Skip to main content
Top
Published in: Brain Topography 6/2019

01-11-2019 | Smelling Disorder | Review

Magnetic Resonance Imaging of Human Olfactory Dysfunction

Authors: Pengfei Han, Yunpeng Zang, Joshi Akshita, Thomas Hummel

Published in: Brain Topography | Issue 6/2019

Login to get access

Abstract

Olfactory dysfunctions affect a larger portion of population (up to 15% with partial olfactory loss, and 5% with complete olfactory loss) as compared to other sensory dysfunctions (e.g. auditory or visual) and have a negative impact on the life quality. The impairment of olfactory functions may happen at each stage of the olfactory system, from epithelium to cortex. Non-invasive neuroimaging techniques such as the magnetic resonance imaging (MRI) have advanced the understanding of the advent and progress of olfactory dysfunctions in humans. The current review summarizes recent MRI studies on human olfactory dysfunction to present an updated and comprehensive picture of the structural and functional alterations in the central olfactory system as a consequence of olfactory loss and regain. Furthermore, the review also highlights recent progress on optimizing the olfactory functional MRI as well as new approaches for data processing that are promising for future clinical practice.
Literature
go back to reference Albrecht J, Kopietz R, Frasnelli J, Wiesmann M, Hummel T, Lundstrom JN (2010) The neuronal correlates of intranasal trigeminal function-an ALE meta-analysis of human functional brain imaging data. Brain Res Rev 62:183–196PubMed Albrecht J, Kopietz R, Frasnelli J, Wiesmann M, Hummel T, Lundstrom JN (2010) The neuronal correlates of intranasal trigeminal function-an ALE meta-analysis of human functional brain imaging data. Brain Res Rev 62:183–196PubMed
go back to reference Arshamian A, Iannilli E, Gerber JC, Willander J, Persson J, Seo HS, Hummel T, Larsson M (2013) The functional neuroanatomy of odor evoked autobiographical memories cued by odors and words. Neuropsychologia 51:123–131PubMed Arshamian A, Iannilli E, Gerber JC, Willander J, Persson J, Seo HS, Hummel T, Larsson M (2013) The functional neuroanatomy of odor evoked autobiographical memories cued by odors and words. Neuropsychologia 51:123–131PubMed
go back to reference Atanasova B, Graux J, El Hage W, Hommet C, Camus V, Belzung C (2008) Olfaction: a potential cognitive marker of psychiatric disorders. Neurosci Biobehav Rev 32:1315–1325PubMed Atanasova B, Graux J, El Hage W, Hommet C, Camus V, Belzung C (2008) Olfaction: a potential cognitive marker of psychiatric disorders. Neurosci Biobehav Rev 32:1315–1325PubMed
go back to reference Baba T, Kikuchi A, Hirayama K, Nishio Y, Hosokai Y, Kanno S, Hasegawa T, Sugeno N, Konno M, Suzuki K, Takahashi S, Fukuda H, Aoki M, Itoyama Y, Mori E, Takeda A (2012) Severe olfactory dysfunction is a prodromal symptom of dementia associated with Parkinson’s disease: a 3 year longitudinal study. Brain 135:161–169PubMed Baba T, Kikuchi A, Hirayama K, Nishio Y, Hosokai Y, Kanno S, Hasegawa T, Sugeno N, Konno M, Suzuki K, Takahashi S, Fukuda H, Aoki M, Itoyama Y, Mori E, Takeda A (2012) Severe olfactory dysfunction is a prodromal symptom of dementia associated with Parkinson’s disease: a 3 year longitudinal study. Brain 135:161–169PubMed
go back to reference Bensafi M, Porter J, Pouliot S, Mainland J, Johnson B, Zelano C, Young N, Bremner E, Aframian D, Khan R, Sobel N (2003) Olfactomotor activity during imagery mimics that during perception. Nat Neurosci 6:1142–1144PubMed Bensafi M, Porter J, Pouliot S, Mainland J, Johnson B, Zelano C, Young N, Bremner E, Aframian D, Khan R, Sobel N (2003) Olfactomotor activity during imagery mimics that during perception. Nat Neurosci 6:1142–1144PubMed
go back to reference Bensafi M, Sobel N, Khan RM (2007) Hedonic-specific activity in piriform cortex during odor imagery mimics that during odor perception. J Neurophysiol 98:3254–3262PubMed Bensafi M, Sobel N, Khan RM (2007) Hedonic-specific activity in piriform cortex during odor imagery mimics that during odor perception. J Neurophysiol 98:3254–3262PubMed
go back to reference Bitter T, Bruderle J, Gudziol H, Burmeister HP, Gaser C, Guntinas-Lichius O (2010a) Gray and white matter reduction in hyposmic subjects—a voxel-based morphometry study. Brain Res 1347:42–47PubMed Bitter T, Bruderle J, Gudziol H, Burmeister HP, Gaser C, Guntinas-Lichius O (2010a) Gray and white matter reduction in hyposmic subjects—a voxel-based morphometry study. Brain Res 1347:42–47PubMed
go back to reference Bitter T, Gudziol H, Burmeister HP, Mentzel HJ, Guntinas-Lichius O, Gaser C (2010b) Anosmia leads to a loss of gray matter in cortical brain areas. Chem Senses 35:407–415PubMed Bitter T, Gudziol H, Burmeister HP, Mentzel HJ, Guntinas-Lichius O, Gaser C (2010b) Anosmia leads to a loss of gray matter in cortical brain areas. Chem Senses 35:407–415PubMed
go back to reference Bramerson A, Johansson L, Ek L, Nordin S, Bende M (2004) Prevalence of olfactory dysfunction: the skovde population-based study. Laryngoscope 114:733–737PubMed Bramerson A, Johansson L, Ek L, Nordin S, Bende M (2004) Prevalence of olfactory dysfunction: the skovde population-based study. Laryngoscope 114:733–737PubMed
go back to reference Braun JJ, Noblet V, Durand M, Scheidecker S, Zinetti-Bertschy A, Foucher J, Marion V, Muller J, Riehm S, Dollfus H, Kremer S (2014) Olfaction evaluation and correlation with brain atrophy in Bardet-Biedl syndrome. Clin Genet 86:521–529PubMed Braun JJ, Noblet V, Durand M, Scheidecker S, Zinetti-Bertschy A, Foucher J, Marion V, Muller J, Riehm S, Dollfus H, Kremer S (2014) Olfaction evaluation and correlation with brain atrophy in Bardet-Biedl syndrome. Clin Genet 86:521–529PubMed
go back to reference Buschhuter D, Smitka M, Puschmann S, Gerber JC, Witt M, Abolmaali ND, Hummel T (2008) Correlation between olfactory bulb volume and olfactory function. Neuroimage 42:498–502PubMed Buschhuter D, Smitka M, Puschmann S, Gerber JC, Witt M, Abolmaali ND, Hummel T (2008) Correlation between olfactory bulb volume and olfactory function. Neuroimage 42:498–502PubMed
go back to reference Campabadal A, Uribe C, Segura B, Baggio HC, Abos A, Garcia-Diaz AI, Marti MJ, Valldeoriola F, Compta Y, Bargallo N, Junque C (2017) Brain correlates of progressive olfactory loss in Parkinson’s disease. Parkinsonism Relat Disord 41:44–50PubMed Campabadal A, Uribe C, Segura B, Baggio HC, Abos A, Garcia-Diaz AI, Marti MJ, Valldeoriola F, Compta Y, Bargallo N, Junque C (2017) Brain correlates of progressive olfactory loss in Parkinson’s disease. Parkinsonism Relat Disord 41:44–50PubMed
go back to reference Cavanna AE, Trimble MR (2006) The precuneus: a review of its functional anatomy and behavioural correlates. Brain 129:564–583PubMed Cavanna AE, Trimble MR (2006) The precuneus: a review of its functional anatomy and behavioural correlates. Brain 129:564–583PubMed
