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When the Sense of Smell Meets Emotion: Anxiety-State-Dependent Olfactory Processing and Neural Circuitry Adaptation
Open accessAbstract
Phylogenetically the most ancient sense, olfaction is characterized by a unique intimacy with the emotion system. However, mechanisms underlying olfaction–emotion interaction remain unclear, especially in an ever-changing environment and dynamic internal milieu. Perturbing the internal state with anxiety induction in human subjects, we interrogated emotion-state-dependent olfactory processing in a functional magnetic resonance imaging (fMRI) study. Following anxiety induction, initially neutral odors become unpleasant and take longer to detect, accompanied by augmented response to these odors in the olfactory (anterior piriform and orbitofrontal) cortices and emotion-relevant pregenual anterior cingulate cortex. In parallel, the olfactory sensory relay adapts with increased anxiety, incorporating amygdala as an integral step via strengthened (afferent or efferent) connections between amygdala and all levels of the olfactory cortical hierarchy. This anxiety-state-dependent neural circuitry thus enables cumulative infusion of limbic affective information throughout the olfactory sensory progression, thereby driving affectively charged olfactory perception. These findings could constitute an olfactory etiology model of emotional disorders, as exaggerated emotion–olfaction interaction in negative mood states turns innocuous odors aversive, fueling anxiety and depression with rising ambient sensory stress.
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“The sense of olfaction is unique in projecting directly to the amygdala and the orbitofrontal cortex, thus providing a close connection with the limbic system”
From The scent of emotions: A systematic review of human intra‐ and interspecific chemical communication of emotions (2020) · cites this paper as Krusemark, Novak, Gitelman, & Li, 2013
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Kaimal, G. (2022) · Oxford University Press eBooks · doi:10.1093/oso/9780197646229.003.0004
Tracking creative self-expression through imaging tools
Kaimal, G. (2022) · Oxford University Press eBooks · doi:10.1093/oso/9780197646229.003.0007
Kaimal, G. (2022) · Oxford University Press eBooks · doi:10.1093/oso/9780197646229.002.0009
Kaimal, G. (2022) · Oxford University Press eBooks · doi:10.1093/oso/9780197646229.002.0003
Philosophical perspectives and theories about creative self-expression and well-being
Kaimal, G. (2022) · Oxford University Press eBooks · doi:10.1093/oso/9780197646229.003.0003
The Influence of Aromatic Scents on Emotions: Using Olfactory Imagery as a Medium
夏, 孝. (2022) · Advances in Psychology · doi:10.12677/ap.2022.1211449
Assessment of Food Odor-Evoked Emotions Using Functional Magnetic Resonance Imaging
Han, P., & Hummel, T. R. (2023) · Methods and protocols in food science · doi:10.1007/978-1-0716-2934-5_20
Les habiletés olfactives des personnes polyhandicapées
Petitpierre, G., & Dind, J. (2023) · Revue suisse de pédagogie spécialisée · doi:10.57161/r2023-02-07
“Il n’est pas rare d’éprouver des émotions positives, ou un sentiment de détente, en sentant de « bonnes odeurs » (Krusemark et al., 2013).”
Metadata
- Authors
- Krusemark, E. A., Novak, L. R., Gitelman, D. R., & Li, W.
- Affiliations
- Northwestern University (US)
- University of Wisconsin–Madison (US)
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2013-09-25
- Volume
- 33
- Issue
- 39
- Pages
- 15324-15332
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC3782615
- OpenAlex
- W2048207916
- Cited by
- 222
- References
- 70
- Citations by year
- 2026: 13 · 2025: 19 · 2024: 11 · 2023: 26 · 2022: 37 · 2021: 23 · 2020: 19 · 2019: 14 · 2018: 14 · 2017: 15 · 2016: 10 · 2015: 18 · 2014: 3
- FWCI
- 5.96
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health
- National Institute of Mental Health (R01MH093413, T32MH018931)
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (P30HD03352., P30HD003352)
- Topics
- Life Sciences › Neuroscience › Sensory Systems › Olfactory and Sensory Function Studies
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Keywords
- anxiety, olfaction, odor detection, piriform cortex, orbitofrontal cortex, pregenual anterior cingulate cortex, amygdala, emotional disorders, depression
- MeSH terms
- Adaptation, Physiological, Adolescent, Adult, Amygdala, Anxiety, Cerebral Cortex, Female, Humans, Male, Nerve Net, Odorants, Smell, Olfactory Perception
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