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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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Arnold, T. C., You, Y., Ding, M., Zuo, X., de Araújo, I., & Li, W. (2020) · eNeuro · doi:10.1523/eneuro.0551-19.2020 · Cited by 42
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Lavender improves sleep through olfactory perception and GABAergic neurons of the central amygdala
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Bagnasco, D., Passalacqua, G., Braido, F., Tagliabue, E., Cosini, F. F., Filauro, M., Ioppi, A., Carobbio, A. L. C., Mocellin, D., Riccio, A., et al. (2021) · World Allergy Organization Journal · doi:10.1016/j.waojou.2020.100497 · Cited by 21
“An inadequate vocabulary in the description of the presented odors may, again, have caused a difficulty in recognizing the odor presented during the test.(32)”
BackgroundMeier, L., Friedrich, H., Federspiel, A., Jann, K., Morishima, Y., Landis, B. N., Wiest, R., Strik, W. K., & Dierks, T. (2015) · NeuroImage · doi:10.1016/j.neuroimage.2015.03.048 · Cited by 19
“…homeostatic (Tataranni et al., 1999, Liotti et al., 2001, Parsons et al., 2001, Denton et al., 2009, Farrell et al., 2011) or sensoryevoked (LeDoux, 2003, Dalgleish, 2004, Craig, 2009, Vytal and Hamann, 2010, Chapman and Anderson, 2012, LeDoux, 2012, Krusemark et al., 2013) emotions independently.”
BackgroundGreening, S. G., Lee, T., & Mather, M. (2016) · Brain Sciences · doi:10.3390/brainsci6010002 · Cited by 19
Bertlich, M., Stihl, C., Lüsebrink, E., Hellmuth, J. C., Scherer, C., Freytag, S., Spiegel, J. L., Stoycheva, I., Canis, M., Weiss, B. G., et al. (2021) · European Archives of Oto-Rhino-Laryngology · doi:10.1007/s00405-021-06796-4 · Cited by 17
“This is particularly important as especially long-term chemosensory dysfunction is associated with a number of severe psychosocial disorders as decreased sexual attraction [8] and increased risk for depression [9, 10].”
BackgroundMady, L. J., Ravin, E. D., Vohra, V., Lu, J. S., Newman, J. G., Hall, D. E., Dalton, P., & Rowan, N. R. (2023) · JAMA Otolaryngology–Head & Neck Surgery · doi:10.1001/jamaoto.2023.1935 · Cited by 16
Long-term monitoring of indoor, outdoor, and personal exposure to gaseous chemical compounds
Uchiyama, S., Noguchi, M., Hishiki, M., Shimizu, M., Kunugita, N., Isobe, T., & Nakayama, S. F. (2023) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2023.167830 · Cited by 16
Iokawa, K., Kohzuki, M., Sone, T., & Ebihara, S. (2017) · Complementary Therapies in Medicine · doi:10.1016/j.ctim.2017.11.009 · Cited by 16
EEG Revealed That Fragrances Positively Affect Menopausal Symptoms in Mid-life Women
Moon, S. A., Bae, J., Kim, K., Cho, S. Y., Kwon, G., Lee, R., Ko, S. H., Lim, S., & Moon, C. (2020) · Experimental Neurobiology · doi:10.5607/en20036 · Cited by 17
Impact of Routine Endoscopic Skull Base Surgery on Subjective Olfaction and Gustation Outcomes
Hura, N., Orlov, C. P., Khalafallah, A. M., Mukherjee, D. R., & Rowan, N. R. (2021) · Operative Neurosurgery · doi:10.1093/ons/opab137 · Cited by 16
Pardasani, M., Ramakrishnan, A. M., Mahajan, S., Kantroo, M., McGowan, E., Das, S., Srikanth, P., Pandey, S., & Abraham, N. M. (2023) · Molecular Psychiatry · doi:10.1038/s41380-023-02244-3 · Cited by 17
Giguère, F. L., Jobin, B., Robert, J., Bastien, L., Giguère, J., Beaumont, L. D., de Guise, É., & Frasnelli, J. (2020) · Chemical Senses · doi:10.1093/chemse/bjaa037 · Cited by 14
Nosewitness Identification: Effects of Negative Emotion
Alho, L., Soares, S. C., Ferreira, J., Rocha, M., da Silva, C. F., & Olsson, M. J. (2015) · PLoS ONE · doi:10.1371/journal.pone.0116706 · Cited by 14
Both anxiety and joint laxity determine the olfactory features in panic disorder
Burón, E., Bulbena, A., Bulbena-Cabré, A., Rosado, S., & Pailhez, G. (2018) · Psychiatry Research · doi:10.1016/j.psychres.2017.09.018 · Cited by 14
Romashchenko, A. V., Петровский, Д. В., Trotsky, S. Y., Morozova, K. N., Illarionova, N. B., Zhukova, M. V., Владимировна, К. Е., Sharapova, M. B., Zuev, D. S., Kuper, K. E., et al. (2023) · Nano Research · doi:10.1007/s12274-022-5302-6 · Cited by 13
Tong, C., Ding, Y., Zhang, Z. G., Zhang, H., Lim, K. J., & Guan, C. (2024) · IEEE Transactions on Neural Systems and Rehabilitation Engineering · doi:10.1109/tnsre.2024.3399326 · Cited by 13
“T HE sense of smell is known to be related to human memory and emotion [1], [2], [3], [4], [5], [6].”
