Advertisement

Neural networks involved in nausea in adult humans: A systematic review

Published:December 19, 2022DOI:https://doi.org/10.1016/j.autneu.2022.103059

      Highlights

      • A systematic review of brain imaging studies identifies areas related with nausea.
      • Inferior frontal gyrus, anterior insula and cingulate cortex were most commonly activated.
      • Basal ganglia (e.g., putamen) structures were also consistently activated.
      • Some evidence for lateralization was identified (e.g., left inferior frontal gyrus).
      • Results are discussed in relation to visceral sensations, study limitations and research lacunae.

      Abstract

      Nausea is a common clinical symptom, poorly managed with anti-emetic drugs. To identify potential brain regions which may be therapeutic targets we systematically reviewed brain imaging in subjects reporting nausea. The systematic review followed PRISMA statements with methodological quality (MINORS) and risk of bias (ROBINS-I) assessed. Irrespective of the nauseagenic stimulus the common (but not only) cortical structures activated were the inferior frontal gyrus (IFG), the anterior cingulate cortex (ACC) and the anterior insula (AIns) with some evidence for lateralization (Left-IFG, Right-AIns, Right-ACC). Basal ganglia structures (e.g., putamen) were also consistently activated. Inactivation was rarely reported but occurred mainly in the cerebellum and occipital lobe. During nausea, functional connectivity increased, mainly between the posterior and mid- cingulate cortex. Limitations include, a paucity of studies and stimuli, subject demographics, inconsistent definition and measurement of nausea. Structures implicated in nausea are discussed in the context of knowledge of central pathways for interoception, emotion and autonomic control. Comparisons are made between nausea and other aversive sensations as multimodal aversive conscious experiences.

      Graphical abstract

      Keywords

      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'

      Subscribe:

      Subscribe to Autonomic Neuroscience: Basic and Clinical
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

        • Aapro M.
        CINV: still troubling patients after all these years.
        Support Care Cancer. 2018; 26: 5-9https://doi.org/10.1007/s00520-018-4131-3
        • Allaire J.J.
        • Ellis P.
        • Gandrud C.
        • Kuo K.
        • Lewis B.W.
        • Owen J.
        • Russell K.
        • Rogers J.
        • Sese C.
        • Yetman C.
        NetworkD3 package.
        (accessed 10.10.21)
        • Andrews P.L.R.
        • Sanger G.J.
        Nausea and the quest for the perfect anti-emetic.
        Eur. J. Pharmacol. 2014; 722: 108-121https://doi.org/10.1016/j.ejphar.2013.09.072
        • Apfel C.C.
        • Kranke P.
        • Greim C.A.
        • Roewer N.
        What can be expected from risk scores for predicting postoperative nausea and vomiting?.
        Br. J. Anaesth. 2001; 86: 822-827https://doi.org/10.1093/bja/86.6.822
        • Arsalan Naqvi S.A.
        • Badruddin N.
        • Jatoi M.A.
        • Malik A.S.
        • Hazabbah W.
        • Abdullah B.
        EEG based time and frequency dynamics analysis of visually induced motion sickness (VIMS).
        Australas. Phys. Eng. Sci. Med. 2015; 38: 721-729https://doi.org/10.1007/s13246-015-0379-9
        • Baars B.J.
        Global workspace theory of consciousness: toward a cognitive neuroscience of human experience.
        Prog. Brain Res. 2005; 150: 45-53https://doi.org/10.1016/S0079-6123(05)50004-9
        • Barrett L.F.
        • Simmons W.K.
        Interoceptive predictions in the brain.
        Nat. Rev. Neurosci. 2015; 16: 419-429https://doi.org/10.1038/nrn3950
        • Beissner F.
        • Meissner K.
        • Bär K.-J.
        • Napadow V.
        The autonomic brain: an activation likelihood estimation meta-analysis for central processing of autonomic function.
        J. Neurosci. 2013; 33: 10503-10511https://doi.org/10.1523/JNEUROSCI.1103-13.2013
        • Benarroch E.E.
        The central autonomic network: functional organization, dysfunction, and perspective.
        Mayo Clin. Proc. 1993; 68: 988-1001https://doi.org/10.1016/s0025-6196(12)62272-1
        • Blanke O.
        Multisensory brain mechanisms of bodily self-consciousness.
        Nat. Rev. Neurosci. 2012; 13: 556-571https://doi.org/10.1038/nrn3292
        • Blasco T.
        • Pallarés C.
        • Alonso C.
        • López López J.J.
        The role of anxiety and adaptation to illness in the intensity of postchemotherapy nausea in cancer patients.
        Span. J. Psychol. 2000; 3: 47-52https://doi.org/10.1017/s1138741600005539
        • Borsook D.
        • Upadhyay J.
        • Klimas M.
        • Schwarz A.J.
        • Coimbra A.
        • Baumgartner R.
        • George E.
        • Potter W.Z.
        • Large T.
        • Bleakman D.
        • Evelhoch J.
        • Iyengar S.
        • Becerra L.
        • Hargreaves R.J.
        Decision-making using fMRI in clinical drug development: revisiting NK-1 receptor antagonists for pain.