go back to reference Croy I, Hummel T (2017) Olfaction as a marker for depression. J Neurol 264:631–638PubMed Croy I, Hummel T (2017) Olfaction as a marker for depression. J Neurol 264:631–638PubMed
go back to reference Croy I, Nordin S, Hummel T (2014) Olfactory disorders and quality of life—an updated review. Chem Senses 39:185–194PubMed Croy I, Nordin S, Hummel T (2014) Olfactory disorders and quality of life—an updated review. Chem Senses 39:185–194PubMed
go back to reference Curtis CE, D’Esposito M (2003) Persistent activity in the prefrontal cortex during working memory. Trends Cogn Sci 7:415–423PubMed Curtis CE, D’Esposito M (2003) Persistent activity in the prefrontal cortex during working memory. Trends Cogn Sci 7:415–423PubMed
go back to reference Dade LA, Zatorre RJ, Evans AC, Jones-Gotman M (2001) Working memory in another dimension: functional imaging of human olfactory working memory. Neuroimage 14:650–660PubMed Dade LA, Zatorre RJ, Evans AC, Jones-Gotman M (2001) Working memory in another dimension: functional imaging of human olfactory working memory. Neuroimage 14:650–660PubMed
go back to reference Damoiseaux JS, Rombouts SA, Barkhof F, Scheltens P, Stam CJ, Smith SM, Beckmann CF (2006) Consistent resting-state networks across healthy subjects. Proc Natl Acad Sci USA 103:13848–13853PubMedPubMedCentral Damoiseaux JS, Rombouts SA, Barkhof F, Scheltens P, Stam CJ, Smith SM, Beckmann CF (2006) Consistent resting-state networks across healthy subjects. Proc Natl Acad Sci USA 103:13848–13853PubMedPubMedCentral
go back to reference Davatzikos C, Resnick SM, Wu X, Parmpi P, Clark CM (2008) Individual patient diagnosis of AD and FTD via high-dimensional pattern classification of MRI. Neuroimage 41:1220–1227PubMed Davatzikos C, Resnick SM, Wu X, Parmpi P, Clark CM (2008) Individual patient diagnosis of AD and FTD via high-dimensional pattern classification of MRI. Neuroimage 41:1220–1227PubMed
go back to reference de Araujo IE, Rolls ET, Velazco MI, Margot C, Cayeux I (2005) Cognitive modulation of olfactory processing. Neuron 46:671–679PubMed de Araujo IE, Rolls ET, Velazco MI, Margot C, Cayeux I (2005) Cognitive modulation of olfactory processing. Neuron 46:671–679PubMed
go back to reference Djordjevic J, Zatorre RJ, Petrides M, Boyle JA, Jones-Gotman M (2005) Functional neuroimaging of odor imagery. Neuroimage 24:791–801PubMed Djordjevic J, Zatorre RJ, Petrides M, Boyle JA, Jones-Gotman M (2005) Functional neuroimaging of odor imagery. Neuroimage 24:791–801PubMed
go back to reference Dwyer DB, Falkai P, Koutsouleris N (2018) Machine learning approaches for clinical psychology and psychiatry. Annu Rev Clin Psychol 14:91–118PubMed Dwyer DB, Falkai P, Koutsouleris N (2018) Machine learning approaches for clinical psychology and psychiatry. Annu Rev Clin Psychol 14:91–118PubMed
go back to reference Erb K, Bohner G, Harms L, Goektas O, Fleiner F, Dommes E, Schmidt FA, Dahlslett B, Ludemann L (2012) Olfactory function in patients with multiple sclerosis: a diffusion tensor imaging study. J Neurol Sci 316:56–60PubMed Erb K, Bohner G, Harms L, Goektas O, Fleiner F, Dommes E, Schmidt FA, Dahlslett B, Ludemann L (2012) Olfactory function in patients with multiple sclerosis: a diffusion tensor imaging study. J Neurol Sci 316:56–60PubMed
go back to reference Erb-Eigner K, Bohner G, Goektas O, Harms L, Holinski F, Schmidt FA, Dahlslett B, Dommes E, Asbach P, Ludemann L (2014) Tract-based spatial statistics of the olfactory brain in patients with multiple sclerosis. J Neurol Sci 346:235–240PubMed Erb-Eigner K, Bohner G, Goektas O, Harms L, Holinski F, Schmidt FA, Dahlslett B, Dommes E, Asbach P, Ludemann L (2014) Tract-based spatial statistics of the olfactory brain in patients with multiple sclerosis. J Neurol Sci 346:235–240PubMed
go back to reference Fernandes HM, Van Hartevelt TJ, Boccard SG, Owen SL, Cabral J, Deco G, Green AL, Fitzgerald JJ, Aziz TZ, Kringelbach ML (2015) Novel fingerprinting method characterises the necessary and sufficient structural connectivity from deep brain stimulation electrodes for a successful outcome. New J Phys 17:015001 Fernandes HM, Van Hartevelt TJ, Boccard SG, Owen SL, Cabral J, Deco G, Green AL, Fitzgerald JJ, Aziz TZ, Kringelbach ML (2015) Novel fingerprinting method characterises the necessary and sufficient structural connectivity from deep brain stimulation electrodes for a successful outcome. New J Phys 17:015001
go back to reference Fjaeldstad A, Fernandes HM, Van Hartevelt TJ, Gleesborg C, Moller A, Ovesen T, Kringelbach ML (2017) Brain fingerprints of olfaction: a novel structural method for assessing olfactory cortical networks in health and disease. Sci Rep 7:42534PubMedPubMedCentral Fjaeldstad A, Fernandes HM, Van Hartevelt TJ, Gleesborg C, Moller A, Ovesen T, Kringelbach ML (2017) Brain fingerprints of olfaction: a novel structural method for assessing olfactory cortical networks in health and disease. Sci Rep 7:42534PubMedPubMedCentral
go back to reference Flohr EL, Arshamian A, Wieser MJ, Hummel C, Larsson M, Muhlberger A, Hummel T (2014) The fate of the inner nose: odor imagery in patients with olfactory loss. Neuroscience 268:118–127PubMed Flohr EL, Arshamian A, Wieser MJ, Hummel C, Larsson M, Muhlberger A, Hummel T (2014) The fate of the inner nose: odor imagery in patients with olfactory loss. Neuroscience 268:118–127PubMed
go back to reference Frasnelli J, Hummel T (2005) Olfactory dysfunction and daily life. Eur Arch Otorhinolaryngol 262:231–235PubMed Frasnelli J, Hummel T (2005) Olfactory dysfunction and daily life. Eur Arch Otorhinolaryngol 262:231–235PubMed
go back to reference Frasnelli J, Fark T, Lehmann J, Gerber J, Hummel T (2013) Brain structure is changed in congenital anosmia. Neuroimage 83:1074–1080PubMed Frasnelli J, Fark T, Lehmann J, Gerber J, Hummel T (2013) Brain structure is changed in congenital anosmia. Neuroimage 83:1074–1080PubMed
go back to reference Frohner JH, Teckentrup V, Smolka MN, Kroemer NB (2019) Addressing the reliability fallacy in fMRI: similar group effects may arise from unreliable individual effects. Neuroimage 195:174–189PubMed Frohner JH, Teckentrup V, Smolka MN, Kroemer NB (2019) Addressing the reliability fallacy in fMRI: similar group effects may arise from unreliable individual effects. Neuroimage 195:174–189PubMed
go back to reference Fu CH, Mourao-Miranda J, Costafreda SG, Khanna A, Marquand AF, Williams SC, Brammer MJ (2008) Pattern classification of sad facial processing: toward the development of neurobiological markers in depression. Biol Psychiatry 63:656–662PubMed Fu CH, Mourao-Miranda J, Costafreda SG, Khanna A, Marquand AF, Williams SC, Brammer MJ (2008) Pattern classification of sad facial processing: toward the development of neurobiological markers in depression. Biol Psychiatry 63:656–662PubMed
