Neural plasticity in developing and adult olfactory pathways – focus on the human olfactory bulb

Huart, C.; Rombaux, Ph; Hummel, T.

doi:10.1007/s10863-018-9780-x

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Published: 03 January 2019

Neural plasticity in developing and adult olfactory pathways – focus on the human olfactory bulb

Journal of Bioenergetics and Biomembranes volume 51, pages 77–87 (2019)Cite this article

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Abstract

The topic of human adult neural plasticity and neurogenesis is of great interest for medical and scientific community, but it is also largely debated. In the last years, an increasing interest has been paid to the olfactory system, and particularly to the plasticity of the olfactory bulb (OB). While the molecular/cellular mechanisms underlying OB plasticity remain a matter of debate, measurements of the OB using magnetic resonance imaging clearly indicate that it is a highly plastic structure. In this review, we present results regarding the plasticity of the human adult olfactory system.

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References

Altundag A, Salihoglu M, Tekeli H, Saglam M, Cayonu M, Hummel T (2014) Lateralized differences in olfactory function and olfactory bulb volume relate to nasal septum deviation. J Craniofac Surg 25:359–362. https://doi.org/10.1097/SCS.0000000000000617
Article PubMed Google Scholar
Alvarez-Buylla A, Kohwi M, Nguyen TM, Merkle FT (2008) The heterogeneity of adult neural stem cells and the emerging complexity of their niche. Cold Spring Harb Symp Quant Biol 73:357–365. https://doi.org/10.1101/sqb.2008.73.019
Article CAS PubMed Google Scholar
Askar SM et al (2015) Ipsilateral reduced olfactory bulb volume in patients with unilateral nasal obstruction. Otolaryngolo Head Neck Surg 152:959–963. https://doi.org/10.1177/0194599815573196
Article Google Scholar
Attems J, Lintner F, Jellinger KA (2005) Olfactory involvement in aging and Alzheimer's disease: an autopsy study. J Alzheimers Dis 7:149–157 discussion 173-180
Article CAS PubMed Google Scholar
Benson TE, Ryugo DK, Hinds JW (1984) Effects of sensory deprivation on the developing mouse olfactory system: a light and electron microscopic, morphometric analysis. J Neurosci 4:638–653
Article CAS PubMed Google Scholar
Bergmann O et al (2012) The age of olfactory bulb neurons in humans. Neuron 74:634–639. https://doi.org/10.1016/j.neuron.2012.03.030
Article CAS PubMed Google Scholar
Bergmann O, Spalding KL, Frisen J (2015) Adult Neurogenesis in Humans. Cold Spring Harb Perspect Biol 7:a018994. https://doi.org/10.1101/cshperspect.a018994
Article CAS PubMed PubMed Central Google Scholar
Bhatnagar KP, Kennedy RC, Baron G, Greenberg RA (1987) Number of mitral cells and the bulb volume in the aging human olfactory bulb: a quantitative morphological study. Anat Rec 218:73–87. https://doi.org/10.1002/ar.1092180112
Article CAS PubMed Google Scholar
Breton-Provencher V, Bakhshetyan K, Hardy D, Bamman RR, Cavarretta F, Snapyan M, Côté D, Migliore M, Saghatelyan A (2016) Principal cell activity induces spine relocation of adult-born internuerons in the olfactory bulb. Nat Commun 7:12659
Article CAS PubMed PubMed Central Google Scholar
Buck L, Axel R (1991) A novel multigene family may encode odorant receptors: a molecular basis for odor recognition. Cell 65:175–187
Article CAS PubMed Google Scholar
Burmeister HP, Bitter T, Baltzer PA, Dietzel M, Guntinas-Lichius O, Gudziol H, Kaiser WA (2011a) Olfactory bulb ventricles as a frequent finding--a myth or reality? Evaluation using high resolution 3 tesla magnetic resonance imaging. Neuroscience 172:547–553. https://doi.org/10.1016/j.neuroscience.2010.10.068
Article CAS PubMed Google Scholar
Burmeister HP, Baltzer PA, Mölstein C, Bitter T, Gudziol H, Dietzel M, Guntinas-Lichius O, Kaiser WA (2011b) Reproducibility and repaetability of volumetric measurements for olfactory bulb volumetry: which method is appropriate? An update using 3 Tesla MRI. Acad Radiol 18(7):842–849. https://doi.org/10.1016/j.arca.2011.02.018
Article PubMed Google Scholar
Burmeister HP et al (2012) Imaging of lamination patterns of the adult human olfactory bulb and tract: in vitro comparison of standard- and high-resolution 3T MRI, and MR microscopy at 9.4 T. NeuroImage 60:1662–1670. https://doi.org/10.1016/j.neuroimage.2012.01.101
Article PubMed Google Scholar
Buschhuter D, Smitka M, Puschmann S, Gerber JC, Witt M, Abolmaali ND, Hummel T (2008) Correlation between olfactory bulb volume and olfactory function. NeuroImage 42:498–502. https://doi.org/10.1016/j.neuroimage.2008.05.004