        Drug Discov. Today. 2012; 17: 964-973https://doi.org/10.1016/j.drudis.2012.05.004
        • Camilleri M.
        • Parkman H.P.
        • Shafi M.A.
        • Abell T.L.
        • Gerson L.
        Clinical guideline: management of gastroparesis.
        Am. J. Gastroenterol. 2013; 108 (quiz 38): 18-37https://doi.org/10.1038/ajg.2012.373
        • Cao Z.
        • Liu X.
        • Ju Y.
        • Zhao X.
        Neuroimaging studies in persistent postural-perceptual dizziness and related disease: a systematic review.
        J. Neurol. 2021; https://doi.org/10.1007/s00415-021-10558-x
        • Carlin J.L.
        • Lieberman V.R.
        • Dahal A.
        • Keefe M.S.
        • Xiao C.
        • Birznieks G.
        • Abell T.L.
        • Lembo A.
        • Parkman H.P.
        • Polymeropoulos M.H.
        Efficacy and safety of tradipitant in patients with diabetic and idiopathic gastroparesis in a randomized, placebo-controlled trial.
        Gastroenterology. 2021; 160 (e4): 76-87https://doi.org/10.1053/j.gastro.2020.07.029
        • Ceunen E.
        • Vlaeyen J.W.S.
        • Van Diest I.
        On the origin of interoception.
        Front. Psychol. 2016; https://doi.org/10.3389/fpsyg.2016.00743
        • Chen Y.-C.
        • Duann J.-R.
        • Chuang S.-W.
        • Lin C.-L.
        • Ko L.-W.
        • Jung T.-P.
        • Lin C.-T.
        Spatial and temporal EEG dynamics of motion sickness.
        NeuroImage. 2010; 49: 2862-2870https://doi.org/10.1016/j.neuroimage.2009.10.005
        • Chuang S.-W.
        • Chuang C.-H.
        • Yu Y.-H.
        • King J.-T.
        • Lin C.-T.
        EEG alpha and gamma modulators mediate motion sickness-related spectral responses.
        Int. J. Neural Syst. 2016; 26: 1650007https://doi.org/10.1142/S0129065716500076
        • Cicchetti D.V.
        • Allison T.
        A new procedure for assessing reliability of scoring EEG sleep recordings.
        Am. J. EEG Technol. 1971; 11: 101-110https://doi.org/10.1080/00029238.1971.11080840
        • Cohen M.X.
        Analyzing Neural Time Series Data: Theory and Practice.
        1st ed. The MIT Press, Cambridge, MA2014
        • Critchley H.D.
        • Harrison N.A.
        Visceral influences on brain and behavior.
        Neuron. 2013; 77: 624-638https://doi.org/10.1016/j.neuron.2013.02.008
        • Dehaene S.
        • Naccache L.
        • Cohen L.
        • Bihan D.Le
        • Mangin J.-F.
        • Poline J.-B.
        • Rivière D.
        Cerebral mechanisms of word masking and unconscious repetition priming.
        Nat. Neurosci. 2001; 4: 752-758https://doi.org/10.1038/89551
        • Desbiens N.A.
        • Mueller-Rizner N.
        • Connors A.F.
        • Wenger N.S.
        The relationship of nausea and dyspnea to pain in seriously ill patients.
        Pain. 1997; 71: 149-156https://doi.org/10.1016/S0304-3959(97)03353-8
        • Desikan R.S.
        • Ségonne F.
        • Fischl B.
        • Quinn B.T.
        • Dickerson B.C.
        • Blacker D.
        • Buckner R.L.
        • Dale A.M.
        • Maguire R.P.
        • Hyman B.T.
        • Albert M.S.
        • Killiany R.J.
        An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest.
        NeuroImage. 2006; 31: 968-980https://doi.org/10.1016/j.neuroimage.2006.01.021
        • Devinsky O.
        • Morrell M.J.
        • Vogt B.A.
        Contributions of anterior cingulate cortex to behaviour.
        Brain. 1995; 118: 279-306https://doi.org/10.1093/brain/118.1.279
        • Du J.
        • Rolls E.T.
        • Cheng W.
        • Li Y.
        • Gong W.
        • Qiu J.
        • Feng J.
        Functional connectivity of the orbitofrontal cortex, anterior cingulate cortex, and inferior frontal gyrus in humans.
        Cortex. 2020; 123: 185-199https://doi.org/10.1016/j.cortex.2019.10.012
        • Escobar Y.
        • Cajaraville G.
        • Virizuela J.A.
        • Álvarez R.
        • Muñoz A.
        • Olariaga O.
        • Tamés M.J.
        • Muros B.
        • Lecumberri M.J.
        • Feliu J.
        • Martínez P.
        • Adansa J.C.
        • Martínez M.J.
        • López R.
        • Blasco A.
        • Gascón P.
        • Calvo V.
        • Luna P.
        • Montalar J.
        • Del Barrio P.
        • Tornamira M.V.
        Incidence of chemotherapy-induced nausea and vomiting with moderately emetogenic chemotherapy: ADVICE (Actual data of vomiting incidence by chemotherapy Evaluation) study.