go back to reference Gellrich J, Han P, Manesse C, Betz A, Junghanns A, Raue C, Schriever VA, Hummel T (2018) Brain volume changes in hyposmic patients before and after olfactory training. Laryngoscope 128:1531–1536PubMed Gellrich J, Han P, Manesse C, Betz A, Junghanns A, Raue C, Schriever VA, Hummel T (2018) Brain volume changes in hyposmic patients before and after olfactory training. Laryngoscope 128:1531–1536PubMed
go back to reference Georgiopoulos C, Witt ST, Haller S, Dizdar N, Zachrisson H, Engstrom M, Larsson EM (2018) Olfactory fMRI: implications of stimulation length and repetition time. Chem Senses 43:389–398PubMed Georgiopoulos C, Witt ST, Haller S, Dizdar N, Zachrisson H, Engstrom M, Larsson EM (2018) Olfactory fMRI: implications of stimulation length and repetition time. Chem Senses 43:389–398PubMed
go back to reference Gonzalez J, Barros-Loscertales A, Pulvermuller F, Meseguer V, Sanjuan A, Belloch V, Avila C (2006) Reading cinnamon activates olfactory brain regions. Neuroimage 32:906–912PubMed Gonzalez J, Barros-Loscertales A, Pulvermuller F, Meseguer V, Sanjuan A, Belloch V, Avila C (2006) Reading cinnamon activates olfactory brain regions. Neuroimage 32:906–912PubMed
go back to reference Gottfried JA, Zald DH (2005) On the scent of human olfactory orbitofrontal cortex: meta-analysis and comparison to non-human primates. Brain Res Rev 50:287–304PubMed Gottfried JA, Zald DH (2005) On the scent of human olfactory orbitofrontal cortex: meta-analysis and comparison to non-human primates. Brain Res Rev 50:287–304PubMed
go back to reference Gudziol V, Buschhuter D, Abolmaali N, Gerber J, Rombaux P, Hummel T (2009) Increasing olfactory bulb volume due to treatment of chronic rhinosinusitis—a longitudinal study. Brain 132:3096–3101PubMed Gudziol V, Buschhuter D, Abolmaali N, Gerber J, Rombaux P, Hummel T (2009) Increasing olfactory bulb volume due to treatment of chronic rhinosinusitis—a longitudinal study. Brain 132:3096–3101PubMed
go back to reference Gullmar D, Seeliger T, Gudziol H, Teichgraber UKM, Reichenbach JR, Guntinas-Lichius O, Bitter T (2017) Improvement of olfactory function after sinus surgery correlates with white matter properties measured by diffusion tensor imaging. Neuroscience 360:190–196PubMed Gullmar D, Seeliger T, Gudziol H, Teichgraber UKM, Reichenbach JR, Guntinas-Lichius O, Bitter T (2017) Improvement of olfactory function after sinus surgery correlates with white matter properties measured by diffusion tensor imaging. Neuroscience 360:190–196PubMed
go back to reference Haehner A, Hummel T, Hummel C, Sommer U, Junghanns S, Reichmann H (2007) Olfactory loss may be a first sign of idiopathic Parkinson’s disease. Mov Disord 22:839–842PubMed Haehner A, Hummel T, Hummel C, Sommer U, Junghanns S, Reichmann H (2007) Olfactory loss may be a first sign of idiopathic Parkinson’s disease. Mov Disord 22:839–842PubMed
go back to reference Haehner A, Rodewald A, Gerber JC, Hummel T (2008) Correlation of olfactory function with changes in the volume of the human olfactory bulb. Arch Otolaryngol Head Neck Surg 134:621–624PubMed Haehner A, Rodewald A, Gerber JC, Hummel T (2008) Correlation of olfactory function with changes in the volume of the human olfactory bulb. Arch Otolaryngol Head Neck Surg 134:621–624PubMed
go back to reference Hagemeier J, Woodward MR, Rafique UA, Amrutkar CV, Bergsland N, Dwyer MG, Benedict R, Zivadinov R, Szigeti K (2016) Odor identification deficit in mild cognitive impairment and Alzheimer’s disease is associated with hippocampal and deep gray matter atrophy. Psychiatry Res 255:87–93 Hagemeier J, Woodward MR, Rafique UA, Amrutkar CV, Bergsland N, Dwyer MG, Benedict R, Zivadinov R, Szigeti K (2016) Odor identification deficit in mild cognitive impairment and Alzheimer’s disease is associated with hippocampal and deep gray matter atrophy. Psychiatry Res 255:87–93
go back to reference Han P, Whitcroft KL, Fischer J, Gerber J, Cuevas M, Andrews P, Hummel T (2017) Olfactory brain gray matter volume reduction in patients with chronic rhinosinusitis. Int Forum Allergy Rhinol 7:551–556PubMed Han P, Whitcroft KL, Fischer J, Gerber J, Cuevas M, Andrews P, Hummel T (2017) Olfactory brain gray matter volume reduction in patients with chronic rhinosinusitis. Int Forum Allergy Rhinol 7:551–556PubMed
go back to reference Han P, Winkler N, Hummel C, Hahner A, Gerber J, Hummel T (2018a) Alterations of brain gray matter density and olfactory bulb volume in patients with olfactory loss after traumatic brain injury. J Neurotrauma 35:2632–2640PubMed Han P, Winkler N, Hummel C, Hahner A, Gerber J, Hummel T (2018a) Alterations of brain gray matter density and olfactory bulb volume in patients with olfactory loss after traumatic brain injury. J Neurotrauma 35:2632–2640PubMed
go back to reference Han P, Winkler N, Hummel C, Hahner A, Gerber J, Hummel T (2018b) Impaired brain response to odors in patients with varied severity of olfactory loss after traumatic brain injury. J Neurol 265:2322–2332PubMed Han P, Winkler N, Hummel C, Hahner A, Gerber J, Hummel T (2018b) Impaired brain response to odors in patients with varied severity of olfactory loss after traumatic brain injury. J Neurol 265:2322–2332PubMed
go back to reference Hawkes CH, Shephard BC, Daniel SE (1997) Olfactory dysfunction in Parkinson’s disease. J Neurol Neurosurg Psychiatry 62:436–446PubMedPubMedCentral Hawkes CH, Shephard BC, Daniel SE (1997) Olfactory dysfunction in Parkinson’s disease. J Neurol Neurosurg Psychiatry 62:436–446PubMedPubMedCentral
go back to reference Henkin RI, Levy LM (2002) Functional MRI of congenital hyposmia: brain activation to odors and imagination of odors and tastes. J Comput Assist Tomogr 26:39–61PubMed Henkin RI, Levy LM (2002) Functional MRI of congenital hyposmia: brain activation to odors and imagination of odors and tastes. J Comput Assist Tomogr 26:39–61PubMed
go back to reference Hermundstad AM, Bassett DS, Brown KS, Aminoff EM, Clewett D, Freeman S, Frithsen A, Johnson A, Tipper CM, Miller MB, Grafton ST, Carlson JM (2013) Structural foundations of resting-state and task-based functional connectivity in the human brain. Proc Natl Acad Sci USA 110:6169–6174PubMedPubMedCentral Hermundstad AM, Bassett DS, Brown KS, Aminoff EM, Clewett D, Freeman S, Frithsen A, Johnson A, Tipper CM, Miller MB, Grafton ST, Carlson JM (2013) Structural foundations of resting-state and task-based functional connectivity in the human brain. Proc Natl Acad Sci USA 110:6169–6174PubMedPubMedCentral
go back to reference Hummel T, Bensafi M, Nikolaus J, Knecht M, Laing DG, Schaal B (2007) Olfactory function in children assessed with psychophysical and electrophysiological techniques. Behav Brain Res 180:133–138PubMed Hummel T, Bensafi M, Nikolaus J, Knecht M, Laing DG, Schaal B (2007) Olfactory function in children assessed with psychophysical and electrophysiological techniques. Behav Brain Res 180:133–138PubMed
