Preliminary report on the association between pulvinar volume and the ability to detect backward-masked facial features.

Although backward masking is a powerful experimental tool in mitigating visual awareness of facial expressions of emotion, ~20% of participants consistently report being resistant to its effects. In our previous studies, we excluded these participants from analysis as we focused on neural data in individuals who were subjectively unaware of backward-masked facial features that were presented for a brief period of time (e.g., 17ms). Here, we shifted our focus to potential structural brain difference between aware and unaware participants. To achieve this, structural magnetic resonance imaging (sMRI) data were pooled from two recent backward masking studies of emotional faces or eye whites (Kim et al., 2016, 2010). Out of a total of 64 participants, 12 reported being subjectively aware of the masked faces or their facial features. Whole-brain, voxel-based morphometric analysis of structural MRI data yielded significantly greater volume of the posterior thalamus, including the bilateral pulvinar, for the subjectively aware versus unaware individuals. No other brain region showed significant volumetric differences between groups. The present findings offer a neuroanatomical basis for visual awareness of emotional content in the form of backward-masked facial features, which complements the known functional role of the pulvinar in such neurobehavioral processes.

Human Amygdala Tracks a Feature-Based Valence Signal Embedded within the Facial Expression of Surprise.

Human amygdala function has been traditionally associated with processing the affective valence (negative vs positive) of an emotionally charged event, especially those that signal fear or threat. However, this account of human amygdala function can be explained by alternative views, which posit that the amygdala might be tuned to either (1) general emotional arousal (activation vs deactivation) or (2) specific emotion categories (fear vs happy). Delineating the pure effects of valence independent of arousal or emotion category is a challenging task, given that these variables naturally covary under many circumstances. To circumvent this issue and test the sensitivity of the human amygdala to valence values specifically, we measured the dimension of valence within the single facial expression category of surprise. Given the inherent valence ambiguity of this category, we show that surprised expression exemplars are attributed valence and arousal values that are uniquely and naturally uncorrelated. We then present fMRI data from both sexes, showing that the amygdala tracks these consensus valence values. Finally, we provide evidence that these valence values are linked to specific visual features of the mouth region, isolating the signal by which the amygdala detects this valence information.SIGNIFICANCE STATEMENT There is an open question as to whether human amygdala function tracks the valence value of cues in the environment, as opposed to either a more general emotional arousal value or a more specific emotion category distinction. Here, we demonstrate the utility of surprised facial expressions because exemplars within this emotion category take on valence values spanning the dimension of bipolar valence (positive to negative) at a consistent level of emotional arousal. Functional neuroimaging data showed that amygdala responses tracked the valence of surprised facial expressions, unconfounded by arousal. Furthermore, a machine learning classifier identified particular visual features of the mouth region that predicted this valence effect, isolating the specific visual signal that might be driving this neural valence response.

Intolerance of uncertainty predicts increased striatal volume.

Oversensitivity to uncertain future threat is usefully conceptualized as intolerance of uncertainty (IU). Neuroimaging studies of IU to date have largely focused on its relationship with brain function, but few studies have documented the association between IU and the quantitative properties of brain structure. Here, we examined potential gray and white-matter brain structural correlates of IU from 61 healthy participants. Voxel-based morphometric analysis highlighted a robust positive correlation between IU and striatal volume, particularly the putamen. Conversely, tract-based spatial statistical analysis showed no evidence for a relationship between IU and the structural integrity of white-matter fiber tracts. Current results converge upon findings from individuals with anxiety disorders such as obsessive-compulsive disorder (OCD) or generalized anxiety disorder (GAD), where abnormally increased IU and striatal volume are consistently reported. They also converge with neurobehavioral data implicating the putamen in predictive coding. Most notably, the relationship between IU and striatal volume is observed at a preclinical level, suggesting that the volumetric properties of the striatum reflect the processing of uncertainty per se as it relates to this dimensional personality characteristic. Such a relationship could then potentially contribute to the onset of OCD or GAD, rather than being unique to their pathophysiology. (PsycINFO Database Record

A Mathematical Model Captures the Structure of Subjective Affect.

