Enhanced Olfactory Sensory Perception of Threat in Anxiety: An Event-Related fMRI Study
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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 causal mechanism of anxiety. 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 systematic 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 interaction 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, indicative of 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, highlighting neurosensory mechanisms that may underlie the deleterious symptoms of anxiety.
KeywordsOlfaction Threat fMRI Piriform Perception Anxiety
Thanks to Lucas Novak for help with data collection. Parts of this research were funded by a Training grant from the National Institute of Health T32-MH018931-22 to E.A.K.
- Adolphs R, Damasio H, Tranel D, Damasio AR (1996) Cortical systems for the recognition of emotion in facial expressions. J Neurosci 16:7676–7687Google Scholar
- Dilger S, Straube T, Mentzel HJ, Fitzek C, Reichenbach J, Hecht H, Krieschel S, Gutberlet I, Miltner WHR (2003) Brain activation to phobia-related pictures in spider phobic humans: an event-related functional magnetic resonance imaging study. Neurosci Lett 348:29–32Google Scholar
- Gottfried JA (2006) Smell: central nervous processing. Adv Otorhinolaryngol 63:44–69Google Scholar
- Kanwisher N, McDermott J, Chun MM (1997) The fusiform face area: a module in human extrastriate cortex specialized for face perception. J Neurosci 17:4302–4311Google Scholar
- Kats LB, Dill LM (1998) The scent of death: chemosensory assessment of predation risk by prey animals. Ecoscience 5:361–394Google Scholar
- Mai JK, Assheuer J, Paxinos G (1997) Atlas of the human brain. Academic, CaliforniaGoogle Scholar
- Oya H, Kawasaki H, Howard MA 3rd, Adolphs R (2002) Electrophysiological responses in the human amygdala discriminate emotion categories of complex visual stimuli. J Neurosci 22:9502–9512Google Scholar
- Rorden C, Brett M (2000) Stereotaxic display of brain lesions. Behav Neurol 12:191–200Google Scholar
- Wolpe J, Lazarus AA (1966) Behavior therapy techniques: a guide to treatment of neuroses. Pergamon Press, OxfordGoogle Scholar