1. Enhanced olfactory sensory perception of threat in anxiety: An event-related fMRI study
The current conceptualization of threat processing in anxiety emphasizes emotional hyper-reactivity, which mediates various debilitating symptoms and derangements in anxiety disorders. Here, we investigated olfactory sensory perception of threat as an alternative account for anxiety genesis. Combining an event-related functional magnetic resonance imaging paradigm with an olfactory discrimination task, we examined how anxiety modulates basic perception of olfactory threats at behavioral and neural levels. In spite of subthreshold presentation of negative and neutral odors, a positive systemic association emerged between negative odor discrimination accuracy and anxiety levels. In parallel, the right olfactory primary (piriform) cortex indicated augmented response to subthreshold negative (vs. neutral) odors as a function of individual differences in anxiety. Using a psychophysiological (PPI) analysis, we further demonstrated amplified functional connectivity between the piriform cortex and emotion-related regions (amygdala and hippocampus) in response to negative odor, particularly in anxiety. Finally, anxiety also intensified skin conductance response to negative (vs. neutral) odor, indicating potentiated emotional arousal to subliminal olfactory threat in anxiety. Together, these findings elucidate exaggerated processing of olfactory threat in anxiety across behavioral, autonomic physiological, and neural domains. Critically, our data emphasized anxiety-related hyper-sensitivity of the primary olfactory cortex and basic olfactory perception in response to threat, supporting a novel neurosensory account that may underlie the deleterious symptoms of anxiety.
2. Hemispheric asymmetry and visuo-olfactory integration in perceiving subthreshold fearful expressions
Multisensory integration is ubiquitous, facilitating perception beyond the limit of individual senses. This mechanism is especially salient when individual sensory input is weak, potentially fusing undetectable traces into a tangible percept (“the principle of inverse effectiveness”). Nevertheless, it is unclear how this rule applies to threat perception, synthesizing elusive, discrete traces of a threat into a discernible danger signal. In light of hemispheric asymmetry in threat processing, we combined parafoveal stimulus presentation and the contralateral P1 event-related potential to investigate how aversive olfactory inputs enhance visual perception of highly degraded, subthreshold fearful expressions. The dominant right hemisphere exhibited early visual discrimination between subtle fear and neutral expressions, independently of accompanying odors. In the left hemisphere, differential visual processing occurred only at the convergence of negative odors and minute facial fear, highlighting the success and necessity of visuo-olfactory threat integration in this disadvantaged hemisphere. Reaction time data from a subsequent dot-detection task complemented these neural findings, revealing odor-dependent and hemisphere-specific modulation of spatial attention to facial expressions. Our evidence thus indicates crossmodal threat integration in basic visual perception that captures minimal threat information, especially in the “blind” right hemifield. Critically, this interaction between multisensory synergy and hemispheric asymmetry in threat perception may underlie the multifaceted fear experiences in everyday life, optimizing responses to maximize ecological interest in the face of danger.
3. From early specialization to later generalization: Dynamic perceptual categorization of individual threat emotions
Object perception typically follows a hierarchical progression from simple to complex and from general to specific, but it is unclear how individual threat emotions are categorized in perceptual processing. Using visual event-related potentials in a “looming” paradigm, we demonstrate that two threat subtypes—fear and disgust—engage distinct initial visual encoding (104 ms), succeeded by convergent visual analysis in downstream inferior temporal cortex (>540 ms). That fear enhanced and disgust suppressed early sensory response, relative to neutral emotion, coincides with opposite behavioral and autonomic reflexes these two threats typically elicit. By contrast, the later perceptual confluence of fear and disgust, corroborated by comparable exaggeration in perceived object looming in both conditions, highlights general threat categorization in later perceptual processing to guide motivationally appropriate behavior. Therefore, contrary to standard object perception, human threat perception engages an initial mandatory specialization of individual threats, followed by context-dependent generalization at a later stage.
4. Parametric depiction of early and late processing of fear and disgust in various intensities
In real life, we experience threat in differing intensities, ranging from a mild threat of confronting an unfriendly face to the extreme threat of facing death. Strikingly, how humans respond to varying levels of threat has hardly been systemically studied, especially in terms of the underlying neural mechanisms. Here, combining morphing techniques and brain electrophysiology, we varied the percentage of a fearful face mixed in a neutral face from 2% to 30% (in increments of 4%) to parametrically delineate early and late analysis of threat emotions, and to associate threat processing with individual levels of anxiety. Behavioral data suggested a clear sigmoid function between fear detection rate and fear intensity level. Importantly, we uncovered a fear detection threshold shift due to anxiety: anxious individuals exhibited a lower threshold (i.e. lower fear intensity) than non-anxious participants, highlighting a perceptual acuity to threat. Interestingly, the P3 event-related potential indicated a clear linear function between P3 amplitude and fear intensity, accentuating a parametric tacking system in later visual perception of threat.
