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The Brain Circuitry Underlying the Temporal Evolution of Nausea in Humans
Open accessAbstract
Nausea is a universal human experience. It evolves slowly over time, and brain mechanisms underlying this evolution are not well understood. Our functional magnetic resonance imaging (fMRI) approach evaluated brain activity contributing to and arising from increasing motion sickness. Subjects rated transitions to increasing nausea, produced by visually induced vection within the fMRI environment. We evaluated parametrically increasing brain activity 1) precipitating increasing nausea and 2) following transition to stronger nausea. All subjects demonstrated visual stimulus-associated activation (P < 0.01) in primary and extrastriate visual cortices. In subjects experiencing motion sickness, increasing phasic activity preceding nausea was found in amygdala, putamen, and dorsal pons/locus ceruleus. Increasing sustained response following increased nausea was found in a broader network including insular, anterior cingulate, orbitofrontal, somatosensory and prefrontal cortices. Moreover, sustained anterior insula activation to strong nausea was correlated with midcingulate activation (r = 0.87), suggesting a closer linkage between these specific regions within the brain circuitry subserving nausea perception. Thus, while phasic activation in fear conditioning and noradrenergic brainstem regions precipitates transition to strong nausea, sustained activation following this transition occurs in a broader interoceptive, limbic, somatosensory, and cognitive network, reflecting the multiple dimensions of this aversive commonly occurring symptom.
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“Recently, the brain areas active during the development of nausea have been identified in imaging studies (Napadow et al. 2013; Sugiyama et al. 2011; Suzuki et al. 2012; Yates 1996a, b; Yates et al. 1995a, b; Yates and Bronstein 2005; Yates and Miller 2009).”
From Motion sickness: more than nausea and vomiting (2014) · cites this paper as Napadow et al. 2013
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“implicated in nausea and vomiting as indicated in Figure 1.(77) Indeed, aberrant sympathetic activation is associated with CVS and CHS.”
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“The cingulum area is related to motor control and cognition (Paus, 2001), pain and emotion (Vogt, 2005), and other symptoms like nausea (Napadow et al., 2013).”
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Self-citationZhou, W., Wang, J., Pan, L., Qi, R., Liu, P., Liu, J., & Cai, Y. (2017) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2017.00029 · Cited by 28
“Functional magnetic resonance imaging studies found that the amygdala was activated in humans experiencing motion sickness-induced nausea or mal de debarquement syndrome (Cha et al., 2012; Napadow et al., 2013).”
BackgroundWilcox, S. L., Ludwick, A., Lebel, A., & Borsook, D. (2017) · Cephalalgia · doi:10.1177/0333102417722570 · Cited by 28
Ruffle, J. K., Patel, A., Giampietro, V., Howard, M. A., Sanger, G. J., Andrews, P. L. R., Williams, S., Aziz, Q., & Farmer, A. D. (2019) · The Journal of Physiology · doi:10.1113/jp277474 · Cited by 29
“Using a priori selection of regions (Stern et al., 2011a; Napadow et al., 2012; Critchley & Harrison, 2013), 22 regions of interest (ROI) parcellation masks were generated using the Harvard-Oxford Cortical Structural Probability Atlas and FSLeyes (Smith et al.”
MethodPharmacogenetics of Chemotherapy-Induced Nausea and Vomiting
Sugino, S., & Janicki, P. K. (2015) · Pharmacogenomics · doi:10.2217/pgs.14.168 · Cited by 26
Endocannabinoid signaling in stress, nausea, and vomiting
DeVuono, M. V., Venkatesan, T., & Hillard, C. J. (2024) · Neurogastroenterology & Motility · doi:10.1111/nmo.14911 · Cited by 24
The Application and Pharmaceutical Development of Etomidate: Challenges and Strategies
Zhang, H., Wu, A., Nan, X., Yang, L., Zhang, D., Zhang, Z., & Liu, H. (2024) · Molecular Pharmaceutics · doi:10.1021/acs.molpharmaceut.4c00325 · Cited by 24
Analysis of Motion Sickness Associated Brain Activity Using fNIRS: A Driving Simulator Study
Zhang, C., Li, S., Li, Y., Li, S. E., & Nie, B. (2020) · IEEE Access · doi:10.1109/access.2020.3038039 · Cited by 24
“used fMRI to study motion sickness and found that the occurrence of motion sickness is related to the middle prefrontal cortex of the brain [47].”