        Support Care Cancer. 2015; 23: 2833-2840https://doi.org/10.1007/s00520-015-2809-3
        • Evans K.C.
        • Banzett R.B.
        • Adams L.
        • McKay L.
        • Frackowiak R.S.J.
        • Corfield D.R.
        BOLD fMRI identifies limbic, paralimbic, and cerebellar activation during air hunger.
        J. Neurophysiol. 2002; 88: 1500-1511https://doi.org/10.1152/jn.2002.88.3.1500
        • Farmer A.D.
        • Ban V.F.
        • Coen S.J.
        • Sanger G.J.
        • Barker G.J.
        • Gresty M.A.
        • Giampietro V.P.
        • Williams S.C.
        • Webb D.L.
        • Hellström P.M.
        • Andrews P.L.R.
        • Aziz Q.
        Visually induced nausea causes characteristic changes in cerebral, autonomic and endocrine function in humans.
        J. Physiol. 2015; 593: 1183-1196https://doi.org/10.1113/jphysiol.2014.284240
        • Fischl B.
        • Salat D.H.
        • Busa E.
        • Albert M.
        • Dieterich M.
        • Haselgrove C.
        • Van Der Kouwe A.
        • Killiany R.
        • Kennedy D.
        • Klaveness S.
        • Montillo A.
        • Makris N.
        • Rosen B.
        • Dale A.M.
        Whole brain segmentation: automated labeling of neuroanatomical structures in the human brain.
        Neuron. 2002; 33: 341-355https://doi.org/10.1016/S0896-6273(02)00569-X
        • Fleisher D.R.
        The cyclic vomiting syndrome described.
        J. Pediatr. Gastroenterol. Nutr. 1995; 21: S1-S5https://doi.org/10.1097/00005176-199501001-00003
        • Fortunato J.E.
        • Laurienti P.J.
        • Wagoner A.L.
        • Shaltout H.A.
        • Diz D.I.
        • Silfer J.L.
        • Burdette J.H.
        Children with chronic nausea and orthostatic intolerance have unique brain network organization: a case-control trial.
        Neurogastroenterol. Motil. Off. J. Eur. Gastrointest. Motil. Soc. 2022; 34e14271https://doi.org/10.1111/nmo.14271
        • Foubert J.
        • Vaessen G.
        Nausea: the neglected symptom?.
        Eur. J. Oncol. Nurs. 2005; 9: 21-32https://doi.org/10.1016/j.ejon.2004.03.006
        • Fredrikson M.
        • Hursti T.
        • Wik G.
        Neural networks in chemotherapy-induced delayed nausea - a pilot-study using positron emission tomography.
        Oncol. Rep. 1995; 2: 1001-1003https://doi.org/10.3892/or.2.6.1001
        • Furlan A.D.
        • Pennick V.
        • Bombardier C.
        • van Tulder M.
        2009 updated method guidelines for systematic reviews in the Cochrane Back Review Group.
        Spine (Phila. Pa. 1976). 2009; 34: 1929-1941https://doi.org/10.1097/BRS.0b013e3181b1c99f
        • Gavgani A.M.
        • Wong R.H.X.
        • Howe P.R.C.
        • Hodgson D.M.
        • Walker F.R.
        • Nalivaiko E.
        Cybersickness-related changes in brain hemodynamics: a pilot study comparing transcranial doppler and near-infrared spectroscopy assessments during a virtual ride on a roller coaster.
        Physiol. Behav. 2018; 191: 56-64https://doi.org/10.1016/j.physbeh.2018.04.007
        • Geeraerts B.
        • Van Oudenhove L.
        • Dupont P.
        • Vanderghinste D.
        • Bormans G.
        • Van Laere K.
        • Tack J.
        Different regional brain activity during physiological gastric distension compared to balloon distension: a H2 15O-PET study.
        Neurogastroenterol. Motil. 2011; 23: 533-e203https://doi.org/10.1111/j.1365-2982.2010.01642.x
        • Golding J.F.
        Motion sickness.
        in: Furman J.M. Lempert T. Handbook of Clinical Neurology. Neuro-Otology. Elsevier, 2016: 371-390
        • Griffin A.M.
        • Butow P.N.
        • Coates A.S.
        • Childs A.M.
        • Ellis P.M.
        • Dunn S.M.
        • Tattersall M.H.N.
        On the receiving end V : patient perceptions of the side effects of cancer chemotherapy in 1993.
        Ann. Oncol. 1996; 7: 189-195https://doi.org/10.1093/oxfordjournals.annonc.a010548
        • Güntürkün O.
        • Ströckens F.
        • Ocklenburg S.
        Brain lateralization: a comparative perspective.
        Physiol. Rev. 2020; 100: 1019-1063https://doi.org/10.1152/physrev.00006.2019
        • Haile A.
        • Watts M.
        • Aichner S.
        • Stahlberg F.
        • Hoffmann V.
        • Tschoep M.H.
        • Meissner K.
        Central correlates of placebo effects in nausea differ between men and women.
        Brain Behav. 2022; 12e2685https://doi.org/10.1002/brb3.2685
        • Harrison N.A.
        • Gray M.A.
