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, providing a close connection with the limbic system.
“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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Roles of olfactory system dysfunction in depression
Yuan, T., & Slotnick, B. M. (2014) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2014.05.013 · Cited by 90 · see citing works
“In addition, the level of olfactory performance, such as detection acuity was correlated to emotion status of the subject (Hardy et al., 2012; Krusemark et al., 2013).”
BackgroundRespiratory regulation & interactions with neuro-cognitive circuitry
Maric, V., Ramanathan, D., & Mishra, J. (2020) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2020.02.001 · Cited by 82 · see citing works
Yao, T., Lin, W. C., Bao, Z., & Zeng, C. (2024) · Sustainable Cities and Society · doi:10.1016/j.scs.2024.105293 · Cited by 75 · see citing works
The halogen bond with isocyano carbon reduces isocyanide odor
Mikherdov, A. S., Novikov, A. S., Boyarskiy, V. P., & Kukushkin, V. Y. (2020) · Nature Communications · doi:10.1038/s41467-020-16748-x · Cited by 74 · see citing works
Calvi, E., Quassolo, U., Massaia, M., Scandurra, A., D'Aniello, B., & D'Amelio, P. (2020) · Brain and Behavior · doi:10.1002/brb3.1585 · Cited by 71 · see citing works
Lasting connectivity increase and anxiety reduction via transcranial alternating current stimulation
Clancy, K. J., Baisley, S. K., Albizu, A., Kartvelishvili, N., Ding, M., & Li, W. (2018) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsy096 · Cited by 69 · see citing works
“…changes would be accompanied by lasting anxiety reduction, measured here by anxious arousal and negative perception of sensory stimuli (in the auditory and olfactory modalities given their sensitivity to states of anxious arousal) (Adler et al., 1988; Grillon et al., 1991; Krusemark et al., 2013).”
BackgroundSelf-citationMasuo, Y., Satou, T., Takemoto, H., & Koike, K. (2021) · Molecules · doi:10.3390/molecules26092571 · Cited by 68 · see citing works
Grounding Semantics in Olfactory Perception
Kiela, D., Bulat, L., & Clark, S. C. (2015) · doi:10.3115/v1/p15-2038 · Cited by 64 · see citing works
Sensing fear: Fast-and-precise threat evaluation in human sensory cortex
Li, W., & Keil, A. (2022) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2023.01.001 · Cited by 59 · see citing works
“In addition, an fMRI study modeled causal information fl ow between sensory and limbic areas and demonstrated that projections from the sensory cortex to the amygdala drove negative perception induced by an anxious state [85].”
Self-citationChung, J. H., Lee, Y. J., Kang, T. W., Kim, K. R., Jang, D. P., Kim, I. Y., & Cho, S. H. (2015) · Annals of Otology Rhinology & Laryngology · doi:10.1177/0003489415576181 · Cited by 61 · see citing works
“Numerous studies have been conducted to investigate the association between the olfactory dysfunction and psychological health.(27,28) Moreover, olfactory loss itself affects brain function, particularly for emotion and memory through reduced sensory input from the olfactory bulb via the amygdala into the limbic syste…”
BackgroundOdor-induced recall of emotional memories in PTSD–Review and new paradigm for research
Daniels, J. K., & Vermetten, E. H. G. J. M. (2016) · Experimental Neurology · doi:10.1016/j.expneurol.2016.08.001 · Cited by 63 · see citing works
“New insights into the close interrelation between emotion and olfaction stemsfrom a laboratory study using anxietyinductionto studycorrelat-ed changes in olfactory functioning in humans (Krusemark et al., 2013).”