MethodThe Effectiveness of Common Cannabis Products for Treatment of Nausea
Stith, S. S., Li, X., Orozco, J., et al. (2021) · Journal of Clinical Gastroenterology · doi:10.1097/mcg.0000000000001534 · Cited by 24
Aapro, M., Jordan, K., Scotté, F., Celio, L., Karthaus, M., & Roeland, E. J. (2022) · Current Cancer Drug Targets · doi:10.2174/1568009622666220513094352 · Cited by 24
“The pathophysiology of nausea is far less understood [17, 18], and because it is a subjective symptom, its assessment is an ongoing clinical challenge [19].”
BackgroundKovacic, K. K., & Lorenzo, C. D. (2015) · Journal of Pediatric Gastroenterology and Nutrition · doi:10.1097/mpg.0000000000001076 · Cited by 24
“Co experimentally induced nausea (motion induced) (13).”
ResultYu, Z., Lv, Y.-B., Song, L.-H., Liu, D., Huang, X.-L., Hu, X., Zuo, Z., Wang, Y., Yang, Q., Peng, J., et al. (2017) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2017.00124 · Cited by 24
“…et al., 2008, 2012; Borsook et al., 2016), cognitive function (Bossaerts, 2010; Wiech et al., 2010; Nieuwenhuys, 2012; James et al., 2013), selfregulation (Preuschoff et al., 2008), external sensation (Wright et al., 2004), and internal sensation (Fasold et al., 2002; Napadow et al., 2013).”
BackgroundBrain white matter microstructure is associated with susceptibility to motion‐induced nausea
Napadow, V., Sheehan, J., Kim, J., et al. (2013) · Neurogastroenterology & Motility · doi:10.1111/nmo.12084 · Cited by 22
Self-citationWei, Y., Okazaki, Y. O., So, R. H. Y., Chu, C. W., & Kitajo, K. (2019) · NeuroImage · doi:10.1016/j.neuroimage.2019.116028 · Cited by 22
Variants in the CNR1 gene predispose to headache with nausea in the presence of life stress
Juhász, G., Csépány, É., Magyar, M., Édes, A. E., Eszlári, N., Hullám, G., Antal, P., Kökönyei, G., Anderson, I. M., Deakin, J. F. W., et al. (2016) · Genes Brain & Behavior · doi:10.1111/gbb.12352 · Cited by 22
“A recent human functional magnetic resonance imaging (fMRI) study suggested that sustained nausea activates an extensive network of limbic, interoceptive and cognitive brain areas including the insular cortex and the anterior cingulate (Napadow et al. 2013).”