go back to reference Hummel T, Fliessbach K, Abele M, Okulla T, Reden J, Reichmann H, Wullner U, Haehner A (2010) Olfactory FMRI in patients with Parkinson’s disease. Front Integr Neurosci 4:125PubMedPubMedCentral Hummel T, Fliessbach K, Abele M, Okulla T, Reden J, Reichmann H, Wullner U, Haehner A (2010) Olfactory FMRI in patients with Parkinson’s disease. Front Integr Neurosci 4:125PubMedPubMedCentral
go back to reference Hummel T, Urbig A, Huart C, Duprez T, Rombaux P (2015) Volume of olfactory bulb and depth of olfactory sulcus in 378 consecutive patients with olfactory loss. J Neurol 262:1046–1051PubMed Hummel T, Urbig A, Huart C, Duprez T, Rombaux P (2015) Volume of olfactory bulb and depth of olfactory sulcus in 378 consecutive patients with olfactory loss. J Neurol 262:1046–1051PubMed
go back to reference Hummel T, Whitcroft KL, Andrews P, Altundag A, Cinghi C, Costanzo RM, Damm M, Frasnelli J, Gudziol H, Gupta N, Haehner A, Holbrook E, Hong SC, Hornung D, Huttenbrink KB, Kamel R, Kobayashi M, Konstantinidis I, Landis BN, Leopold DA, Macchi A, Miwa T, Moesges R, Mullol J, Mueller CA, Ottaviano G, Passali GC, Philpott C, Pinto JM, Ramakrishnan VJ, Rombaux P, Roth Y, Schlosser RA, Shu B, Soler G, Stjarne P, Stuck BA, Vodicka J, Welge-Luessen A (2016) Position paper on olfactory dysfunction. Rhinology 56:1–30PubMed Hummel T, Whitcroft KL, Andrews P, Altundag A, Cinghi C, Costanzo RM, Damm M, Frasnelli J, Gudziol H, Gupta N, Haehner A, Holbrook E, Hong SC, Hornung D, Huttenbrink KB, Kamel R, Kobayashi M, Konstantinidis I, Landis BN, Leopold DA, Macchi A, Miwa T, Moesges R, Mullol J, Mueller CA, Ottaviano G, Passali GC, Philpott C, Pinto JM, Ramakrishnan VJ, Rombaux P, Roth Y, Schlosser RA, Shu B, Soler G, Stjarne P, Stuck BA, Vodicka J, Welge-Luessen A (2016) Position paper on olfactory dysfunction. Rhinology 56:1–30PubMed
go back to reference Iannilli E, Gerber J, Frasnelli J, Hummel T (2007) Intranasal trigeminal function in subjects with and without an intact sense of smell. Brain Res 1139:235–244PubMed Iannilli E, Gerber J, Frasnelli J, Hummel T (2007) Intranasal trigeminal function in subjects with and without an intact sense of smell. Brain Res 1139:235–244PubMed
go back to reference Iannilli E, Bitter T, Gudziol H, Burmeister HP, Mentzel HJ, Chopra AP, Hummel T (2011) Differences in anosmic and normosmic group in bimodal odorant perception: a functional-MRI study. Rhinology 49:458–463PubMed Iannilli E, Bitter T, Gudziol H, Burmeister HP, Mentzel HJ, Chopra AP, Hummel T (2011) Differences in anosmic and normosmic group in bimodal odorant perception: a functional-MRI study. Rhinology 49:458–463PubMed
go back to reference Ibarretxe-Bilbao N, Junque C, Marti MJ, Valldeoriola F, Vendrell P, Bargallo N, Zarei M, Tolosa E (2010) Olfactory impairment in Parkinson’s disease and white matter abnormalities in central olfactory areas: a voxel-based diffusion tensor imaging study. Mov Disord 25:1888–1894PubMed Ibarretxe-Bilbao N, Junque C, Marti MJ, Valldeoriola F, Vendrell P, Bargallo N, Zarei M, Tolosa E (2010) Olfactory impairment in Parkinson’s disease and white matter abnormalities in central olfactory areas: a voxel-based diffusion tensor imaging study. Mov Disord 25:1888–1894PubMed
go back to reference Jones DK, Leemans A (2011) Diffusion tensor imaging. Magn Reson Neuroimaging 711:127–144 Jones DK, Leemans A (2011) Diffusion tensor imaging. Magn Reson Neuroimaging 711:127–144
go back to reference Jones DK, Knosche TR, Turner R (2013) White matter integrity, fiber count, and other fallacies: the do’s and don’ts of diffusion MRI. Neuroimage 73:239–254PubMed Jones DK, Knosche TR, Turner R (2013) White matter integrity, fiber count, and other fallacies: the do’s and don’ts of diffusion MRI. Neuroimage 73:239–254PubMed
go back to reference Kareken DA, Sabri M, Radnovich AJ, Claus E, Foresman B, Hector D, Hutchins GD (2004) Olfactory system activation from sniffing: effects in piriform and orbitofrontal cortex. Neuroimage 22:456–465PubMed Kareken DA, Sabri M, Radnovich AJ, Claus E, Foresman B, Hector D, Hutchins GD (2004) Olfactory system activation from sniffing: effects in piriform and orbitofrontal cortex. Neuroimage 22:456–465PubMed
go back to reference Karstensen HG, Vestergaard M, Baare WFC, Skimminge A, Djurhuus B, Ellefsen B, Bruggemann N, Klausen C, Leffers AM, Tommerup N, Siebner HR (2018) Congenital olfactory impairment is linked to cortical changes in prefrontal and limbic brain regions. Brain Imaging Behav 12:1569–1582PubMed Karstensen HG, Vestergaard M, Baare WFC, Skimminge A, Djurhuus B, Ellefsen B, Bruggemann N, Klausen C, Leffers AM, Tommerup N, Siebner HR (2018) Congenital olfactory impairment is linked to cortical changes in prefrontal and limbic brain regions. Brain Imaging Behav 12:1569–1582PubMed
go back to reference Kjelvik G, Saltvedt I, White LR, Stenumgard P, Sletvold O, Engedal K, Skatun K, Lyngvaer AK, Steffenach HA, Haberg AK (2014) The brain structural and cognitive basis of odor identification deficits in mild cognitive impairment and Alzheimer’s disease. BMC Neurol 14:168PubMedPubMedCentral Kjelvik G, Saltvedt I, White LR, Stenumgard P, Sletvold O, Engedal K, Skatun K, Lyngvaer AK, Steffenach HA, Haberg AK (2014) The brain structural and cognitive basis of odor identification deficits in mild cognitive impairment and Alzheimer’s disease. BMC Neurol 14:168PubMedPubMedCentral
go back to reference Kleinhans NM, Reilly M, Blake M, Greco G, Sweigert J, Davis GE, Velasquez F, Reitz F, Shusterman D, Dager SR (2019) FMRI correlates of olfactory processing in typically-developing school-aged children. Psychiatry Res Neuroimaging 283:67–76PubMed Kleinhans NM, Reilly M, Blake M, Greco G, Sweigert J, Davis GE, Velasquez F, Reitz F, Shusterman D, Dager SR (2019) FMRI correlates of olfactory processing in typically-developing school-aged children. Psychiatry Res Neuroimaging 283:67–76PubMed
go back to reference Kloppel S, Stonnington CM, Chu C, Draganski B, Scahill RI, Rohrer JD, Fox NC, Jack CR Jr, Ashburner J, Frackowiak RS (2008) Automatic classification of MR scans in Alzheimer’s disease. Brain 131:681–689PubMed Kloppel S, Stonnington CM, Chu C, Draganski B, Scahill RI, Rohrer JD, Fox NC, Jack CR Jr, Ashburner J, Frackowiak RS (2008) Automatic classification of MR scans in Alzheimer’s disease. Brain 131:681–689PubMed
go back to reference Koehler L, Fournel A, Albertowski K, Roessner V, Gerber J, Hummel C, Hummel T, Bensafi M (2018) Impaired odor perception in autism spectrum disorder is associated with decreased activity in olfactory cortex. Chem Senses 43:627–634PubMed Koehler L, Fournel A, Albertowski K, Roessner V, Gerber J, Hummel C, Hummel T, Bensafi M (2018) Impaired odor perception in autism spectrum disorder is associated with decreased activity in olfactory cortex. Chem Senses 43:627–634PubMed