MethodJain, R., & Ramakrishnan, A. G. (2020) · Frontiers in Neuroscience · doi:10.3389/fnins.2020.555093 · Cited by 56 · see citing works
He, Z., Cui, Q., Zheng, J., Duan, X., Pang, Y., Gao, Q. C., Han, S., Long, Z., Wang, Y., Li, J., et al. (2016) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2016.07.011 · Cited by 54 · see citing works
Qamar, M. A., Sauerbier, A., Politis, M., Carr, H. J., Loehrer, P. A., & Chaudhuri, К. R. (2017) · npj Parkinson s Disease · doi:10.1038/s41531-016-0006-9 · Cited by 53 · see citing works
“However, involvement of the cholinergic system is also likely given the recent definition of the olfactory-limbic pathway.(199,200) Abnormal weight change is a common symptom in PD, affecting patients early.”
Extinction reverses olfactory fear-conditioned increases in neuron number and glomerular size
Morrison, F. G., Dias, B. G., & Ressler, K. J. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1505068112 · Cited by 53 · see citing works
Learning to smell danger: acquired associative representation of threat in the olfactory cortex
Li, W. (2014) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2014.00098 · Cited by 48 · see citing works
Self-citationPerception and emotions: On the relationships between stress and olfaction
Bombail, V. (2018) · Applied Animal Behaviour Science · doi:10.1016/j.applanim.2018.12.013 · Cited by 49 · see citing works
Amygdalar Gating of Early Sensory Processing through Interactions with Locus Coeruleus
Fast, C. D., & McGann, J. P. (2017) · Journal of Neuroscience · doi:10.1523/jneurosci.2797-16.2017 · Cited by 47 · see citing works
“…amygdala-dependent experimental tasks, including fear conditioning (Li et al., 2008; Fletcher, 2012; Åhs et al., 2013; Kass et al., 2013d; Krusemark et al., 2013; Dias and Ressler, 2014; Morrison et al., 2015; Parma et al., 2015) and appetitive conditioning (Abraham et al., 2014) in both…”
BackgroundZhou, S., Wei, T., Liu, X., Liu, Y., Song, W., Que, X., Xing, Y., Wang, Z., & Tang, Y. (2023) · BMC Medicine · doi:10.1186/s12916-023-02952-1 · Cited by 42 · see citing works
“As this brain region is the core of the olfaction-emotion neural circuit, abnormal activation could lead to cacosmia and might further cause anxiety and depression in patients with COVID-19 [50, 51].”
BackgroundOlfactory-visual integration facilitates perception of subthreshold negative emotion
Novak, L. R., Gitelman, D. R., Schuyler, B. S., & Li, W. (2015) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2015.09.005 · Cited by 41 · see citing works
“Nevertheless, among all senses, olfaction holds a unique intimacy with the emotion system, and olfactory processing closely interacts with emotion processing (Yeshurun and Sobel, 2010; Krusemark et al., 2013).”
Self-citationImpaired sense of smell and altered olfactory system in RAG-1−∕− immunodeficient mice
Rattazzi, L., Cariboni, A. M., Poojara, R., Shoenfeld, Y., & D’Acquisto, F. (2015) · Frontiers in Neuroscience · doi:10.3389/fnins.2015.00318 · Cited by 42 · see citing works
“RAG-1−/− Immunodeficient Mice Have an Altered”
BackgroundFunctional Connectome Analyses Reveal the Human Olfactory Network Organization
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 · see citing works
“This design permits rapid odor delivery in the absence of tactile, thermal, or auditory confounds (Lorig et al., 1999; Krusemark et al., 2013; Novak et al., 2015).”