BackgroundInfluentialInter-hemispheric desynchronization of the human MT+ during visually induced motion sickness
Miyazaki, J., Yamamoto, H., Ichimura, Y., Yamashiro, H., Murase, T., Yamamoto, T., Umeda, M., & Higuchi, T. (2015) · Experimental Brain Research · doi:10.1007/s00221-015-4312-y · Cited by 22
“…the course of VIMS, 411 fMRI activity in right fronto-insular cortex (including the anterior insula) was correlated 412 with the severity of nausea (Napadow et al. 2012), and the white matter tract connecting 413 the right insular cortex and right MT+ was associated with VIMS susceptibility…”
InfluentialPaiar, F., Cristaudo, A., Gonnelli, A., et al. (2019) · Head & Neck · doi:10.1002/hed.25982 · Cited by 21
“Recent investigations using functional MRI techniques in healthy adults have shown that two areas of the brain involved in higher cognitive function and emotion, namely the medial prefrontal cortex and the pregenual anterior cingulate cortex, are positively correlated with an increase in heart rate during nausea, sugg…”
BackgroundCentral Nervous System Mechanisms of Nausea in Gastroparesis: An fMRI-Based Case–Control Study
Snodgrass, P., Sandoval, H., Calhoun, V. D., Ramos-Duran, L. R., Song, G., Sun, Y., Alvarado, B., Bashashati, M., Sarosiek, I., & McCallum, R. W. (2019) · Digestive Diseases and Sciences · doi:10.1007/s10620-019-05766-5 · Cited by 21
Ayoub, S. (2021) · The Atrium (University of Guelph) · doi:10.1007/s00213-020-05570-4
“The insular cortex is also essential for the sensation of nausea in humans (Penfield and Faulk 1955; Napadow et al. 2013; Sclocco et al. 2016) and rats (Contreras et al.”
BackgroundLi, N., Liu, L., Sun, M., et al. (2021) · BMC Anesthesiology · doi:10.1186/s12871-021-01449-9 · Cited by 20
Ishii, A., Tanaka, M., Iwamae, M., Kim, C., Yamano, E., & Watanabe, Y. (2013) · Behavioral and Brain Functions · doi:10.1186/1744-9081-9-24 · Cited by 21
“For example, inhalation of odorants producing a strong feeling of disgust caused activation in the insular cortex [31], nausea produced by visually induced circular vection resulted in activation in the insular cortex [32], and observing aversive pictures also activated the insular cortex [33].”
BackgroundEndocannabinoid Mechanisms Influencing Nausea
Sticht, M. A., Rock, E. M., Limebeer, C. L., & Parker, L. A. (2015) · International review of neurobiology · doi:10.1016/bs.irn.2015.09.001 · Cited by 20
Nalivaiko, E. (2018) · Handbook of clinical neurology · doi:10.1016/b978-0-444-63912-7.00027-8 · Cited by 19
Lu, D., Wang, Y., Zhao, T., et al. (2020) · BMC Neurology · doi:10.1186/s12883-020-01699-z · Cited by 20
RetractedHorn, C. C. (2016) · Springer eBooks · doi:10.1007/978-3-319-34076-0_2 · Cited by 19
Methodologic considerations for studies of chronic nausea and vomiting in adults and children
Hasler, W. L., Li, B. U. K., Koch, K. L., Parkman, H. P., Kovacic, K. K., & McCallum, R. W. (2016) · Autonomic Neuroscience · doi:10.1016/j.autneu.2016.08.001 · Cited by 19
Seifert, C. L., Schönbach, E. M., Zimmer, C., Förschler, A., Tölle, T. R., Feurer, R., Gempt, J., Papadopoulou, A., Magon, S., Sprenger, T., et al. (2016) · Cephalalgia · doi:10.1177/0333102416686342 · Cited by 19
“The authors further found that those subjects who experienced higher levels of nausea associated with the visual motion stimulus had greater activation in several non-visual gray matter regions, including the anterior insula and fronto-insular cortex (26).”
BackgroundRock, E. M., Moreno‐Sanz, G., Limebeer, C. L., Petrie, G. N., Angelini, R., Piomelli, D., & Parker, L. A. (2017) · British Journal of Pharmacology · doi:10.1111/bph.13980 · Cited by 19
“(2016) demonstrated that elevation of 2-AG by MAGL inhibition in the interoceptive insular cortex (IIC), a cortical site responsible for the experience of nausea (Penfield and Faulk, 1955; Napadow et al., 2013), reduces nauseainduced conditioned gaping in rats.”