        • Gianaros P.J.
        • Critchley H.D.
        The embodiment of emotional feelings in the brain.
        J. Neurosci. 2010; 30: 12878-12884https://doi.org/10.1523/JNEUROSCI.1725-10.2010
        • van den Heuvel M.P.
        • Sporns O.
        Rich-club organization of the human connectome.
        J. Neurosci. 2011; 31: 15775-15786https://doi.org/10.1523/JNEUROSCI.3539-11.2011
        • Higgins J.
        • Green S.
        Cochrane Handbook for Systematic Reviews of Interventions Version 5.1.0[M].
        Wiley-Blackwell, 2008
        • Holtz Y.
        Sankey Diagram.
        (accessed 10.10.21)
        • Horn C.C.
        Why is the neurobiology of nausea and vomiting so important?.
        Appetite. 2008; 50: 430-434https://doi.org/10.1016/j.appet.2007.09.015
        • Hromatka B.S.
        • Tung J.Y.
        • Kiefer A.K.
        • Do C.B.
        • Hinds D.A.
        • Eriksson N.
        Genetic variants associated with motion sickness point to roles for inner ear development, neurological processes and glucose homeostasis.
        Hum. Mol. Genet. 2015; 24: 2700-2708https://doi.org/10.1093/hmg/ddv028
        • Huizinga J.D.
        Commentary: phase-amplitude coupling at the organism level: the amplitude of spontaneous alpha rhythm fluctuations varies with the phase of the infra-slow gastric basal rhythm.
        Front. Neurosci. 2017; https://doi.org/10.3389/fnins.2017.00102
        • Jensen K.B.
        • Regenbogen C.
        • Ohse M.C.
        • Frasnelli J.
        • Freiherr J.
        • Lundström J.N.
        Brain activations during pain: a neuroimaging meta-analysis of patients with pain and healthy controls.
        Pain. 2016; 157: 1279-1286https://doi.org/10.1097/j.pain.0000000000000517
        • Kilpatrick L.
        • Cahill L.
        Amygdala modulation of parahippocampal and frontal regions during emotionally influenced memory storage.
        NeuroImage. 2003; 20: 2091-2099https://doi.org/10.1016/j.neuroimage.2003.08.006
        • Kim J.
        • Napadow V.
        • Kuo B.
        • Barbieri R.
        A combined HRV-fMRI approach to assess cortical control of cardiovagal modulation by motion sickness.
        in: 2011 Annual International Conference of the IEEE Engineering in Medicine and Biology Society. IEEE, 2011: 2825-2828https://doi.org/10.1109/IEMBS.2011.6090781
        • Koch K.L.
        • Hasler W.L.
        Nausea and vomiting: Diagnosis and Treatment.
        Springer International Publishing, Switzerland2017
        • Koch A.
        • Cascorbi I.
        • Westhofen M.
        • Dafotakis M.
        • Klapa S.
        • Kuhtz-Buschbeck J.P.
        The neurophysiology and treatment of motion sickness.
        Dtsch. Arztebl. Int. 2018; 115: 687-696https://doi.org/10.3238/arztebl.2018.0687
        • von Leupoldt A.
        • Sommer T.
        • Kegat S.
        • Baumann H.J.
        • Klose H.
        • Dahme B.
        • Büchel C.
        Dyspnea and pain share emotion-related brain network.
        NeuroImage. 2009; 48: 200-206https://doi.org/10.1016/j.neuroimage.2009.06.015
        • Li B.U.
        • Murray R.D.
        • Heitlinger L.A.
        • Robbins J.L.
        • Hayes J.R.
        Is cyclic vomiting syndrome related to migraine?.
        J. Pediatr. 1999; 134: 567-572https://doi.org/10.1016/s0022-3476(99)70242-8
        • Li D.
        • Zucker N.L.
        • Kragel P.A.
        • Covington V.E.
        • LaBar K.S.
        Adolescent development of insula-dependent interoceptive regulation.
        Dev. Sci. 2017; 20https://doi.org/10.1111/desc.12438
        • Liakakis G.
        • Nickel J.
        • Seitz R.J.
        Diversity of the inferior frontal gyrus—a meta-analysis of neuroimaging studies.
        Behav. Brain Res. 2011; 225: 341-347https://doi.org/10.1016/j.bbr.2011.06.022
        • Lin C.-T.
        • Chuang S.-W.
        • Chen Y.-C.
        • Ko L.-W.
        • Liang S.-F.
        • Jung T.-P.
        EEG effects of motion sickness induced in a dynamic virtual reality environment.
        in: Annu. Int. Conf. IEEE Eng. Med. Biol. Soc. IEEE Eng. Med. Biol. Soc. Annu. Int. Conf. 2007. 2007: 3872-3875https://doi.org/10.1109/IEMBS.2007.4353178
        • Luck S.J.
        An Introduction to the Event-related Potential Technique.
        2nd ed. The MIT Press, 2014
        • Malamood M.
        • Roberts A.
        • Kataria R.
        • Parkman H.P.
        • Schey R.
        Mirtazapine for symptom control in refractory gastroparesis.