BackgroundSelf-citationClinical specificity profile for novel rapid acting antidepressant drugs
Scala, M., Fanelli, G., De Ronchi, D., Serretti, A., & Fabbri, C. (2023) · International Clinical Psychopharmacology · doi:10.1097/yic.0000000000000488 · Cited by 41 · see citing works
Bombini, M. F., Peres, F. A., Lapa, A. T., Sinicato, N. A., Quental, B. R., Pincelli, Á. D. S. M., Amaral, T. N., Gomes, C. C., del Rio, A. P., Marques-Neto, J. F., et al. (2018) · Autoimmunity Reviews · doi:10.1016/j.autrev.2018.02.002 · Cited by 40 · see citing works
Kaimal, G., Carroll-Haskins, K., Topoglu, Y., Ramakrishnan, A., Arslanbek, A., & Ayaz, H. (2021) · Art Therapy · doi:10.1080/07421656.2021.1957341 · Cited by 40 · see citing works
“Willander and Larsson (2006) demonstrated that memories induced by olfactory stimulation were associated with stronger feelings compared to other visual and auditory systems including relaxant effects and impacts on mood (Chen et al., 2020; Genc & Saritas, 2020; Krusemark et al., 2013).”
BackgroundAl-Zubaidi, A., Mertins, A., Heldmann, M., Jauch‐Chara, K., & Münte, T. F. (2019) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2019.00164 · Cited by 40 · see citing works
“The olfactory cortex (OLFC), whose activity was modulated by metabolic states as well, is involved in the experience and processing of negative affective states, including anxiety and depression (Krusemark et al., 2013).”
BackgroundPossible relation between olfaction and anxiety in healthy subjects
Takahashi, T., Itoh, H., Nishikawa, Y., Higuchi, Y., Nakamura, M., Sasabayashi, D., Nishiyama, S., Mizukami, Y., Masaoka, Y., & Suzuki, M. (2015) · Psychiatry and Clinical Neurosciences · doi:10.1111/pcn.12277 · Cited by 40 · see citing works
“Interestingly, a recent functional magnetic resonance imaging study proposed a neural circuitry model of anxiety-state-dependent olfactory processing, where induced anxiety strengthened functional connections between olfactory (piriform and orbitofrontal cortices) and emotion (amygdala and pregenual anterior cingulate…”
BackgroundPain, Smell, and Taste in Adults: A Narrative Review of Multisensory Perception and Interaction
Sandri, A., Cecchini, M. P., Riello, M., Zanini, A., Nocini, R., Fiorio, M., & Tinazzi, M. (2021) · Pain and Therapy · doi:10.1007/s40122-021-00247-y · Cited by 42 · see citing works
Aromas Influencing the GABAergic System
Hartley, N., & Mclachlan, C. (2022) · Molecules · doi:10.3390/molecules27082414 · Cited by 38 · see citing works
“The olfactory neuroanatomy is intertwined with the primary emotional areas, including the amygdala, hippocampus, and orbitofrontal cortex via extensive reciprocal axonal connections [7].”
BackgroundSadrian, B., & Wilson, D. A. (2015) · Frontiers in Neural Circuits · doi:10.3389/fncir.2015.00081 · Cited by 36 · see citing works
“Induction of anxiety results in a shift in valence evaluation of neutral odors in a negative direction (Krusemark et al., 2013).”
BackgroundExposure to Particulate Matter Air Pollution and Anosmia
Zhang, Z., Rowan, N. R., Pinto, J. M., London, N. R., Lane, A. P., Biswal, S. S., & Ramanathan, M. (2021) · JAMA Network Open · doi:10.1001/jamanetworkopen.2021.11606 · Cited by 35 · see citing works
The smell of “anxiety”: Behavioral modulation by experimental anosmia in zebrafish
de Abreu, M. S., Giacomini, A. C. V. V., Kalueff, A. V., & Barcellos, L. J. G. (2016) · Physiology & Behavior · doi:10.1016/j.physbeh.2016.01.030 · Cited by 35 · see citing works
“Finally, olfaction has long been strongly linked to emotional behavior in humans, especially since various olfactory deficits, such as anosmia, hypertrophic turbinates, nasal mucosal atrophy or chronic rhinosinusitis, all present with elevated fear and anxiety [2-3,27].”