5. An fMRI investigation of olfactory alliesthesia: Enhanced olfactory sensory acuity in anxiety.
The current literature offers little information about threat processing in senses other than vision. Among all senses, olfaction has nonetheless a uniquely intimate relationship with emotion. Moreover, accruing evidence suggests that olfactory dysfunction is associated with emotional disorders in addition to schizophrenia, meriting deliberate investigation of olfactory threat processing to uncover an olfactory-specific etiological mechanism of anxiety. Importantly, olfactory hedonic evaluation tends to depend on the perceiver’s internal state (i.e., olfactory alliesthesia). As such, anxiety as an internal state can negatively shift odor valence and confront anxious people with increased olfactory stress in everyday life. Combining experimental provocation of anxiety with fMRI techniques, we tested the hypothesis that anxiety improves olfactory acuity such that initially undetectable/negligible nuisance odors become perceptible, accompanied by enhanced activation of the emotion network in the brain and augmented autonomic arousal in the periphery. This is the first study to extricate the neural mechanisms of anxiety-state-dependent olfactory encoding, a system that could potentially mediate fundamental anxiety pathology.
6. Olfactory-visual synthesis sharpens subthreshold threat perception: an fMRI study.
As noted above, all species equipped with multiple senses integrate them to optimize perception and action. This process is especially prominent when minimal sensory information is available. In line with our overarching theorization of aberrant threat perception in anxiety, we examined the hypothesis that crossmodal synergy of threat perception is particularly elevated in anxiety, such that concordant multisensory threat signals, even though individually unnoticeable, become evident in anxious people. This model may stand as a highly novel pathological mechanism for anxiety, by exposing people to otherwise unnoticeable sensory stressors and thus fueling anxious response. In this fMRI study, we presented subthreshold threat cues through both faces and odors that contained either neutral or subtle negative emotion, where the bimodal inputs are either concordant or disconcordant in the affective content, forming a 2-by-2 factorial design. This project represents the first study to elucidate the neural basis of crossmodal (olfactory-visual) synergy in perceiving otherwise undetectable threat in faces and smells. Notably, this work addresses a key question in basic affective neuroscience research by integrating multimodal representations of threat. Furthermore, to examine the modulatory effect of anxiety, we measured subjects’ anxiety levels (trait and state) based on self-report inventories, and recorded skin conductance response data during fMRI scanning to further specify anxiety-related responses.
7. In search of a “deliciousness” brain: Neural basis of food palatability coding
Feeding is one of the most fundamental biological needs for all living organisms. In human society, to greater or lesser degrees, life revolves around food. Appropriate food intake brings joy and gratification, but aberrant feeding behavior can lead to serious medical and social problems such as obesity and eating disorders. Nevertheless, we know very little about how the incentive-motivational value of food (i.e., “deliciousness” or food palatability) is encoded in the brain. Food palatability is known as a supralinear product of a complex system, a fusion of senses of the taste (gustatory sense), smell (olfactory sense), texture (haptic sense) and appearance (visual sense) of the food. Therefore, it is important to consider food palatability in a multisensory context. Presumably, vision is the most important sense in humans, and variations in color, gloss and shape can greatly impact food palatability. Additionally, olfaction plays a predominant role in the appreciation of flavor; numerous aromas have the capacity to turn a handful of tastes (e.g., sweet, sour, salt) into virtually limitless varieties of food experience. Therefore, combining functional magnetic resonance imaging (fMRI) and sophisticated psychophysics, we aim to investigate the neural coding of food palatability by examining how visual and olfactory food cues interact with each other to instigate response in affect- and food-related neural networks. Critically, by contrasting pleasant food versus pleasant non-food stimuli, we aim to isolate specific neural circuitry assigned to primary reinforcers (e.g., a chocolate cookie) as opposed to secondary reinforcers (e.g., a rose). We believe that this study will address a couple of fundamental questions in affective neuroscience that remain obscure. Finally, my lab will be in collaboration with the C. Auger lab integrating salivary biomarkers (alpha-amylase, vasopressin, etc) and neural assays to precisely delineate the mechanisms in question here.
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