        Drug Des. Devel. Ther. 2017; 11: 1035-1041https://doi.org/10.2147/DDDT.S125743
        • Maniyar F.H.
        • Sprenger T.
        • Schankin C.
        • Goadsby P.J.
        The origin of nausea in migraine–a PET study.
        J. Headache Pain. 2014; 15: 1-6https://doi.org/10.1186/1129-2377-15-84
        • McGuire P.K.
        • Silbersweig D.A.
        • Murray R.M.
        • David A.S.
        • Frackowiak R.S.J.
        • Frith C.D.
        Functional anatomy of inner speech and auditory verbal imagery.
        Psychol. Med. 1996; 26: 29-38https://doi.org/10.1017/S0033291700033699
        • McHugh M.L.
        Interrater reliability: the kappa statistic.
        Biochem. Medica. 2012; 22: 276-282https://doi.org/10.11613/bm.2012.031
        • Menon V.
        • Crottaz-Herbette S.
        Combined EEG and fMRI studies of human brain function.
        Int. Rev. Neurobiol. 2005; 66: 291-321https://doi.org/10.1016/S0074-7742(05)66010-2
        • Menon V.
        • Uddin L.Q.
        Saliency, switching, attention and control: a network model of insula function.
        Brain Struct. Funct. 2010; 214: 655-667https://doi.org/10.1007/s00429-010-0262-0
        • Miller A.D.
        • Rowley H.A.
        • Roberts T.P.
        • Kucharczyk J.
        Human cortical activity during vestibular- and drug-induced nausea detected using MSI.
        Ann. N. Y. Acad. Sci. 1996; 781: 670-672https://doi.org/10.1111/j.1749-6632.1996.tb15755.x
        • Molassiotis A.
        Time to re-think the olanzapine dose.
        Lancet. Oncol. 2020; 21: 189-190https://doi.org/10.1016/S1470-2045(19)30791-0
        • Mowinckel A.M.
        • Vidal-Piñeiro D.
        Visualization of brain statistics with R packages ggseg and ggseg3d.
        Adv. Methods Pract. Psychol. Sci. 2020; 3: 466-483https://doi.org/10.1177/2515245920928009
        • Müller V.I.
        • Cieslik E.C.
        • Laird A.R.
        • Fox P.T.
        • Radua J.
        • Mataix-Cols D.
        • Tench C.R.
        • Yarkoni T.
        • Nichols T.E.
        • Turkeltaub P.E.
        • Wager T.D.
        • Eickhoff S.B.
        Ten simple rules for neuroimaging meta-analysis.
        Neurosci. Biobehav. Rev. 2018; 84: 151-161https://doi.org/10.1016/j.neubiorev.2017.11.012
        • Nakae T.
        • Matsumoto R.
        • Kunieda T.
        • Arakawa Y.
        • Kobayashi K.
        • Shimotake A.
        • Yamao Y.
        • Kikuchi T.
        • Aso T.
        • Matsuhashi M.
        • Yoshida K.
        • Ikeda A.
        • Takahashi R.
        • Lambon Ralph M.A.
        • Miyamoto S.
        Connectivity gradient in the human left inferior frontal gyrus: intraoperative cortico-cortical evoked potential study.
        Cereb. Cortex. 2020; 30: 4633-4650https://doi.org/10.1093/cercor/bhaa065
        • Napadow V.
        • Sheehan J.D.
        • Kim J.
        • LaCount L.T.
        • Park K.
        • Kaptchuk T.J.
        • Rosen B.R.
        • Kuo B.
        The brain circuitry underlying the temporal evolution of nausea in humans.
        Cereb. Cortex. 2013; 23: 806-813https://doi.org/10.1093/cercor/bhs073
        • National Cancer Institute
        Nausea.
        (accessed 10.7.21)
        • Olver I.N.
        • Eliott J.A.
        • Koczwara B.
        A qualitative study investigating chemotherapy-induced nausea as a symptom cluster.
        Support Care Cancer. 2014; 22: 2749-2756https://doi.org/10.1007/s00520-014-2276-2
        • Oosterwijk S.
        • Lindquist K.A.
        • Anderson E.
        • Dautoff R.
        • Moriguchi Y.
        • Barrett L.F.
        States of mind: emotions, body feelings, and thoughts share distributed neural networks.
        NeuroImage. 2012; 62: 2110-2128https://doi.org/10.1016/j.neuroimage.2012.05.079
        • Ouzzani M.
        • Hammady H.
        • Fedorowicz Z.
        • Elmagarmid A.
        Rayyan—a web and mobile app for systematic reviews.
        Syst. Rev. 2016; 5: 210https://doi.org/10.1186/s13643-016-0384-4
        • Page M.J.
        • McKenzie J.E.
        • Bossuyt P.M.
        • Boutron I.
        • Hoffmann T.C.
        • Mulrow C.D.
        • Shamseer L.
        • Tetzlaff J.M.
        • Akl E.A.
        • Brennan S.E.
        • Chou R.
        • Glanville J.
        • Grimshaw J.M.
        • Hróbjartsson A.
        • Lalu M.M.
        • Li T.
        • Loder E.W.
        • Mayo-Wilson E.
        • McDonald S.
        • McGuinness L.A.