BackgroundOlfactory functioning in panic disorder
Burón, E., Bulbena, A., & Bulbena‐Cabré, A. (2015) · Journal of Affective Disorders · doi:10.1016/j.jad.2015.01.049 · Cited by 33 · see citing works
Delplanque, S., Coppin, G., & Sander, D. (2017) · Springer eBooks · doi:10.1007/978-3-319-26932-0_40 · Cited by 32 · see citing works
Holmes, N. M., Raipuria, M., Qureshi, O. A., Killcross, S., & Westbrook, R. F. (2018) · eNeuro · doi:10.1523/eneuro.0381-17.2017 · Cited by 31 · see citing works
“…enhance activity in brain areas associated with early sensory processes (Sabatinelli et al., 2005; LaBar and Cabeza, 2006; Levita et al., 2015; Krusemark et al., 2013), as well as interactions between those areas and limbic regions associated with defensive reactions (Miskovic and Keil, 2012,…”
BackgroundKaimal, G., Carroll-Haskins, K., Ramakrishnan, A., Magsamen, S. H., Arslanbek, A., & Herres, J. L. (2020) · Frontiers in Psychology · doi:10.3389/fpsyg.2020.589461 · Cited by 31 · see citing works
Olfactory perceptual decision-making is biased by motivational state
Shanahan, L. K., Bhutani, S., & Kahnt, T. (2021) · PLoS Biology · doi:10.1371/journal.pbio.3001374 · Cited by 31 · see citing works
Incentive disengagement and the adaptive significance of frustrative nonreward
Papini, M. R., Guarino, S., Hagen, C. W., & Torres, C. (2022) · Learning & Behavior · doi:10.3758/s13420-022-00519-3 · Cited by 29 · see citing works
“Olfactory inputs connect profusely with additional brain areas involved in emotion, including the hippocampus, orbitofrontal cortex, piriform cortex, and anterior cingulate cortex (e.g., Krusemark et al., 2013).”
BackgroundHuman body odor increases familiarity for faces during encoding‐retrieval task
Cecchetto, C., Fischmeister, F. P. S., Gorkiewicz, S., Schuehly, W., Bagga, D., Parma, V., & Schöpf, V. (2020) · Human Brain Mapping · doi:10.1002/hbm.24920 · Cited by 28 · see citing works
Pizzoli, S. F. M., Monzani, D., Mazzocco, K., Maggioni, E., & Pravettoni, G. (2021) · Perspectives on Psychological Science · doi:10.1177/17456916211014196 · Cited by 31 · see citing works
“Olfaction can also adapt itself according to arousal levels and emotions (Krusemark et al., 2013; Pollatos et al., 2007); thus, there is a problem linked to the sensorial level of stimulations and real-time receptor adaptation.”
BackgroundChronic variable stress exposure in male Wistar rats affects the first step of olfactory detection
Raynaud, A., Meunier, N., Acquistapace, A., & Bombail, V. (2015) · Behavioural Brain Research · doi:10.1016/j.bbr.2015.05.013 · Cited by 26 · see citing works
Stress lowers the detection threshold for foul-smelling 2-mercaptoethanol
Pacharra, M., Schäper, M., Kleinbeck, S., Blaszkewicz, M., Wolf, O. T., & van Thriel, C. (2015) · Stress · doi:10.3109/10253890.2015.1105212 · Cited by 27 · see citing works
“The olfactory system is closely linked to emotion processing (Adolph & Pause, 2012; Krusemark et al., 2013) and one of its key functions is threat detection (Stevenson, 2010).”
Parallel processing of general and specific threat during early stages of perception
You, Y., & Li, W. (2015) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsv123 · Cited by 26 · see citing works
Self-citationLin, P., Lin, Y.-P., Chen, K., Yang, S., Shih, Y.-H., & Wang, P.-Y. (2021) · PLoS ONE · doi:10.1371/journal.pone.0249795 · Cited by 26 · see citing works
“Essential oils can be absorbed into the body through the digestive system, skin, or olfactory system with the response being fastest via the olfactory system [20,21].”
