The DOI matches its Crossref record; 70 of the 70 references it cites were found in a registry or an index.
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
Citations
Cites
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Darwin, C. D. (1872) · J. Murray eBooks · doi:10.1037/10001-000 · Cited by 12,120
AFNI: Software for analysis and visualization of functional magnetic resonance neuroimages
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“Imaging data were preprocessed using AFNI (Cox, 1996), where images were slice-time corrected, spatially realigned and coregistered with the T1, and field-map corrected.”
MethodA fast diffeomorphic image registration algorithm
Ashburner, J. (2007) · NeuroImage · doi:10.1016/j.neuroimage.2007.07.007 · Cited by 8,122 · cited 1×
“Normalization was based on Diffeomorphic Anatomical Registration Through Exponentiated Lie algebra, a preferable approach relative to conventional normalization to achieve more precise spatial registration (Ashburner, 2007).”
Method(1975) · Medical Entomology and Zoology · Cited by 7,245
Barsalou, L. W. (2008) · Annual Review of Psychology · doi:10.1146/annurev.psych.59.103006.093639 · Cited by 5,936 · cited 2×
“To some degree, this state-dependent process in olfaction also aligns with the embodied perception literature, demonstrating various perceptual alterations given different internal/bodily states (e.g., fatigue and affect) (Proffitt, 2006; Barsalou, 2008).”
Background(2005) · CTIT technical reports series · Cited by 5,307
Friston, K. J., Harrison, L., & Penny, W. (2003) · NeuroImage · doi:10.1016/s1053-8119(03)00202-7 · Cited by 4,583
Psychophysiological and Modulatory Interactions in Neuroimaging
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“Finally, we further incorporated neural connectivity analysis (using dynamic causal modeling and psychophysiological interaction analysis; Friston et al., 1997, 2003; Gitelman et al., 2003) to unveil the neural circuitry subserving this dynamic, state-dependent process.”
BackgroundMethodEmotional processing in anterior cingulate and medial prefrontal cortex
Etkin, A., Egner, T., & Kalisch, R. (2011) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2010.11.004 · Cited by 3,059 · cited 2×
“, 1994; Zelano and Sobel, 2005; Gottfried, 2010); and emotion areas—amygdala and anterior cingulate cortex (ACC), especially considering their close relationship with anxiety (Rauch et al., 2003; Bishop et al., 2004; Etkin et al., 2011).”
BackgroundStereotaxic Display of Brain Lesions
Rorden, C., & Brett, M. (2000) · Behavioural Neurology · doi:10.1155/2000/421719 · Cited by 2,573 · cited 2×
“Other ROIs were based on anatomical masks assembled in MRIcro (Rorden and Brett, 2000) and drawn on the mean T1 image, with reference to a human brain atlas (Mai et al., 1997).”
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Research works printed but not linked: 1
- 10.1037/0894-4105.12.3.446 · DOI
Cited by
Sorted by citations
The Association Between Olfaction and Depression: A Systematic Review
Kohli, P., Soler, Z. M., Nguyen, S. A., Muus, J. S., & Schlosser, R. J. (2016) · Chemical Senses · doi:10.1093/chemse/bjw061 · Cited by 354
“These areas also transmit “top-down” reciprocal axons (Krusemark et al. 2013).”
BackgroundCharacterizing functional pathways of the human olfactory system
Zhou, G., Lane, G., Echevarria‐Cooper, S. L., Kahnt, T., & Zelano, C. (2019) · eLife · doi:10.7554/elife.47177 · Cited by 203
Behavioral and Neurobiological Convergence of Odor, Mood and Emotion: A Review
Kontaris, I., East, B. S., & Wilson, D. A. (2020) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2020.00035 · Cited by 158
“This anxiety-induced change in odor perception is associated with enhanced PCX and OFC odor-evoked activity, and enhanced functional connectivity between the amygdala and olfactory cortex (Krusemark et al., 2013).”
BackgroundInfluentialEmotion regulation and the salience network: a hypothetical integrative model of fibromyalgia
Pinto, A. M., Geenen, R., Wager, T. D., Lumley, M. A., Häuser, W., Kosek, E., Ablin, J. N., Amris, K., Branco, J., Buskila, D., et al. (2022) · Nature Reviews Rheumatology · doi:10.1038/s41584-022-00873-6 · Cited by 161
Effects by inhalation of abundant fragrances in indoor air – An overview
Wolkoff, P., & Nielsen, G. D. (2017) · Environment International · doi:10.1016/j.envint.2017.01.013 · Cited by 134
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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