BackgroundCieri, F., Giriprakash, P. P., Nandy, R. R., Zhuang, X., Doty, R. L., Caldwell, J., & Cordes, D. (2024) · Neuroscience · doi:10.1016/j.neuroscience.2024.08.031 · Cited by 13
“…’ s (AD), and is often present in Mild Cognitive Impairment (MCI), (Cowart, 1989; Doty et al., 1984) showing a positive correlation with cognitive performance (Doty, 2012; Doty & Kamath, 2014; Windon et al., 2020) and a negative correlation with anxiety (Cieri et al., 2023; Krusemark et al., 2013).”
Cannabinoids as an Emerging Therapy for Posttraumatic Stress Disorder and Substance Use Disorders
Cohen, J., Wei, Z., Phang, J., Laprairie, R. B., & Zhang, Y. (2019) · Journal of Clinical Neurophysiology · doi:10.1097/wnp.0000000000000612 · Cited by 12
Are All Anxieties Created Equal? Stress-related Networks and Anxiety Phenotypes in Old Age
Kolobaric, A., Karim, H. T., Banihashemi, L., Mizuno, A. N., Aizenstein, H. J., & Andreescu, C. (2021) · American Journal of Geriatric Psychiatry · doi:10.1016/j.jagp.2021.12.007 · Cited by 13
Narla, C., Dunn, H. A., Ferguson, S. S. G., & Poulter, M. O. (2015) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2015.00200 · Cited by 13
“Odor perception can induce stressor responses which are highly context dependent (Kadohisa, 2013; Krusemark et al., 2013) and therefore it is reasonable to hypothesize the PC could be modulated by neurochemical processes depending on the nature of the stressor.”
BackgroundAi, Y., Hummel, T. R., Nie, H., Yang, J., & Han, P. (2023) · NeuroImage · doi:10.1016/j.neuroimage.2023.120474 · Cited by 12
“A transient anxious emotional state decreases the pleasantness rating of an initially neutral odor, which is accompanied by an enhanced odor-induced brain response in the olfactory and emotion-relevant cortices (Krusemark et al., 2013).”
Perceptual Mechanisms of Anxiety and Its Disorders
Li, W. (2018) · Cambridge University Press eBooks · doi:10.1017/9781108140416.004 · Cited by 10
“…of threat? fMRI data have revealed enhanced visual (Åhs et al., 2009; Etkin & Wager, 2007; Lipka et al., 2011; Paquette et al., 2003; Straube et al., 2005) and olfactory cortical activity (Krusemark & Li, 2012; Krusemark et al., 2013) in response to threat in anxious patients and individuals.”
Self-citationKaimal, G. (2022) · doi:10.1093/oso/9780197646229.001.0001 · Cited by 11
TESANet: Self-attention network for olfactory EEG classification
Tong, C., Ding, Y., Liang, K. L. J., Zhang, Z., Zhang, H., & Guan, C. (2022) · International Joint Conference on Neural Networks (IJCNN) · doi:10.1109/ijcnn55064.2022.9892920 · Cited by 11
Effect of scent on comfort of aircraft passengers
Yao, X., Song, Y., & Vink, P. (2020) · Work · doi:10.3233/wor-208025 · Cited by 11
“Lieff and Alper [15] also described olfactory as “our most emotional sense” , which could be explained by the neural structure involved in odor signal processing, as the neuroanatomy of olfactory is intertwined with emotion processing regions in the brain [16].”
BackgroundGenetic influences of autism candidate genes on circuit wiring and olfactory decoding
Hartig, R., Wolf, D., Schmeißer, M. J., & Kelsch, W. (2021) · Cell and Tissue Research · doi:10.1007/s00441-020-03390-8 · Cited by 11
“Salient odors evoking emotional responses have been found to modulate olfactory cortices as well as breathing rhythmicity (Krusemark et al. 2013).”
BackgroundSex differences in hedonic judgement of odors in schizophrenia cases and healthy controls
Walsh‐Messinger, J., Wong, P. S., Antonius, D., McMahon, K. L., Opler, L. A., RAMIREZ, P. M., & Malaspina, D. (2018) · Psychiatry Research · doi:10.1016/j.psychres.2018.08.058 · Cited by 14
“Further clarification of these associations may come from a recent finding in which healthy individuals who underwent anxiety induction rated neutral odors as more unpleasant, took longer to detect neutral odors, and showed greater neural response in the orbitofrontal cortex and pregenual anterior cingulate cortex, re…”
BackgroundGlial cells in the mammalian olfactory bulb
Zhao, D., Hu, M., & Liu, S. (2024) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2024.1426094 · Cited by 11
Repeated stress gradually impairs auditory processing and perception
Bisharat, G., Kaganovski, E., Sapir, H., Temnogorod, A., Levy, T., & Resnik, J. (2025) · PLoS Biology · doi:10.1371/journal.pbio.3003012 · Cited by 10
Functional Connectivity of the Chemosenses: A Review
Farruggia, M. C., Pellegrino, R., & Scheinost, D. (2022) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2022.865929 · Cited by 14
Lullaland: A Multisensory Virtual Reality Experience to Reduce Stress
Liu, B., Wang, W., Zhang, Y., Huang, R., & Raiti, J. (2023) · CHI Conference Extended Abstracts on Human Factors in Computing Systems (CHI EA) · doi:10.1145/3544549.3585636 · Cited by 10
“However, the VR immersive experience can be easily disrupted by the hospital smell of disinfectant [23].”
Background
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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