClinicalTrials.gov], identifier [NCT04189146].

Cross-cultural reading the mind in the eyes: an fMRI investigation.

The ability to infer others' thoughts, intentions, and feelings is regarded as uniquely human. Over the last few decades, this remarkable ability has captivated the attention of philosophers, primatologists, clinical and developmental psychologists, anthropologists, social psychologists, and cognitive neuroscientists. Most would agree that the capacity to reason about others' mental states is innately prepared, essential for successful human social interaction. Whether this ability is culturally tuned, however, remains entirely uncharted on both the behavioral and neural levels. Here we provide the first behavioral and neural evidence for an intracultural advantage (better performance for same- vs. other-culture) in mental state decoding in a sample of native Japanese and white American participants. We examined the neural correlates of this intracultural advantage using fMRI, revealing greater bilateral posterior superior temporal sulci recruitment during same- versus other-culture mental state decoding in both cultural groups. These findings offer preliminary support for cultural consistency in the neurological architecture subserving high-level mental state reasoning, as well as its differential recruitment based on cultural group membership.

Magnocellular and parvocellular pathway contributions to facial threat cue processing.

Human faces evolved to signal emotions, with their meaning contextualized by eye gaze. For instance, a fearful expression paired with averted gaze clearly signals both presence of threat and its probable location. Conversely, direct gaze paired with facial fear leaves the source of the fear-evoking threat ambiguous. Given that visual perception occurs in parallel streams with different processing emphases, our goal was to test a recently developed hypothesis that clear and ambiguous threat cues would differentially engage the magnocellular (M) and parvocellular (P) pathways, respectively. We employed two-tone face images to characterize the neurodynamics evoked by stimuli that were biased toward M or P pathways. Human observers (N = 57) had to identify the expression of fearful or neutral faces with direct or averted gaze while their magnetoencephalogram was recorded. Phase locking between the amygdaloid complex, orbitofrontal cortex (OFC) and fusiform gyrus increased early (0-300 ms) for M-biased clear threat cues (averted-gaze fear) in the ß-band (13-30 Hz) while P-biased ambiguous threat cues (direct-gaze fear) evoked increased θ (4-8 Hz) phase locking in connections with OFC of the right hemisphere. We show that M and P pathways are relatively more sensitive toward clear and ambiguous threat processing, respectively, and characterize the neurodynamics underlying emotional face processing in the M and P pathways.

Differential magnocellular versus parvocellular pathway contributions to the combinatorial processing of facial threat.

Recently, speed of presentation of facially expressive stimuli was found to influence the processing of compound threat cues (e.g., anger/fear/gaze). For instance, greater amygdala responses were found to clear (e.g., direct gaze anger/averted gaze fear) versus ambiguous (averted gaze anger/direct gaze fear) combinations of threat cues when rapidly presented (33 and 300ms), but greater to ambiguous versus clear threat cues when presented for more sustained durations (1, 1.5, and 2s). A working hypothesis was put forth (Adams et al., 2012) that these effects were due to differential magnocellular versus parvocellular pathways contributions to the rapid versus sustained processing of threat, respectively. To test this possibility directly here, we restricted visual stream processing in the fMRI environment using facially expressive stimuli specifically designed to bias visual input exclusively to the magnocellular versus parvocellular pathways. We found that for magnocellular-biased stimuli, activations were predominantly greater to clear versus ambiguous threat-gaze pairs (on par with that previously found for rapid presentations of threat cues), whereas activations to ambiguous versus clear threat-gaze pairs were greater for parvocellular-biased stimuli (on par with that previously found for sustained presentations). We couch these findings in an adaptive dual process account of threat perception and highlight implications for other dual process models within psychology.

Magnocellular projections as the trigger of top-down facilitation in recognition.