go back to reference Kollndorfer K, Fischmeister FP, Kowalczyk K, Hoche E, Mueller CA, Trattnig S, Schopf V (2015a) Olfactory training induces changes in regional functional connectivity in patients with long-term smell loss. Neuroimage Clin 9:401–410PubMedPubMedCentral Kollndorfer K, Fischmeister FP, Kowalczyk K, Hoche E, Mueller CA, Trattnig S, Schopf V (2015a) Olfactory training induces changes in regional functional connectivity in patients with long-term smell loss. Neuroimage Clin 9:401–410PubMedPubMedCentral
go back to reference Kollndorfer K, Jakab A, Mueller CA, Trattnig S, Schopf V (2015b) Effects of chronic peripheral olfactory loss on functional brain networks. Neuroscience 310:589–599PubMed Kollndorfer K, Jakab A, Mueller CA, Trattnig S, Schopf V (2015b) Effects of chronic peripheral olfactory loss on functional brain networks. Neuroscience 310:589–599PubMed
go back to reference Lavagnino L, Mwangi B, Cao B, Shott ME, Soares JC, Frank GKW (2018) Cortical thickness patterns as state biomarker of anorexia nervosa. Int J Eat Disord 51:241–249PubMedPubMedCentral Lavagnino L, Mwangi B, Cao B, Shott ME, Soares JC, Frank GKW (2018) Cortical thickness patterns as state biomarker of anorexia nervosa. Int J Eat Disord 51:241–249PubMedPubMedCentral
go back to reference Lee EY, Eslinger PJ, Du G, Kong L, Lewis MM, Huang X (2014) Olfactory-related cortical atrophy is associated with olfactory dysfunction in Parkinson’s disease. Mov Disord 29:1205–1208PubMedPubMedCentral Lee EY, Eslinger PJ, Du G, Kong L, Lewis MM, Huang X (2014) Olfactory-related cortical atrophy is associated with olfactory dysfunction in Parkinson’s disease. Mov Disord 29:1205–1208PubMedPubMedCentral
go back to reference Levy LM, Henkin RI, Hutter A, Lin CS, Schellinger D (1998) Mapping brain activation to odorants in patients with smell loss by functional MRI. J Comput Assist Tomogr 22:96–103PubMed Levy LM, Henkin RI, Hutter A, Lin CS, Schellinger D (1998) Mapping brain activation to odorants in patients with smell loss by functional MRI. J Comput Assist Tomogr 22:96–103PubMed
go back to reference Levy LM, Henkin RI, Lin CS, Finley A (1999a) Rapid imaging of olfaction by functional MRI (fMRI): identification of presence and type of hyposmia. J Comput Assist Tomogr 23:767–775PubMed Levy LM, Henkin RI, Lin CS, Finley A (1999a) Rapid imaging of olfaction by functional MRI (fMRI): identification of presence and type of hyposmia. J Comput Assist Tomogr 23:767–775PubMed
go back to reference Levy LM, Henkin RI, Lin CS, Hutter A, Schellinger D (1999b) Odor memory induces brain activation as measured by functional MRI. J Comput Assist Tomogr 23:487–498PubMed Levy LM, Henkin RI, Lin CS, Hutter A, Schellinger D (1999b) Odor memory induces brain activation as measured by functional MRI. J Comput Assist Tomogr 23:487–498PubMed
go back to reference Li W, Howard JD, Gottfried JA (2010) Disruption of odour quality coding in piriform cortex mediates olfactory deficits in Alzheimer’s disease. Brain 133:2714–2726PubMedPubMedCentral Li W, Howard JD, Gottfried JA (2010) Disruption of odour quality coding in piriform cortex mediates olfactory deficits in Alzheimer’s disease. Brain 133:2714–2726PubMedPubMedCentral
go back to reference Lotsch J, Hummel T, Ultsch A (2016) Machine-learned pattern identification in olfactory subtest results. Sci Rep 6:35688PubMedPubMedCentral Lotsch J, Hummel T, Ultsch A (2016) Machine-learned pattern identification in olfactory subtest results. Sci Rep 6:35688PubMedPubMedCentral
go back to reference Lotsch J, Kringel D, Hummel T (2019) Machine learning in human olfactory research. Chem Senses 44:11–22PubMed Lotsch J, Kringel D, Hummel T (2019) Machine learning in human olfactory research. Chem Senses 44:11–22PubMed
go back to reference Lu J, Wang X, Qing Z, Li Z, Zhang W, Liu Y, Yuan L, Cheng L, Li M, Zhu B, Zhang X, Yang QX, Zhang B (2018) Detectability and reproducibility of the olfactory fMRI signal under the influence of magnetic susceptibility artifacts in the primary olfactory cortex. Neuroimage 178:613–621PubMed Lu J, Wang X, Qing Z, Li Z, Zhang W, Liu Y, Yuan L, Cheng L, Li M, Zhu B, Zhang X, Yang QX, Zhang B (2018) Detectability and reproducibility of the olfactory fMRI signal under the influence of magnetic susceptibility artifacts in the primary olfactory cortex. Neuroimage 178:613–621PubMed
go back to reference Lueken U, Straube B, Yang Y, Hahn T, Beesdo-Baum K, Wittchen HU, Konrad C, Strohle A, Wittmann A, Gerlach AL, Pfleiderer B, Arolt V, Kircher T (2015) Separating depressive comorbidity from panic disorder: a combined functional magnetic resonance imaging and machine learning approach. J Affect Disord 184:182–192PubMed Lueken U, Straube B, Yang Y, Hahn T, Beesdo-Baum K, Wittchen HU, Konrad C, Strohle A, Wittmann A, Gerlach AL, Pfleiderer B, Arolt V, Kircher T (2015) Separating depressive comorbidity from panic disorder: a combined functional magnetic resonance imaging and machine learning approach. J Affect Disord 184:182–192PubMed
go back to reference Mandairon N, Linster C (2009) Odor perception and olfactory bulb plasticity in adult mammals. J Neurophysiol 101:2204–2209PubMed Mandairon N, Linster C (2009) Odor perception and olfactory bulb plasticity in adult mammals. J Neurophysiol 101:2204–2209PubMed
go back to reference Marine N, Boriana A (2014) Olfactory markers of depression and Alzheimer’s disease. Neurosci Biobehav Rev 45:262–270PubMed Marine N, Boriana A (2014) Olfactory markers of depression and Alzheimer’s disease. Neurosci Biobehav Rev 45:262–270PubMed
go back to reference Mazal PP, Haehner A, Hummel T (2016) Relation of the volume of the olfactory bulb to psychophysical measures of olfactory function. Eur Arch Otorhinolaryngol 273:1–7PubMed Mazal PP, Haehner A, Hummel T (2016) Relation of the volume of the olfactory bulb to psychophysical measures of olfactory function. Eur Arch Otorhinolaryngol 273:1–7PubMed
go back to reference McGann JP (2015) Associative learning and sensory neuroplasticity: how does it happen and what is it good for? Learn Mem 22:567–576PubMedPubMedCentral McGann JP (2015) Associative learning and sensory neuroplasticity: how does it happen and what is it good for? Learn Mem 22:567–576PubMedPubMedCentral
go back to reference McGann JP (2017) Poor human olfaction is a 19th-century myth. Science 356:597 McGann JP (2017) Poor human olfaction is a 19th-century myth. Science 356:597
go back to reference Miwa T, Furukawa M, Tsukatani T, Costanzo RM, DiNardo LJ, Reiter ER (2001) Impact of olfactory impairment on quality of life and disability. Arch Otolaryngol Head Neck Surg 127:497–503PubMed Miwa T, Furukawa M, Tsukatani T, Costanzo RM, DiNardo LJ, Reiter ER (2001) Impact of olfactory impairment on quality of life and disability. Arch Otolaryngol Head Neck Surg 127:497–503PubMed