BackgroundSad man’s nose: Emotion induction and olfactory perception.
Flohr, E. L. R., Erwin, E., Croy, I., & Hummel, T. R. (2016) · Emotion · doi:10.1037/emo0000224 · Cited by 28 · see citing works
Shi, Z., Xi, L., Wang, Y., & Zhao, X. (2023) · Environmental Science & Technology · doi:10.1021/acs.est.3c04875 · Cited by 25 · see citing works
Neuroimaging of smell and taste
Olofsson, J., & Freiherr, J. (2019) · Handbook of clinical neurology · doi:10.1016/b978-0-444-63855-7.00017-4 · Cited by 25 · see citing works
A Scent of Anxiety: Olfactory Context Conditioning and its Influence on Social Cues
Kastner, A. K., Flohr, E. L. R., Pauli, P., & Wieser, M. J. (2015) · Chemical Senses · doi:10.1093/chemse/bjv067 · Cited by 24 · see citing works
Kafaei, M., Latifi, M., Burry, J., Ciorciari, J., Aminitabar, A., & Ji, K. (2025) · Building and Environment · doi:10.1016/j.buildenv.2025.112626 · Cited by 23 · see citing works
Pereira, A., Foz, F. B., & da Rocha, A. F. (2017) · Psychology of Consciousness Theory Research and Practice · doi:10.1037/cns0000115 · Cited by 23 · see citing works
Pattern differentiation and tuning shift in human sensory cortex underlie long-term threat memory
You, Y., Novak, L. R., Clancy, K. J., & Li, W. (2022) · Current Biology · doi:10.1016/j.cub.2022.02.076 · Cited by 25 · see citing works
Self-citationIntrinsic sensory disinhibition contributes to intrusive re-experiencing in combat veterans
Clancy, K. J., Albizu, A., Schmidt, N. B., & Li, W. (2020) · Scientific Reports · doi:10.1038/s41598-020-57963-2 · Cited by 23 · see citing works
Self-citationHuman Sensory Cortex Contributes to the Long-Term Storage of Aversive Conditioning
You, Y., Brown, J. C., & Li, W. (2021) · Journal of Neuroscience · doi:10.1523/jneurosci.2325-20.2021 · Cited by 23 · see citing works
“That is, stored representation of acquired threat in the sensory cortex can be activated by feedforward transmission of CSs, triggering threat encoding in the sensory cortex (Krusemark and Li, 2011; Kumar et al., 2012; Krusemark et al., 2013; Krusemark and Li, 2013; Kragel et al., 2019).”
Self-citationCentral olfactory processing in patients with disorders of consciousness
Nigri, A., Ferraro, S., Bruzzone, M. G., Nava, S., D’Incerti, L., Bertolino, N., Sattin, D., Leonardi, M., & Lundström, J. N. (2015) · European Journal of Neurology · doi:10.1111/ene.12907 · Cited by 23 · see citing works
“Of special interest for the study in DOC patients is that areas implicated in saliency processing (amygdala) and memory (hippocampus) are closely connected with the olfactory receptor [17], thus rendering it likely that olfaction is closely linked to emotional processing [18].”
BackgroundElevated Anxiety and Impaired Attention in Super-Smeller, Kv1.3 Knockout Mice
Huang, Z., Hoffman, C. A., Chelette, B. M., Thiebaud, N., & Fadool, D. A. (2018) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2018.00049 · Cited by 20 · see citing works
“In human subjects, Krusemark et al. (2013) interestingly were able to drive changes in anxiety levels to the extent that previously neutral or innocuous odorants became unpleasant and took longer to detect.”