        • Stewart L.A.
        • Thomas J.
        • Tricco A.C.
        • Welch V.A.
        • Whiting P.
        • Moher D.
        The PRISMA 2020 statement: an updated guideline for reporting systematic reviews.
        BMJ. 2021; 372n71https://doi.org/10.1136/bmj.n71
        • Park J.-R.
        • Lim D.-W.
        • Lee S.-Y.
        • Lee H.-W.
        • Choi M.-H.
        • Chung S.-C.
        Long-term study of simulator sickness: differences in EEG response due to individual sensitivity.
        Int. J. Neurosci. 2008; 118: 857-865https://doi.org/10.1080/00207450701239459
        • Parkman H.P.
        • Van Natta M.L.
        • Abell T.L.
        • McCallum R.W.
        • Sarosiek I.
        • Nguyen L.
        • Snape W.J.
        • Koch K.L.
        • Hasler W.L.
        • Farrugia G.
        • Lee L.
        • Unalp-Arida A.
        • Tonascia J.
        • Hamilton F.
        • Pasricha P.J.
        Effect of nortriptyline on symptoms of idiopathic gastroparesis: the NORIG randomized clinical trial.
        JAMA. 2013; 310: 2640-2649https://doi.org/10.1001/jama.2013.282833
        • Pasricha P.J.
        • Snape W.
        Toward a better drug for gastroparesis: the problem with a moving target.
        Gastroenterology. 2016; https://doi.org/10.1053/j.gastro.2016.05.019
        • Pasricha P.J.
        • Yates K.P.
        • Sarosiek I.
        • McCallum R.W.
        • Abell T.L.
        • Koch K.L.
        • Nguyen L.A.B.
        • Snape W.J.
        • Hasler W.L.
        • Clarke J.O.
        • Dhalla S.
        • Stein E.M.
        • Lee L.A.
        • Miriel L.A.
        • Van Natta M.L.
        • Grover M.
        • Farrugia G.
        • Tonascia J.
        • Hamilton F.A.
        • Parkman H.P.
        Aprepitant has mixed effects on nausea and reduces other symptoms in patients with gastroparesis and related disorders.
        Gastroenterology. 2018; 154: 65-76.e11https://doi.org/10.1053/j.gastro.2017.08.033
        • Pedersen T.L.
        patchwork: The Composer of Plots.
        (accessed 10.10.21)
        • Peyrot des Gachons C.
        • Beauchamp G.K.
        • Stern R.M.
        • Koch K.L.
        • Breslin P.A.S.
        Bitter taste induces nausea.
        Curr. Biol. 2011; 21: R247-R248https://doi.org/10.1016/j.cub.2011.02.028
        • Quigley E.M.M.
        • Hasler W.L.
        • Parkman H.P.
        AGA technical review on nausea and vomiting.
        Gastroenterology. 2001; 120: 263-286https://doi.org/10.1053/gast.2001.20516
        • R Core Team
        R: A Language and Environment for Statistical Computing.
        2021
        • Raja S.N.
        • Carr D.B.
        • Cohen M.
        • Finnerup N.B.
        • Flor H.
        • Gibson S.
        • Keefe F.J.
        • Mogil J.S.
        • Ringkamp M.
        • Sluka K.A.
        • Song X.-J.
        • Stevens B.
        • Sullivan M.D.
        • Tutelman P.R.
        • Ushida T.
        • Vader K.
        The revised International Association for the Study of Pain definition of pain: concepts, challenges, and compromises.
        Pain. 2020; 161https://doi.org/10.1097/j.pain.0000000000001939
        • Richter C.G.
        • Babo-Rebelo M.
        • Schwartz D.
        • Tallon-Baudry C.
        Phase-amplitude coupling at the organism level: the amplitude of spontaneous alpha rhythm fluctuations varies with the phase of the infra-slow gastric basal rhythm.
        NeuroImage. 2017; 146: 951-958https://doi.org/10.1016/j.neuroimage.2016.08.043
        • Rolls E.T.
        The Brain and Emotion.
        Oxford University Press (OUP), Oxford, England1999
        • RStudio Team
        RStudio: Integrated Development Environment for R.
        2021
        • Ruffle J.K.
        • Coen S.J.
        • Giampietro V.
        • Williams S.C.R.
        • Apkarian A.V.
        • Farmer A.D.
        • Aziz Q.
        Morphology of subcortical brain nuclei is associated with autonomic function in healthy humans.
        Hum. Brain Mapp. 2018; 39: 381-392https://doi.org/10.1002/hbm.23850
        • Ruffle J.K.
        • Patel A.
        • Giampietro V.
        • Howard M.A.
        • Sanger G.J.
        • Andrews P.L.R.
        • Williams S.C.R.
        • Aziz Q.
        • Farmer A.D.
        Functional brain networks and neuroanatomy underpinning nausea severity can predict nausea susceptibility using machine learning.
        J. Physiol. 2019; 597: 1517-1529https://doi.org/10.1113/JP277474
        • Sanger G.J.
        • Andrews P.L.R.
        Treatment of nausea and vomiting: gaps in our knowledge.