go back to reference Moberg PJ, Agrin R, Gur RE, Gur RC, Turetsky BI, Doty RL (1999) Olfactory dysfunction in schizophrenia: a qualitative and quantitative review. Neuropsychopharmacology 21:325–340PubMed Moberg PJ, Agrin R, Gur RE, Gur RC, Turetsky BI, Doty RL (1999) Olfactory dysfunction in schizophrenia: a qualitative and quantitative review. Neuropsychopharmacology 21:325–340PubMed
go back to reference Moon WJ, Park M, Hwang M, Kim JK (2018) Functional MRI as an objective measure of olfaction deficit in patients with traumatic anosmia. AJNR Am J Neuroradiol 39:2320–2325PubMedPubMedCentral Moon WJ, Park M, Hwang M, Kim JK (2018) Functional MRI as an objective measure of olfaction deficit in patients with traumatic anosmia. AJNR Am J Neuroradiol 39:2320–2325PubMedPubMedCentral
go back to reference Morrot G, Bonny JM, Lehallier B, Zanca M (2013) fMRI of human olfaction at the individual level: interindividual variability. J Magn Reson Imaging 37:92–100PubMed Morrot G, Bonny JM, Lehallier B, Zanca M (2013) fMRI of human olfaction at the individual level: interindividual variability. J Magn Reson Imaging 37:92–100PubMed
go back to reference Mueller A, Abolmaali ND, Hakimi AR, Gloeckler T, Herting B, Reichmann H, Hummel T (2005a) Olfactory bulb volumes in patients with idiopathic Parkinson’s disease a pilot study. J Neural Transm 112:1363–1370PubMed Mueller A, Abolmaali ND, Hakimi AR, Gloeckler T, Herting B, Reichmann H, Hummel T (2005a) Olfactory bulb volumes in patients with idiopathic Parkinson’s disease a pilot study. J Neural Transm 112:1363–1370PubMed
go back to reference Mueller A, Rodewald A, Reden J, Gerber J, von Kummer R, Hummel T (2005b) Reduced olfactory bulb volume in post-traumatic and post-infectious olfactory dysfunction. NeuroReport 16:475–478PubMed Mueller A, Rodewald A, Reden J, Gerber J, von Kummer R, Hummel T (2005b) Reduced olfactory bulb volume in post-traumatic and post-infectious olfactory dysfunction. NeuroReport 16:475–478PubMed
go back to reference Murphy C, Schubert CR, Cruickshanks KJ, Klein BE, Klein R, Nondahl DM (2002) Prevalence of olfactory impairment in older adults. JAMA 288:2307–2312PubMed Murphy C, Schubert CR, Cruickshanks KJ, Klein BE, Klein R, Nondahl DM (2002) Prevalence of olfactory impairment in older adults. JAMA 288:2307–2312PubMed
go back to reference Murphy C, Jernigan TL, Fennema-Notestine C (2003) Left hippocampal volume loss in Alzheimer’s disease is reflected in performance on odor identification: a structural MRI study. J Int Neuropsychol Soc 9:459–471PubMed Murphy C, Jernigan TL, Fennema-Notestine C (2003) Left hippocampal volume loss in Alzheimer’s disease is reflected in performance on odor identification: a structural MRI study. J Int Neuropsychol Soc 9:459–471PubMed
go back to reference Murphy C, Cerf-Ducastel B, Calhoun-Haney R, Gilbert PE, Ferdon S (2005) ERP, fMRI and functional connectivity studies of brain response to odor in normal aging and Alzheimer’s disease. Chem Senses 30(Suppl 1):i170–171PubMed Murphy C, Cerf-Ducastel B, Calhoun-Haney R, Gilbert PE, Ferdon S (2005) ERP, fMRI and functional connectivity studies of brain response to odor in normal aging and Alzheimer’s disease. Chem Senses 30(Suppl 1):i170–171PubMed
go back to reference Nigri A, Ferraro S, D’Incerti L, Critchley HD, Bruzzone MG, Minati L (2013) Connectivity of the amygdala, piriform, and orbitofrontal cortex during olfactory stimulation: a functional MRI study. NeuroReport 24:171–175PubMed Nigri A, Ferraro S, D’Incerti L, Critchley HD, Bruzzone MG, Minati L (2013) Connectivity of the amygdala, piriform, and orbitofrontal cortex during olfactory stimulation: a functional MRI study. NeuroReport 24:171–175PubMed
go back to reference Olofsson JK, Gottfried JA (2015) The muted sense: neurocognitive limitations of olfactory language. Trends Cogn Sci 19:314–321PubMedPubMedCentral Olofsson JK, Gottfried JA (2015) The muted sense: neurocognitive limitations of olfactory language. Trends Cogn Sci 19:314–321PubMedPubMedCentral
go back to reference Pellegrino R, Hahner A, Bojanowski V, Hummel C, Gerber J, Hummel T (2016) Olfactory function in patients with hyposmia compared to healthy subjects—an fMRI study. Rhinology 54:374–381PubMed Pellegrino R, Hahner A, Bojanowski V, Hummel C, Gerber J, Hummel T (2016) Olfactory function in patients with hyposmia compared to healthy subjects—an fMRI study. Rhinology 54:374–381PubMed
go back to reference Peng P, Gu H, Xiao W, Si LF, Wang JF, Wang SK, Zhai RY, Wei YX (2013) A voxel-based morphometry study of anosmic patients. Br J Radiol 86:20130207PubMedPubMedCentral Peng P, Gu H, Xiao W, Si LF, Wang JF, Wang SK, Zhai RY, Wei YX (2013) A voxel-based morphometry study of anosmic patients. Br J Radiol 86:20130207PubMedPubMedCentral
go back to reference Plailly J, Delon-Martin C, Royet JP (2012) Experience induces functional reorganization in brain regions involved in odor imagery in perfumers. Hum Brain Mapp 33:224–234PubMed Plailly J, Delon-Martin C, Royet JP (2012) Experience induces functional reorganization in brain regions involved in odor imagery in perfumers. Hum Brain Mapp 33:224–234PubMed
go back to reference Pomp J, Bestgen AK, Schulze P, Muller CJ, Citron FMM, Suchan B, Kuchinke L (2018) Lexical olfaction recruits olfactory orbitofrontal cortex in metaphorical and literal contexts. Brain Lang 179:11–21PubMed Pomp J, Bestgen AK, Schulze P, Muller CJ, Citron FMM, Suchan B, Kuchinke L (2018) Lexical olfaction recruits olfactory orbitofrontal cortex in metaphorical and literal contexts. Brain Lang 179:11–21PubMed
go back to reference Reichert JL, Postma EM, Smeets PAM, Boek WM, de Graaf K, Schopf V, Boesveldt S (2018) Severity of olfactory deficits is reflected in functional brain networks—an fMRI study. Hum Brain Mapp 39:3166–3177PubMedPubMedCentral Reichert JL, Postma EM, Smeets PAM, Boek WM, de Graaf K, Schopf V, Boesveldt S (2018) Severity of olfactory deficits is reflected in functional brain networks—an fMRI study. Hum Brain Mapp 39:3166–3177PubMedPubMedCentral
go back to reference Rombaux P, Mouraux A, Bertrand B, Nicolas G, Duprez T, Hummel T (2006a) Olfactory function and olfactory bulb volume in patients with postinfectious olfactory loss. Laryngoscope 116:436–439PubMed Rombaux P, Mouraux A, Bertrand B, Nicolas G, Duprez T, Hummel T (2006a) Olfactory function and olfactory bulb volume in patients with postinfectious olfactory loss. Laryngoscope 116:436–439PubMed
go back to reference Rombaux P, Mouraux A, Bertrand B, Nicolas G, Duprez T, Hummel T (2006b) Retronasal and orthonasal olfactory function in relation to olfactory bulb volume in patients with posttraumatic loss of smell. Laryngoscope 116:901–905PubMed Rombaux P, Mouraux A, Bertrand B, Nicolas G, Duprez T, Hummel T (2006b) Retronasal and orthonasal olfactory function in relation to olfactory bulb volume in patients with posttraumatic loss of smell. Laryngoscope 116:901–905PubMed