BackgroundInfluentialEffects of Creative Thinking and Its Personality Determinants on Negative Emotion Regulation
Chiu, F.-C., Hsu, C.-C., Lin, Y.-N., Liu, C.-H., Chen, H.-C., & Lin, C.-H. (2018) · Psychological Reports · doi:10.1177/0033294118775973 · Cited by 23 · see citing works
Azuma, K., Uchiyama, I., Tanigawa, M., Bamba, I., Azuma, M., Takano, H., Yoshikawa, T., & Sakabe, K. (2015) · Environmental Health and Preventive Medicine · doi:10.1007/s12199-015-0448-4 · Cited by 22 · see citing works
“The olfactory sense has a unique intimacy with the emotion system, and the perception of smell is known to be dominated by emotion [41].”
In the Moment: Fostering Mindfulness and Reducing Stressors in the Healthcare Workplace
Valipoor, S., & Bosch, S. J. (2021) · HERD Health Environments Research & Design Journal · doi:10.1177/1937586720988243 · Cited by 23 · see citing works
“In regard to olfactory stimulus, while research shows that smells can have a powerful impact on human behavior (Krusemark et al., 2013), less is known about their types and acceptable exposure levels to avoid overstimulation.”
BackgroundEast, B. S., Fleming, G., Vervoordt, S. M., Shah, P., Sullivan, R. M., & Wilson, D. A. (2021) · Scientific Reports · doi:10.1038/s41598-021-01320-4 · Cited by 21 · see citing works
Capturing the Semantics of Smell: The Odeuropa Data Model for Olfactory Heritage Information
Lisena, P., Schwabe, D., van Erp, M., Raphaël Troncy, A., Tullett, W., Leemans, I., Marx, L., & Ehrich, S. (2022) · Lecture notes in computer science · doi:10.1007/978-3-031-06981-9_23 · Cited by 21 · see citing works
“As olfactory information goes straight from the nose, from the olfactory bulb, to the limbic system, the amygdala and hyp-pocampus, smells often evoke strong emotions and memories [32].”
BackgroundThreat Memory in the Sensory Cortex: Insights from Olfaction
Li, W., & Wilson, D. A. (2023) · The Neuroscientist · doi:10.1177/10738584221148994 · Cited by 21 · see citing works
Self-citationEffects of ZnSO4-induced peripheral anosmia on zebrafish behavior and physiology
de Abreu, M. S., Giacomini, A. C. V. V., Rodriguez, R., Kalueff, A. V., & Barcellos, L. J. G. (2016) · Behavioural Brain Research · doi:10.1016/j.bbr.2016.12.014 · Cited by 20 · see citing works
Lavender improves sleep through olfactory perception and GABAergic neurons of the central amygdala
Ren, Y.-L., Chu, W., Yang, X.-W., Xin, L., Gao, J.-X., Yan, G., Wang, C., Chen, Y.-N., Xie, J.-F., Spruyt, K., et al. (2024) · Journal of Ethnopharmacology · doi:10.1016/j.jep.2024.118942 · Cited by 19 · see citing works
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 19 · see citing works
“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 · see citing works
“…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 18 · see citing works
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 · see citing works
“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 · see citing works
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 · see citing works
Iokawa, K., Kohzuki, M., Sone, T., & Ebihara, S. (2017) · Complementary Therapies in Medicine · doi:10.1016/j.ctim.2017.11.009 · Cited by 16 · see citing works
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 · see citing works
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 · see citing works
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 15 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
“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 · see citing works
“…’ 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 · see citing works
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 · see citing works
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 · see citing works
“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 · see citing works
“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 · see citing works
“…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 · see citing works
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 · see citing works
Effect of scent on comfort of aircraft passengers
Yao, X., Song, Y., & Vink, P. (2020) · Work · doi:10.3233/wor-208025 · Cited by 11 · see citing works
“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 · see citing works
“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 11 · see citing works
“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 10 · see citing works
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 · see citing works
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 10 · see citing works
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 · see citing works
“However, the VR immersive experience can be easily disrupted by the hospital smell of disinfectant [23].”
Background
- 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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