BackgroundInfluentialNeural networks involved in nausea in adult humans: A systematic review
Varangot‐Reille, C., Sanger, G. J., Andrews, P. L. R., Herranz‐Gómez, A., Suso‐Martí, L., de la Nava, J., & Cuenca‐Martínez, F. (2022) · Autonomic Neuroscience · doi:10.1016/j.autneu.2022.103059 · Cited by 19
Mittelstädt, J. M., Wacker, J., & Stelling, D. (2018) · Human Factors The Journal of the Human Factors and Ergonomics Society · doi:10.1177/0018720818804382 · Cited by 17
“Investigations of brain activity underlying cybersickness revealed complex patterns of activation, including increased activation in the left amygdala, the pregenual anterior cingulate cortex, the anterior cingulate cortex (ACC), and the right anterior insula (Farmer et al., 2015; Napadow et al., 2013).”
BackgroundSpiegel, D. R., Pattison, A., Lyons, A. B., et al. (2017) · PubMed · Cited by 17
Ginger for treating nausea and vomiting: an overview of systematic reviews and meta-analyses
Li, Z., Wu, J., Song, J., & Wen, Y. (2024) · International Journal of Food Sciences and Nutrition · doi:10.1080/09637486.2023.2284647 · Cited by 17
“Multiple regions of the cerebral cortex become active during nausea, which supported by functional brain imaging research (Napadow et al. 2013).”
BackgroundKenward, H., Pelligand, L., & Elliott, J. (2014) · Experimental Brain Research · doi:10.1007/s00221-014-3961-6 · Cited by 16
“For both study 1 and 2, all dogs were given 0.9 % saline and mannitol infusions to reduce the nephrotoxic effects of cisplatin (Ogilvie et al. 1988) (Fig.”
BackgroundInfluential
Metadata
- Authors
- Napadow, V., Sheehan, J. D., Kim, J., LaCount, L. T., Park, K., Kaptchuk, T. J., Rosen, B. R., & Kuo, B.
- Affiliations
- Harvard University (US)
- Massachusetts General Hospital (US)
- Kyung Hee University (KR)
- Beth Israel Deaconess Medical Center (US)
- Venue
- Cerebral Cortex
- Publisher
- Oxford University Press (OUP)
- Published
- 2012-04-02
- Volume
- 23
- Issue
- 4
- Pages
- 806-813
- ISSN
- 1047-3211 (ISSN-L)
- 1460-2199
- PMC
- PMC3593575
- OpenAlex
- W2147691780
- Semantic Scholar
- 0a06a06e294f3469f9768684508df0ae84ee9339
- Cited by
- 215
- References
- 55
- Citations by year
- 2026: 20 · 2025: 7 · 2024: 12 · 2023: 14 · 2022: 14 · 2021: 11 · 2020: 18 · 2019: 19 · 2018: 14 · 2017: 15 · 2016: 27 · 2015: 14 · 2014: 14 · 2013: 13 · 2012: 2
- FWCI
- 6.91
- Type
- journal article
- Language
- en
- Open access
- green
- europepmc.org
- Locations
- Cerebral Cortex (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institute of Diabetes and Digestive and Kidney Diseases (K23DK069614)
- National Center for Research Resources (P41-RR-14075, UL1RR025758, P41RR014075)
- National Center for Complementary and Integrative Health (R01AT004714, F05AT003770, K24AT004095, K01AT002166, P01AT002048)
- Topics
- Life Sciences › Neuroscience › Neurology › Vestibular and auditory disorders
- Health Sciences › Medicine › Surgery › Nausea and vomiting management
- Physical Sciences › Computer Science › Human-Computer Interaction › Virtual Reality Applications and Impacts
- Keywords
- nausea, motion sickness, brain circuits, amygdala, anterior insula, anterior cingulate cortex, locus coeruleus, interoception, noradrenergic system, fear conditioning, somatosensory cortex, orbitofrontal cortex
- MeSH terms
- Adult, Brain, Brain Mapping, Female, Humans, Image Processing, Computer-Assisted, Magnetic Resonance Imaging, Middle Aged, Motion Perception, Nausea, Nerve Net, Neural Pathways, Oxygen, Photic Stimulation, Reaction Time, Young Adult
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