go back to reference Rombaux P, Weitz H, Mouraux A, Nicolas G, Bertrand B, Duprez T, Hummel T (2006c) Olfactory function assessed with orthonasal and retronasal testing, olfactory bulb volume, and chemosensory event-related potentials. Arch Otolaryngol Head Neck Surg 132:1346–1351PubMed Rombaux P, Weitz H, Mouraux A, Nicolas G, Bertrand B, Duprez T, Hummel T (2006c) Olfactory function assessed with orthonasal and retronasal testing, olfactory bulb volume, and chemosensory event-related potentials. Arch Otolaryngol Head Neck Surg 132:1346–1351PubMed
go back to reference Rombaux P, Potier H, Bertrand B, Duprez T, Hummel T (2008) Olfactory bulb volume in patients with sinonasal disease. Am J Rhinol 22:598–601PubMed Rombaux P, Potier H, Bertrand B, Duprez T, Hummel T (2008) Olfactory bulb volume in patients with sinonasal disease. Am J Rhinol 22:598–601PubMed
go back to reference Rombaux P, Potier H, Markessis E, Duprez T, Hummel T (2010) Olfactory bulb volume and depth of olfactory sulcus in patients with idiopathic olfactory loss. Eur Arch Otorhinolaryngol 267:1551–1556PubMed Rombaux P, Potier H, Markessis E, Duprez T, Hummel T (2010) Olfactory bulb volume and depth of olfactory sulcus in patients with idiopathic olfactory loss. Eur Arch Otorhinolaryngol 267:1551–1556PubMed
go back to reference Ross GW, Petrovitch H, Abbott RD, Tanner CM, Popper J, Masaki K, Launer L, White LR (2008) Association of olfactory dysfunction with risk for future Parkinson’s disease. Ann Neurol 63:167–173PubMed Ross GW, Petrovitch H, Abbott RD, Tanner CM, Popper J, Masaki K, Launer L, White LR (2008) Association of olfactory dysfunction with risk for future Parkinson’s disease. Ann Neurol 63:167–173PubMed
go back to reference Santos DV, Reiter ER, DiNardo LJ, Costanzo RM (2004) Hazardous events associated with impaired olfactory function. Arch Otolaryngol Head Neck Surg 130:317–319PubMed Santos DV, Reiter ER, DiNardo LJ, Costanzo RM (2004) Hazardous events associated with impaired olfactory function. Arch Otolaryngol Head Neck Surg 130:317–319PubMed
go back to reference Segura B, Baggio HC, Solana E, Palacios EM, Vendrell P, Bargallo N, Junque C (2013) Neuroanatomical correlates of olfactory loss in normal aged subjects. Behav Brain Res 246:148–153PubMed Segura B, Baggio HC, Solana E, Palacios EM, Vendrell P, Bargallo N, Junque C (2013) Neuroanatomical correlates of olfactory loss in normal aged subjects. Behav Brain Res 246:148–153PubMed
go back to reference Seubert J, Freiherr J, Frasnelli J, Hummel T, Lundstrom JN (2013) Orbitofrontal cortex and olfactory bulb volume predict distinct aspects of olfactory performance in healthy subjects. Cereb Cortex 23:2448–2456PubMed Seubert J, Freiherr J, Frasnelli J, Hummel T, Lundstrom JN (2013) Orbitofrontal cortex and olfactory bulb volume predict distinct aspects of olfactory performance in healthy subjects. Cereb Cortex 23:2448–2456PubMed
go back to reference Sobel N, Prabhakaran V, Desmond JE, Glover GH, Goode RL, Sullivan EV, Gabrieli JD (1998) Sniffing and smelling: separate subsystems in the human olfactory cortex. Nature 392:282–286PubMed Sobel N, Prabhakaran V, Desmond JE, Glover GH, Goode RL, Sullivan EV, Gabrieli JD (1998) Sniffing and smelling: separate subsystems in the human olfactory cortex. Nature 392:282–286PubMed
go back to reference Sobhani S, Rahmani F, Aarabi MH, Sadr AV (2019) Exploring white matter microstructure and olfaction dysfunction in early parkinson disease: diffusion MRI reveals new insight. Brain Imaging Behav 13:210–219PubMed Sobhani S, Rahmani F, Aarabi MH, Sadr AV (2019) Exploring white matter microstructure and olfaction dysfunction in early parkinson disease: diffusion MRI reveals new insight. Brain Imaging Behav 13:210–219PubMed
go back to reference Stevenson RJ (2010) An initial evaluation of the functions of human olfaction. Chem Senses 35:3–20PubMed Stevenson RJ (2010) An initial evaluation of the functions of human olfaction. Chem Senses 35:3–20PubMed
go back to reference Su M, Wang S, Fang W, Zhu Y, Li R, Sheng K, Zou D, Han Y, Wang X, Cheng O (2015) Alterations in the limbic/paralimbic cortices of Parkinson’s disease patients with hyposmia under resting-state functional MRI by regional homogeneity and functional connectivity analysis. Parkinsonism Relat Disord 21:698–703PubMed Su M, Wang S, Fang W, Zhu Y, Li R, Sheng K, Zou D, Han Y, Wang X, Cheng O (2015) Alterations in the limbic/paralimbic cortices of Parkinson’s disease patients with hyposmia under resting-state functional MRI by regional homogeneity and functional connectivity analysis. Parkinsonism Relat Disord 21:698–703PubMed
go back to reference Takeda A, Saito N, Baba T, Kikuchi A, Sugeno N, Kobayashi M, Hasegawa T, Itoyama Y (2010) Functional imaging studies of hyposmia in Parkinson’s disease. J Neurol Sci 289:36–39PubMed Takeda A, Saito N, Baba T, Kikuchi A, Sugeno N, Kobayashi M, Hasegawa T, Itoyama Y (2010) Functional imaging studies of hyposmia in Parkinson’s disease. J Neurol Sci 289:36–39PubMed
go back to reference Temmel AF, Quint C, Schickinger-Fischer B, Klimek L, Stoller E, Hummel T (2002) Characteristics of olfactory disorders in relation to major causes of olfactory loss. Arch Otolaryngol Head Neck Surg 128:635–641PubMed Temmel AF, Quint C, Schickinger-Fischer B, Klimek L, Stoller E, Hummel T (2002) Characteristics of olfactory disorders in relation to major causes of olfactory loss. Arch Otolaryngol Head Neck Surg 128:635–641PubMed
go back to reference Tobia MJ, Yang QX, Karunanayaka P (2016) Intrinsic intranasal chemosensory brain networks shown by resting-state functional MRI. NeuroReport 27:527–531PubMed Tobia MJ, Yang QX, Karunanayaka P (2016) Intrinsic intranasal chemosensory brain networks shown by resting-state functional MRI. NeuroReport 27:527–531PubMed
go back to reference van den Heuvel MP, Hulshoff Pol HE (2010) Exploring the brain network: a review on resting-state fMRI functional connectivity. Eur Neuropsychopharmacol 20:519–534PubMed van den Heuvel MP, Hulshoff Pol HE (2010) Exploring the brain network: a review on resting-state fMRI functional connectivity. Eur Neuropsychopharmacol 20:519–534PubMed
go back to reference Van Hartevelt TJ, Kringelbach ML (2011) The olfactory system. In: Mai JK, Paxinos G (eds) The human nervous system. Academic Press, San Diego, pp 1219–1238 Van Hartevelt TJ, Kringelbach ML (2011) The olfactory system. In: Mai JK, Paxinos G (eds) The human nervous system. Academic Press, San Diego, pp 1219–1238
go back to reference Vasavada MM, Wang J, Eslinger PJ, Gill DJ, Sun X, Karunanayaka P, Yang QX (2015) Olfactory cortex degeneration in Alzheimer’s disease and mild cognitive impairment. J Alzheimers Dis 45:947–958PubMed Vasavada MM, Wang J, Eslinger PJ, Gill DJ, Sun X, Karunanayaka P, Yang QX (2015) Olfactory cortex degeneration in Alzheimer’s disease and mild cognitive impairment. J Alzheimers Dis 45:947–958PubMed