        Auton. Neurosci. Basic Clin. 2006; 129: 3-16https://doi.org/10.1016/j.autneu.2006.07.009
        • Sanger G.J.
        • Andrews P.L.R.
        A history of drug discovery for treatment of nausea and vomiting and the implications for future research.
        Front. Pharmacol. 2018; 9: 913https://doi.org/10.3389/fphar.2018.00913
        • Saper C.B.
        The central autonomic nervous system: conscious visceral perception and autonomic pattern generation.
        Annu. Rev. Neurosci. 2002; 25: 433-469https://doi.org/10.1146/annurev.neuro.25.032502.111311
        • Sclocco R.
        • Citi L.
        • Garcia R.G.
        • Cerutti S.
        • Bianchi A.M.
        • Kuo B.
        • Napadow V.
        • Barbieri R.
        Combining sudomotor nerve impulse estimation with fMRI to investigate the central sympathetic response to nausea.
        in: 37th Annu. Int. Conf. IEEE Eng. Med. Biol. Soc.2015. 2015: 4683-4686https://doi.org/10.1109/EMBC.2015.7319439
        • Sclocco R.
        • Kim J.
        • Garcia R.G.
        • Sheehan J.D.
        • Beissner F.
        • Bianchi A.M.
        • Cerutti S.
        • Kuo B.
        • Barbieri R.
        • Napadow V.
        Brain circuitry supporting multi-organ autonomic outflow in response to nausea.
        Cereb. Cortex. 2016; 26: 485-497https://doi.org/10.1093/cercor/bhu172
        • Seghier M.L.
        The angular gyrus: multiple functions and multiple subdivisions.
        Neuroscience. 2012; 19: 43-61https://doi.org/10.1177/1073858412440596
        • Seth A.K.
        • Suzuki K.
        • Critchley H.D.
        An interoceptive predictive coding model of conscious presence.
        Front. Psychol. 2012; 2: 395https://doi.org/10.3389/fpsyg.2011.00395
        • Slim K.
        • Nini E.
        • Forestier D.
        • Kwiatkowski F.
        • Panis Y.
        • Chipponi J.
        Methodological index for non-randomized studies (minors): development and validation of a new instrument.
        ANZ J. Surg. 2003; 73: 712-716https://doi.org/10.1046/j.1445-2197.2003.02748.x
        • Snodgrass P.
        • Sandoval H.
        • Calhoun V.D.
        • Ramos-Duran L.
        • Song G.
        • Sun Y.
        • Alvarado B.
        • Bashashati M.
        • Sarosiek I.
        • McCallum R.W.
        Central nervous system mechanisms of nausea in gastroparesis: an fMRI-based case-control study.
        Dig. Dis. Sci. 2020; 65: 551-556https://doi.org/10.1007/s10620-019-05766-5
        • Starr C.J.
        • Sawaki L.
        • Wittenberg G.F.
        • Burdette J.H.
        • Oshiro Y.
        • Quevedo A.S.
        • McHaffie J.G.
        • Coghill R.C.
        The contribution of the putamen to sensory aspects of pain: insights from structural connectivity and brain lesions.
        Brain. 2011; 134: 1987-2004https://doi.org/10.1093/brain/awr117
        • Stern R.M.
        • Koch K.L.
        • Andrews P.L.R.
        Nausea: Mechanisms and management.
        1st ed. Oxford University Press, New York2011
        • Sterne J.A.C.
        • Hernán M.A.
        • Reeves B.C.
        • Savović J.
        • Berkman N.D.
        • Viswanathan M.
        • Henry D.
        • Altman D.G.
        • Ansari M.T.
        • Boutron I.
        • Carpenter J.R.
        • Chan A.-W.
        • Churchill R.
        • Deeks J.J.
        • Hróbjartsson A.
        • Kirkham J.
        • Jüni P.
        • Loke Y.K.
        • Pigott T.D.
        • Ramsay C.R.
        • Regidor D.
        • Rothstein H.R.
        • Sandhu L.
        • Santaguida P.L.
        • Schünemann H.J.
        • Shea B.
        • Shrier I.
        • Tugwell P.
        • Turner L.
        • Valentine J.C.
        • Waddington H.
        • Waters E.
        • Wells G.A.
        • Whiting P.F.
        • Higgins J.P.T.
        ROBINS-I: a tool for assessing risk of bias in non-randomised studies of interventions.
        BMJ. 2016; 355i4919https://doi.org/10.1136/bmj.i4919
        • Stilwell P.
        • Harman K.
        An enactive approach to pain: beyond the biopsychosocial model.
        Phenomenol. Cogn. Sci. 2019; 18: 637-665https://doi.org/10.1007/s11097-019-09624-7
        • Strigo I.A.
        • Craig A.D.(Bud)
        Interoception, homeostatic emotions and sympathovagal balance.
        Philos. Trans. R. Soc. B Biol. Sci. 2016; 371: 20160010https://doi.org/10.1098/rstb.2016.0010
        • Sugumar A.
        • Singh A.
        • Pasricha P.J.
        A systematic review of the efficacy of domperidone for the treatment of diabetic gastroparesis.