Although it is possible to observe when another person is having an emotional moment, we also derive information about the affective states of others from what they tell us they are feeling. In an effort to distill the complexity of affective experience, psychologists routinely focus on a simplified subset of subjective rating scales (i.e., dimensions) that capture considerable variability in reported affect: reported valence (i.e., how good or bad?) and reported arousal (e.g., how strong is the emotion you are feeling?). Still, existing theoretical approaches address the basic organization and measurement of these affective dimensions differently. Some approaches organize affect around the dimensions of bipolar valence and arousal (e.g., the circumplex model), whereas alternative approaches organize affect around the dimensions of unipolar positivity and unipolar negativity (e.g., the bivariate evaluative model). In this report, we (a) replicate the data structure observed when collected according to the two approaches described above, and reinterpret these data to suggest that the relationship between each pair of affective dimensions is conditional on valence ambiguity, and (b) formalize this structure with a mathematical model depicting a valence ambiguity dimension that decreases in range as arousal decreases (a triangle). This model captures variability in affective ratings better than alternative approaches, increasing variance explained from ~60% to over 90% without adding parameters.

The Inverse Relationship between the Microstructural Variability of Amygdala-Prefrontal Pathways and Trait Anxiety Is Moderated by Sex.

Anxiety impacts the quality of everyday life and may facilitate the development of affective disorders, possibly through concurrent alterations in neural circuitry. Findings from multimodal neuroimaging studies suggest that trait-anxious individuals may have a reduced capacity for efficient communication between the amygdala and the ventral prefrontal cortex (vPFC). A diffusion-weighted imaging protocol with 61 directions was used to identify lateral and medial amygdala-vPFC white matter pathways. The structural integrity of both pathways was inversely correlated with self-reported levels of trait anxiety. When this mask from our first dataset was then applied to an independent validation dataset, both pathways again showed a consistent inverse relationship with trait anxiety. Importantly, a moderating effect of sex was found, demonstrating that the observed brain-anxiety relationship was stronger in females. These data reveal a potential neuroanatomical mediator of previously documented functional alterations in amygdala-prefrontal connectivity that is associated with trait anxiety, which might prove informative for future studies of psychopathology.

A face versus non-face context influences amygdala responses to masked fearful eye whites.

The structure of the mask stimulus is crucial in backward masking studies and we recently demonstrated such an effect when masking faces. Specifically, we showed that activity of the amygdala is increased to fearful facial expressions masked with neutral faces and decreased to fearful expressions masked with a pattern mask-but critically both masked conditions discriminated fearful expressions from happy expressions. Given this finding, we sought to test whether masked fearful eye whites would produce a similar profile of amygdala response in a face vs non-face context. During functional magnetic resonance imaging scanning sessions, 30 participants viewed fearful or happy eye whites masked with either neutral faces or pattern images. Results indicated amygdala activity was increased to fearful vs happy eye whites in the face mask condition, but decreased to fearful vs happy eye whites in the pattern mask condition-effectively replicating and expanding our previous report. Our data support the idea that the amygdala is responsive to fearful eye whites, but that the nature of this activity observed in a backward masking design depends on the mask stimulus.

Differential effects of cognitive load on subjective versus motor responses to ambiguously valenced facial expressions.

Valence is a principal dimension by which we understand emotional experiences, but oftentimes events are not easily classified as strictly positive or negative. Inevitably, individuals vary in how they tend to interpret the valence of ambiguous situations. Surprised facial expressions are one example of a well-defined, ambiguous affective event that induces trait-like differences in the propensity to form a positive or negative interpretation. To investigate the nature of this affective bias, we asked participants to organize emotional facial expressions (surprised, happy, sad) into positive/negative categories while recording their hand-movement trajectories en route to each response choice. We found that positivity-negativity bias resulted in differential hand movements for modal versus nonmodal response trajectories, such that when an individual categorized a surprised face according to his or her nonmodal interpretation (e.g., a negatively biased individual selecting a positive interpretation), the hand showed an enhanced spatial attraction to the alternative, modal response option (e.g., negative) in the opposite corner of the computer screen (Experiment 1). Critically, we also demonstrate that this asymmetry between modal versus nonmodal response trajectories is mitigated when the valence interpretations are made under a cognitive load, although the frequency of modal interpretations is unaffected by the load (Experiment 2). These data inform a body of seemingly disparate findings regarding the effect of cognitive effort on affective responses, by showing within a single paradigm that varying cognitive load selectively alters the dynamic motor movements involved in indicating affective interpretations, whereas the subjective interpretations themselves remain consistent across variable cognitive loads. (PsycINFO Database Record

Interpreting ambiguous social cues in unpredictable contexts.