Object recognition is traditionally viewed as a hierarchical, bottom-up neural process. This view has been challenged recently by theoretical models and by findings indicating that top-down processes are involved in facilitating recognition. However, how such high-level information can be activated quickly enough to facilitate the bottom-up processing is yet unknown. We propose that such top-down facilitation is triggered by magnocellular information projected early and rapidly to the orbitofrontal cortex. Using human neuroimaging, we show that stimuli designed to bias processing toward the magnocellular pathway differentially activated the orbitofrontal cortex compared with parvocellular-biased stimuli. Although the magnocellular stimuli had a lower contrast than the parvocellular stimuli, they were recognized faster and just as accurately. Moreover, orbitofrontal activity predicted the performance advantage for the magnocellular, but not for the parvocellular-biased, stimuli, whereas the opposite was true in the fusiform gyrus. Last, analyses of effective connectivity using dynamic causal modeling showed that magnocellular-biased stimuli significantly activated pathways from occipital visual cortex to orbitofrontal cortex and from orbitofrontal cortex to fusiform gyrus. Conversely, parvocellular-biased stimuli significantly activated a pathway from the occipital visual cortex to fusiform gyrus. Our findings support the proposal that fast magnocellular projections linking early visual and inferotemporal object recognition regions with the orbitofrontal cortex facilitate object recognition by enabling the generation of early predictions.

Line-Drawn Scenes Provide Sufficient Information for Discrimination of Threat and Mere Negativity.

Previous work using color photographic scenes has shown that human observers are keenly sensitive to different types of threatening and negative stimuli and reliably classify them by the presence, and spatial and temporal directions of threat. To test whether such distinctions can be extracted from impoverished visual information, we used 500 line drawings made by hand-tracing the original set of photographic scenes. Sixty participants rated the scenes on spatial and temporal dimensions of threat. Based on these ratings, trend analysis revealed five scene categories that were comparable to those identified for the matching color photographic scenes. Another 61 participants were randomly assigned to rate the valence or arousal evoked by the line drawings. The line drawings perceived to be the most negative were also perceived to be the most arousing, replicating the finding for color photographic scenes. We demonstrate here that humans are very sensitive to the spatial and temporal directions of threat even when they must extract this information from simple line drawings, and rate the line drawings very similarly to matched color photographs. The set of 500 hand-traced line-drawing scenes has been made freely available to the research community: http://www.kveragalab.org/threat.html.

Neurodynamics and connectivity during facial fear perception: The role of threat exposure and signal congruity.

Fearful faces convey threat cues whose meaning is contextualized by eye gaze: While averted gaze is congruent with facial fear (both signal avoidance), direct gaze (an approach signal) is incongruent with it. We have previously shown using fMRI that the amygdala is engaged more strongly by fear with averted gaze during brief exposures. However, the amygdala also responds more to fear with direct gaze during longer exposures. Here we examined previously unexplored brain oscillatory responses to characterize the neurodynamics and connectivity during brief (~250 ms) and longer (~883 ms) exposures of fearful faces with direct or averted eye gaze. We performed two experiments: one replicating the exposure time by gaze direction interaction in fMRI (N = 23), and another where we confirmed greater early phase locking to averted-gaze fear (congruent threat signal) with MEG (N = 60) in a network of face processing regions, regardless of exposure duration. Phase locking to direct-gaze fear (incongruent threat signal) then increased significantly for brief exposures at ~350 ms, and at ~700 ms for longer exposures. Our results characterize the stages of congruent and incongruent facial threat signal processing and show that stimulus exposure strongly affects the onset and duration of these stages.

Social Vision: Applying a Social-Functional Approach to Face and Expression Perception.

A social-functional approach to face processing comes with a number of assumptions. First, given that humans possess limited cognitive resources, it assumes that we naturally allocate attention to processing and integrating the most adaptively relevant social cues. Second, from these cues, we make behavioral forecasts about others in order to respond in an efficient and adaptive manner. This assumption aligns with broader ecological accounts of vision that highlight a direct action-perception link, even for nonsocial vision. Third, humans are naturally predisposed to process faces in this functionally adaptive manner. This latter contention is implied by our attraction to dynamic aspects of the face, including looking behavior and facial expressions, from which we tend to overgeneralize inferences, even when forming impressions of stable traits. The functional approach helps to address how and why observers are able to integrate functionally related compound social cues in a manner that is ecologically relevant and thus adaptive.

Internal valence modulates the speed of object recognition.

Brain regions that process affect are strongly connected with visual regions, but the functional consequences of this structural organization have been relatively unexplored. How does the momentary affect of an observer influence perception? We induced either pleasant or unpleasant affect in participants and then recorded their neural activity using magnetoencephalography while they completed an object recognition task. We hypothesized, and found, that affect influenced the speed of object recognition by modulating the speed and amplitude of evoked responses in occipitotemporal cortex and regions important for representing affect. Furthermore, affect modulated functional interactions between affective and perceptual regions early during perceptual processing. These findings indicate that affect can serve as an important contextual influence on object recognition processes.