        Clin. Gastroenterol. Hepatol. Off. Clin. Pract. J. Am. Gastroenterol. Assoc. 2008; 6: 726-733https://doi.org/10.1016/j.cgh.2008.02.065
        • Suzuki M.
        • Kitano H.
        • Ito R.
        • Kitanishi T.
        • Yazawa Y.
        • Ogawa T.
        • Shiino A.
        • Kitajima K.
        Cortical and subcortical vestibular response to caloric stimulation detected by functional magnetic resonance imaging.
        Brain Res. Cogn. Brain Res. 2001; 12: 441-449https://doi.org/10.1016/s0926-6410(01)00080-5
        • Symon D.N.
        • Russell G.
        The relationship between cyclic vomiting syndrome and abdominal migraine.
        J. Pediatr. Gastroenterol. Nutr. 1995; 21: S42-S43https://doi.org/10.1097/00005176-199501001-00012
        • Tanasescu R.
        • Cottam W.J.
        • Condon L.
        • Tench C.R.
        • Auer D.P.
        Functional reorganisation in chronic pain and neural correlates of pain sensitisation: a coordinate based meta-analysis of 266 cutaneous pain fMRI studies.
        Neurosci. Biobehav. Rev. 2016; 68: 120-133https://doi.org/10.1016/j.neubiorev.2016.04.001
        • The Jamovi Project
        jamovi (Version 1.6).
        • Toschi N.
        • Kim J.
        • Sclocco R.
        • Duggento A.
        • Barbieri R.
        • Kuo B.
        • Napadow V.
        Motion sickness increases functional connectivity between visual motion and nausea-associated brain regions.
        Auton. Neurosci. 2017; 202: 108-113https://doi.org/10.1016/j.autneu.2016.10.003
        • Venkatesan T.
        • Levinthal D.J.
        • Tarbell S.E.
        • Jaradeh S.S.
        • Hasler W.L.
        • Issenman R.M.
        • Adams K.A.
        • Sarosiek I.
        • Stave C.D.
        • Sharaf R.N.
        • Sultan S.
        • Li B.U.K.
        Guidelines on management of cyclic vomiting syndrome in adults by the american neurogastroenterology and motility society and the cyclic vomiting syndrome association.
        Neurogastroenterol. Motil. 2019; 31e13604https://doi.org/10.1111/nmo.13604
        • Wang J.
        • Yang Y.
        • Zhao X.
        • Zuo Z.
        • Tan L.-H.
        Evolutional and developmental anatomical architecture of the left inferior frontal gyrus.
        NeuroImage. 2020; 222117268https://doi.org/10.1016/j.neuroimage.2020.117268
        • Warr D.
        Prognostic factors for chemotherapy induced nausea and vomiting.
        Eur. J. Pharmacol. 2014; 722: 192-196https://doi.org/10.1016/j.ejphar.2013.10.015
        • Wei Y.
        • Okazaki Y.O.
        • So R.H.Y.
        • Chu W.C.W.
        • Kitajo K.
        Motion sickness-susceptible participants exposed to coherent rotating dot patterns show excessive N2 amplitudes and impaired theta-band phase synchronization.
        NeuroImage. 2019; 202116028https://doi.org/10.1016/j.neuroimage.2019.116028
        • Wickham H.
        • Averick M.
        • Bryan J.
        • Chang W.
        • McGowan L.
        • François R.
        • Grolemund G.
        • Hayes A.
        • Henry L.
        • Hester J.
        • Kuhn M.
        • Pedersen T.
        • Miller E.
        • Bache S.
        • Müller K.
        • Ooms J.
        • Robinson D.
        • Seidel D.
        • Spinu V.
        • Takahashi K.
        • Vaughan D.
        • Wilke C.
        • Woo K.
        • Yutani H.
        Welcome to the tidyverse.
        J. Open Source Softw. 2019; 4: 1686https://doi.org/10.21105/joss.01686
        • Wu J.
        • Zhou Q.
        • Li J.
        • Kong X.
        • Xiao Y.
        Inhibition-related N2 and P3: indicators of visually induced motion sickness (VIMS).
        Int. J. Ind. Ergon. 2020; 78102981https://doi.org/10.1016/j.ergon.2020.102981
        • Xu A.
        • Larsen B.
        • Baller E.B.
        • Scott J.C.
        • Sharma V.
        • Adebimpe A.
        • Basbaum A.I.
        • Dworkin R.H.
        • Edwards R.R.
        • Woolf C.J.
        • Eickhoff S.B.
        • Eickhoff C.R.
        • Satterthwaite T.D.
        Convergent neural representations of experimentally-induced acute pain in healthy volunteers: a large-scale fMRI meta-analysis.
        Neurosci. Biobehav. Rev. 2020; 112: 300-323https://doi.org/10.1016/j.neubiorev.2020.01.004
        • Yu L.
        • De Mazancourt M.
        • Hess A.
        • Ashadi F.R.
        • Klein I.
        • Mal H.
        • Courbage M.
        • Mangin L.
        Functional connectivity and information flow of the respiratory neural network in chronic obstructive pulmonary disease.
        Hum. Brain Mapp. 2016; 37: 2736-2754https://doi.org/10.1002/hbm.23205