Unpredictable environments can be anxiety-provoking and elicit exaggerated emotional responses to aversive stimuli. Even neutral stimuli, when presented in an unpredictable fashion, prime anxiety-like behavior and elicit heightened amygdala activity. The amygdala plays a key role in initiating responses to biologically relevant information, such as facial expressions of emotion. While some expressions clearly signal negative (anger) or positive (happy) events, other expressions (e.g. surprise) are more ambiguous in that they can predict either valence, depending on the context. Here, we sought to determine whether unpredictable presentations of ambiguous facial expressions would bias participants to interpret them more negatively. We used functional magnetic resonance imaging and facial electromyography (EMG) to characterize responses to predictable vs unpredictable presentations of surprised faces. We observed moderate but sustained increases in amygdala reactivity to predictable presentations of surprised faces, and relatively increased amygdala responses to unpredictable faces that then habituated, similar to previously observed responses to clearly negative (e.g. fearful) faces. We also observed decreased corrugator EMG responses to predictable surprised face presentations, similar to happy faces, and increased responses to unpredictable surprised face presentations, similar to angry faces. Taken together, these data suggest that unpredictability biases people to interpret ambiguous social cues negatively.

Parcellation of Human Amygdala Subfields Using Orientation Distribution Function and Spectral K-means Clustering.

Amygdala plays an important role in fear and emotional learning, which are critical for human survival. Despite the functional relevance and unique circuitry of each human amygdaloid subnuclei, there has yet to be an efficient imaging method for identifying these regions in vivo. A data-driven approach without prior knowledge provides advantages of efficient and objective assessments. The present study uses high angular and high spatial resolution diffusion magnetic resonance imaging to generate orientation distribution function, which bears distinctive microstructural features. The features were extracted using spherical harmonic decomposition to assess microstructural similarity within amygdala subfields are identified via similarity matrices using spectral k-mean clustering. The approach was tested on 32 healthy volunteers and three distinct amygdala subfields were identified including medial, posterior-superior lateral, and anterior-inferior lateral.

BRAIN REWARD ACTIVITY TO MASKED IN-GROUP SMILING FACES PREDICTS FRIENDSHIP DEVELOPMENT.

This study examined whether neural responses in the ventral striatum (VS) to in-group facial expressions-presented without explicit awareness-could predict friendship patterns in newly arrived individuals from China six months later. Individuals who initially showed greater VS activity in response to in-group happy expressions during functional neuroimaging later made considerably more in-group friends, suggesting that VS activity might reflect reward processes that drive in-group approach behaviors.

Neuroimaging and Anxiety: the Neural Substrates of Pathological and Non-pathological Anxiety.

Advances in the use of noninvasive neuroimaging to study the neural correlates of pathological and non-pathological anxiety have shone new light on the underlying neural bases for both the development and manifestation of anxiety. This review summarizes the most commonly observed neural substrates of the phenotype of anxiety. We focus on the neuroimaging paradigms that have shown promise in exposing this relevant brain circuitry. In this way, we offer a broad overview of how anxiety is studied in the neuroimaging laboratory and the key findings that offer promise for future research and a clearer understanding of anxiety.

To apply yourself is human, to reapply divine.

Prefrontal cortex is involved in adapting our emotional response to setbacks. While we feel that some setbacks are controllable, others are not. Here, Bhanji and Delgado (2014) reveal the neural substrates of persistence in the face of controllable and uncontrollable setbacks.

Fearful, but not angry, expressions diffuse attention to peripheral targets in an attentional blink paradigm.