go back to reference Vasavada MM, Martinez B, Wang J, Eslinger PJ, Gill DJ, Sun X, Karunanayaka P, Yang QX (2017) Central olfactory dysfunction in Alzheimer’s disease and mild cognitive impairment: a functional MRI study. J Alzheimers Dis 59:359–368PubMed Vasavada MM, Martinez B, Wang J, Eslinger PJ, Gill DJ, Sun X, Karunanayaka P, Yang QX (2017) Central olfactory dysfunction in Alzheimer’s disease and mild cognitive impairment: a functional MRI study. J Alzheimers Dis 59:359–368PubMed
go back to reference Vennemann MM, Hummel T, Berger K (2008) The association between smoking and smell and taste impairment in the general population. J Neurol 255:1121–1126PubMed Vennemann MM, Hummel T, Berger K (2008) The association between smoking and smell and taste impairment in the general population. J Neurol 255:1121–1126PubMed
go back to reference Vetter NC, Steding J, Jurk S, Ripke S, Mennigen E, Smolka MN (2017) Reliability in adolescent fMRI within two years—a comparison of three tasks. Sci Rep 7:2287PubMedPubMedCentral Vetter NC, Steding J, Jurk S, Ripke S, Mennigen E, Smolka MN (2017) Reliability in adolescent fMRI within two years—a comparison of three tasks. Sci Rep 7:2287PubMedPubMedCentral
go back to reference Wang J, You H, Liu JF, Ni DF, Zhang ZX, Guan J (2011) Association of olfactory bulb volume and olfactory sulcus depth with olfactory function in patients with Parkinson disease. AJNR Am J Neuroradiol 32:677–681PubMedPubMedCentral Wang J, You H, Liu JF, Ni DF, Zhang ZX, Guan J (2011) Association of olfactory bulb volume and olfactory sulcus depth with olfactory function in patients with Parkinson disease. AJNR Am J Neuroradiol 32:677–681PubMedPubMedCentral
go back to reference Wang J, Sun X, Yang QX (2014) Methods for olfactory fMRI studies: implication of respiration. Hum Brain Mapp 35:3616–3624PubMed Wang J, Sun X, Yang QX (2014) Methods for olfactory fMRI studies: implication of respiration. Hum Brain Mapp 35:3616–3624PubMed
go back to reference Whitcroft KL, Fischer J, Han P, Raue C, Bensafi M, Gudziol V, Andrews P, Hummel T (2018) Structural plasticity of the primary and secondary olfactory cortices: increased gray matter volume following surgical treatment for chronic rhinosinusitis. Neuroscience 395:22–34PubMed Whitcroft KL, Fischer J, Han P, Raue C, Bensafi M, Gudziol V, Andrews P, Hummel T (2018) Structural plasticity of the primary and secondary olfactory cortices: increased gray matter volume following surgical treatment for chronic rhinosinusitis. Neuroscience 395:22–34PubMed
go back to reference Woo CW, Chang LJ, Lindquist MA, Wager TD (2017) Building better biomarkers: brain models in translational neuroimaging. Nat Neurosci 20:365–377PubMedPubMedCentral Woo CW, Chang LJ, Lindquist MA, Wager TD (2017) Building better biomarkers: brain models in translational neuroimaging. Nat Neurosci 20:365–377PubMedPubMedCentral
go back to reference Wu X, Yu C, Fan F, Zhang K, Zhu C, Wu T, Li K, Chan P (2011) Correlation between progressive changes in piriform cortex and olfactory performance in early Parkinson’s disease. Eur Neurol 66:98–105PubMed Wu X, Yu C, Fan F, Zhang K, Zhu C, Wu T, Li K, Chan P (2011) Correlation between progressive changes in piriform cortex and olfactory performance in early Parkinson’s disease. Eur Neurol 66:98–105PubMed
go back to reference Yoshi A, Han P, Faria V, Hummel T (Unpublished) Top-down processing of olfactory associated information in congenital anosmia: an fMRI study Yoshi A, Han P, Faria V, Hummel T (Unpublished) Top-down processing of olfactory associated information in congenital anosmia: an fMRI study
go back to reference Yao L, Pinto JM, Yi X, Li L, Peng P, Wei Y (2014) Gray matter volume reduction of olfactory cortices in patients with idiopathic olfactory loss. Chem Senses 39:755–760PubMedPubMedCentral Yao L, Pinto JM, Yi X, Li L, Peng P, Wei Y (2014) Gray matter volume reduction of olfactory cortices in patients with idiopathic olfactory loss. Chem Senses 39:755–760PubMedPubMedCentral
go back to reference Yao L, Yi X, Pinto JM, Yuan X, Guo Y, Liu Y, Wei Y (2018) Olfactory cortex and olfactory bulb volume alterations in patients with post-infectious olfactory loss. Brain Imaging Behav 12:1355–1362PubMed Yao L, Yi X, Pinto JM, Yuan X, Guo Y, Liu Y, Wei Y (2018) Olfactory cortex and olfactory bulb volume alterations in patients with post-infectious olfactory loss. Brain Imaging Behav 12:1355–1362PubMed
go back to reference Yoneyama N, Watanabe H, Kawabata K, Bagarinao E, Hara K, Tsuboi T, Tanaka Y, Ohdake R, Imai K, Masuda M, Hattori T, Ito M, Atsuta N, Nakamura T, Hirayama M, Maesawa S, Katsuno M, Sobue G (2018) Severe hyposmia and aberrant functional connectivity in cognitively normal Parkinson’s disease. PLoS ONE 13:e0190072PubMedPubMedCentral Yoneyama N, Watanabe H, Kawabata K, Bagarinao E, Hara K, Tsuboi T, Tanaka Y, Ohdake R, Imai K, Masuda M, Hattori T, Ito M, Atsuta N, Nakamura T, Hirayama M, Maesawa S, Katsuno M, Sobue G (2018) Severe hyposmia and aberrant functional connectivity in cognitively normal Parkinson’s disease. PLoS ONE 13:e0190072PubMedPubMedCentral
go back to reference Yousem DM, Geckle RJ, Bilker WB, McKeown DA, Doty RL (1996) Posttraumatic olfactory dysfunction: MR and clinical evaluation. AJNR Am J Neuroradiol 17:1171–1179PubMedPubMedCentral Yousem DM, Geckle RJ, Bilker WB, McKeown DA, Doty RL (1996) Posttraumatic olfactory dysfunction: MR and clinical evaluation. AJNR Am J Neuroradiol 17:1171–1179PubMedPubMedCentral
go back to reference Yousem DM, Geckle RJ, Bilker WB, Doty RL (1998) Olfactory bulb and tract and temporal lobe volumes. Normative data across decades. Ann N Y Acad Sci 855:546–555PubMed Yousem DM, Geckle RJ, Bilker WB, Doty RL (1998) Olfactory bulb and tract and temporal lobe volumes. Normative data across decades. Ann N Y Acad Sci 855:546–555PubMed
go back to reference Zelano C, Mohanty A, Gottfried JA (2011) Olfactory predictive codes and stimulus templates in piriform cortex. Neuron 72:178–187PubMedPubMedCentral Zelano C, Mohanty A, Gottfried JA (2011) Olfactory predictive codes and stimulus templates in piriform cortex. Neuron 72:178–187PubMedPubMedCentral
go back to reference Zhou G, Lane G, Cooper SL, Kahnt T, Zelano C (2019) Characterizing functional pathways of the human olfactory system. Elife 8:e47177PubMedPubMedCentral Zhou G, Lane G, Cooper SL, Kahnt T, Zelano C (2019) Characterizing functional pathways of the human olfactory system. Elife 8:e47177PubMedPubMedCentral
Metadata
Title
Magnetic Resonance Imaging of Human Olfactory Dysfunction
Authors
Pengfei Han
Yunpeng Zang
Joshi Akshita
Thomas Hummel
Publication date
01-11-2019
Publisher
Springer US
Published in
Brain Topography / Issue 6/2019
Print ISSN: 0896-0267
Electronic ISSN: 1573-6792
DOI
https://doi.org/10.1007/s10548-019-00729-5

Other articles of this Issue 6/2019

Brain Topography 6/2019 Go to the issue