We previously demonstrated that fearful facial expressions implicitly facilitate memory for contextual events whereas angry facial expressions do not. The current study sought to more directly address the implicit effect of fearful expressions on attention for contextual events within a classic attentional paradigm (i.e., the attentional blink) in which memory is tested on a trial-by-trial basis, thereby providing subjects with a clear, explicit attentional strategy. Neutral faces of a single gender were presented via rapid serial visual presentation (RSVP) while bordered by four gray pound signs. Participants were told to watch for a gender change within the sequence (T1). It is critical to note that the T1 face displayed a neutral, fearful, or angry expression. Subjects were then told to detect a color change (i.e., gray to green; T2) at one of the four peripheral pound sign locations appearing after T1. This T2 color change could appear at one of six temporal positions. Complementing previous attentional blink paradigms, participants were told to respond via button press immediately when a T2 target was detected. We found that, compared with the neutral T1 faces, fearful faces significantly increased target detection ability at four of the six temporal locations (all ps < .05) whereas angry expressions did not. The results of this study demonstrate that fearful facial expressions can uniquely and implicitly enhance environmental monitoring above and beyond explicit attentional effects related to task instructions.

Botulinum toxin-induced facial muscle paralysis affects amygdala responses to the perception of emotional expressions: preliminary findings from an A-B-A design.

BACKGROUND: It has long been suggested that feedback signals from facial muscles influence emotional experience. The recent surge in use of botulinum toxin (BTX) to induce temporary muscle paralysis offers a unique opportunity to directly test this "facial feedback hypothesis." Previous research shows that the lack of facial muscle feedback due to BTX-induced paralysis influences subjective reports of emotional experience, as well as brain activity associated with the imitation of emotional facial expressions. However, it remains to be seen whether facial muscle paralysis affects brain activity, especially the amygdala, which is known to be responsive to the perception of emotion in others. Further, it is unknown whether these neural changes are permanent or whether they revert to their original state after the effects of BTX have subsided. The present study sought to address these questions by using functional magnetic resonance imaging to measure neural responses to angry and happy facial expressions in the presence or absence of facial paralysis. RESULTS: Consistent with previous research, amygdala activity was greater in response to angry compared to happy faces before BTX treatment. As predicted, amygdala activity in response to angry faces was attenuated when the corrugator/procerus muscles were paralyzed via BTX injection but then returned to its original state after the effects of BTX subsided. This preliminary study comprises a small sample size and no placebo condition; however, the A-B-A design affords the present sample to serve as its own control. CONCLUSIONS: The current demonstration that amygdala responses to facial expressions were influenced by facial muscle paralysis offers direct neural support for the facial feedback hypothesis. Specifically, the present findings offer preliminary causal evidence that amygdala activity is sensitive to facial feedback during the perception of the facial expressions of others. More broadly, these data confirm the utility of using BTX to address the effect of facial feedback on neural responses associated with the perception, in addition to the experience or expression of emotion.

Neural responses to ambiguity involve domain-general and domain-specific emotion processing systems.

Extant research has examined the process of decision making under uncertainty, specifically in situations of ambiguity. However, much of this work has been conducted in the context of semantic and low-level visual processing. An open question is whether ambiguity in social signals (e.g., emotional facial expressions) is processed similarly or whether a unique set of processors come on-line to resolve ambiguity in a social context. Our work has examined ambiguity using surprised facial expressions, as they have predicted both positive and negative outcomes in the past. Specifically, whereas some people tended to interpret surprise as negatively valenced, others tended toward a more positive interpretation. Here, we examined neural responses to social ambiguity using faces (surprise) and nonface emotional scenes (International Affective Picture System). Moreover, we examined whether these effects are specific to ambiguity resolution (i.e., judgments about the ambiguity) or whether similar effects would be demonstrated for incidental judgments (e.g., nonvalence judgments about ambiguously valenced stimuli). We found that a distinct task control (i.e., cingulo-opercular) network was more active when resolving ambiguity. We also found that activity in the ventral amygdala was greater to faces and scenes that were rated explicitly along the dimension of valence, consistent with findings that the ventral amygdala tracks valence. Taken together, there is a complex neural architecture that supports decision making in the presence of ambiguity: (a) a core set of cortical structures engaged for explicit ambiguity processing across stimulus boundaries and (b) other dedicated circuits for biologically relevant learning situations involving faces.

Interactions between transient and sustained neural signals support the generation and regulation of anxious emotion.

Anxious emotion can manifest on brief (threat response) and/or persistent (chronic apprehension and arousal) timescales, and prior work has suggested that these signals are supported by separable neural circuitries. This fMRI study utilized a mixed block-event-related emotional provocation paradigm in 55 healthy participants to simultaneously measure brief and persistent anxious emotional responses, testing the specificity of, and interactions between, these potentially distinct systems. Results indicated that components of emotional processing networks were uniquely sensitive to transient and sustained anxious emotion. Whereas the amygdala and midbrain showed only transient responses, the ventral basal forebrain and anterior insula showed sustained activity during extended emotional contexts that tracked positively with task-evoked anxiety. States of lesser anxiety were associated with greater sustained activity in the ventromedial prefrontal cortex. Furthermore, ventromedial prefrontal recruitment was lower in individuals with higher scores on intolerance of uncertainty measures, and this hyporecruitment predicted greater transient amygdala responding to potential threat cues. This work demonstrates how brain circuitries interact across temporal scales to support brief and persistent anxious emotion and suggests potentially divergent mechanisms of dysregulation in clinical syndromes marked by brief versus persistent symptoms of anxiety.

Amygdala responses to averted vs direct gaze fear vary as a function of presentation speed.

We examined whether amygdala responses to rapidly presented fear expressions are preferentially tuned to averted vs direct gaze fear and conversely whether responses to more sustained presentations are preferentially tuned to direct vs averted gaze fear. We conducted three functional magnetic resonance imaging (fMRI) studies to test these predictions including: Study 1: a block design employing sustained presentations (1 s) of averted vs direct gaze fear expressions taken from the Pictures of Facial Affect; Study 2: a block design employing rapid presentations (300 ms) of these same stimuli and Study 3: a direct replication of these studies in the context of a single experiment using stimuli selected from the NimStim Emotional Face Stimuli. Together, these studies provide evidence consistent with an early, reflexive amygdala response tuned to clear threat and a later reflective response tuned to ambiguous threat.

Valence resolution of ambiguous facial expressions using an emotional oddball task.

Previous research suggests that neural and behavioral responses to surprised faces are modulated by explicit contexts (e.g., "He just found $500"). Here, we examined the effect of implicit contexts (i.e., valence of other frequently presented faces) on both valence ratings and ability to detect surprised faces (i.e., the infrequent target). In Experiment 1, we demonstrate that participants interpret surprised faces more positively when they are presented within a context of happy faces, as compared to a context of angry faces. In Experiments 2 and 3, we used the oddball paradigm to evaluate the effects of clearly valenced facial expressions (i.e., happy and angry) on default valence interpretations of surprised faces. We offer evidence that the default interpretation of surprise is negative, as participants were faster to detect surprised faces when presented within a happy context (Exp. 2). Finally, we kept the valence of the contexts constant (i.e., surprised faces) and showed that participants were faster to detect happy than angry faces (Exp. 3). Together, these experiments demonstrate the utility of the oddball paradigm to explore the default valence interpretation of presented facial expressions, particularly the ambiguously valenced facial expression of surprise.

A tale of two negatives: differential memory modulation by threat-related facial expressions.

Facial expressions serve as cues that encourage viewers to learn about their immediate environment. In studies assessing the influence of emotional cues on behavior, fearful and angry faces are often combined into one category, such as "threat-related," because they share similar emotional valence and arousal properties. However, these expressions convey different information to the viewer. Fearful faces indicate the increased probability of a threat, whereas angry expressions embody a certain and direct threat. This conceptualization predicts that a fearful face should facilitate processing of the environment to gather information to disambiguate the threat. Here, we tested whether fearful faces facilitated processing of neutral information presented in close temporal proximity to the faces. In Experiment 1, we demonstrated that, compared with neutral faces, fearful faces enhanced memory for neutral words presented in the experimental context, whereas angry faces did not. In Experiment 2, we directly compared the effects of fearful and angry faces on subsequent memory for emotional faces versus neutral words. We replicated the findings of Experiment 1 and extended them by showing that participants remembered more faces from the angry face condition relative to the fear condition, consistent with the notion that anger differs from fear in that it directs attention toward the angry individual. Because these effects cannot be attributed to differences in arousal or valence processing, we suggest they are best understood in terms of differences in the predictive information conveyed by fearful and angry facial expressions.