Article CAS PubMed Google Scholar
Carlen M, Cassidy RM, Brismar H, Smith GA, Enquist LW, Frisen J (2002) Functional integration of adult-born neurons. Current Biol 12:606–608
Article CAS Google Scholar
Chen Y, Getchell TV, Sparks DL, Getchell ML (1993) Patterns of adrenergic and peptidergic innervation in human olfactory mucosa: age-related trends. J Comp Neurol 334:104–116. https://doi.org/10.1002/cne.903340109
Article CAS PubMed Google Scholar
Cleland TA, Linster C (2005) Computation in the olfactory system. Chem Senses 30:801–813. https://doi.org/10.1093/chemse/bji072
Article PubMed Google Scholar
Conley DB, Robinson AM, Shinners MJ, Kern RC (2003) Age-related olfactory dysfunction: cellular and molecular characterization in the rat. Am J Rhinol 17:169–175
Article PubMed Google Scholar
Crasto C, Marenco L, Miller P, Shepherd G (2002) Olfactory receptor database: A metadata-driven automated population from sources of gene and protein sequences. Nucleic Acids Res:354–360
Croy I, Negoias S, Symmank A, Schellong J, Joraschky P, Hummel T (2013) Reduced olfactory bulb volume in adults with a history of childhood maltreatment. Chem Senses 38:679–684. https://doi.org/10.1093/chemse/bjt037
Article PubMed Google Scholar
Cummings DM, Brunjes PC (1997) The effects of variable periods of functional deprivation on olfactory bulb development in rats. Exp Neurol 148:360–366. https://doi.org/10.1006/exnr.1997.6660
Article CAS PubMed Google Scholar
Curtis MA et al (2007) Human neuroblasts migrate to the olfactory bulb via a lateral ventricular extension. Science 315:1243–1249. https://doi.org/10.1126/science.1136281
Article CAS PubMed Google Scholar
Doetsch F, Caille I, Lim DA, Garcia-Verdugo JM, Alvarez-Buylla A (1999) Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell 97:703–716
Article CAS PubMed Google Scholar
Duprez TP, Rombaux P (2010) Imaging the olfactory tract (cranial nerve #1). Eur J Radiol 74:288–298. https://doi.org/10.1016/j.ejrad.2009.05.065
Article PubMed Google Scholar
Ennis M, Holy TE (2015) Anatomy and neurobiology of the Main and accessory olfactory bulbs. In: Doty RL (ed) Handbook of olfaction and gustation. John Wiley & Sons, pp 157-182
Goktas O, Cao Van H, Fleiner F, Lacroix JS, Landis BN (2010) Chemosensory function in Wegener's granulomatosis: a preliminary report. Eur Arch Otorhinolaryngol 267:1089–1093. https://doi.org/10.1007/s00405-009-1184-4
Article PubMed Google Scholar
Gritti A, Bonfanti L, Doetsch F, Caille I, Alvarez-Buylla A, Lim DA, Galli R, Verdugo JMG, Herrera DG, Vescovi AL (2002) Multipotent neural stem cells reside into the rostral extension and olfactory bulb of adult rodents. J Neurosci 22:437–445
Article CAS PubMed Google Scholar
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 132:3096–3101. https://doi.org/10.1093/brain/awp243
Article CAS PubMed Google Scholar
Guerrero-Cazares H, Gonzalez-Perez O, Soriano-Navarro M, Zamora-Berridi G, Garcia-Verdugo JM, Quinones-Hinojosa A (2011) Cytoarchitecture of the lateral ganglionic eminence and rostral extension of the lateral ventricle in the human fetal brain. J Comp Neurol 519:1165–1180. https://doi.org/10.1002/cne.22566
Article PubMed Google Scholar
Haehner A, Rodewald A, Gerber JC, Hummel T (2008) Correlation of olfactory function with changes in the volume of the human olfactory bulb. Arch of Otolaryngol Head Neck Surg 134:621–624. https://doi.org/10.1001/archotol.134.6.621
Article Google Scholar
Hardy D, Saghatelyan A (2017) Different forms of structural plasticity in the adult olfactory bulb. Neurogenesis 4(1):e1301850. https://doi.org/10.1080/23262133.2017.1301850
Article PubMed PubMed Central Google Scholar
Hoogland PV, van den Berg R, Huisman E (2003) Misrouted olfactory fibres and ectopic olfactory glomeruli in normal humans and in Parkinson and Alzheimer patients. Neuropathol Appl Neurobiol 29:303–311
Article CAS PubMed Google Scholar
Hummel T, Heilmann S, Murphy C (2002) Age-related changes of chemosensory function. In: Rouby C, Schaal B, Dubois D, Gervais R, Holley A (eds) Olfaction, taste, and cognition. Cambridge University Press, New York, pp 441–456
Chapter Google Scholar
Hummel T, Kobal G, Gudziol H, Mackay-Sim A (2007) Normative data for the "Sniffin' sticks" including tests of odor identification, odor discrimination, and olfactory thresholds: an upgrade based on a group of more than 3,000 subjects. Eur Arch Otorhinolaryngol 264:237–243. https://doi.org/10.1007/s00405-006-0173-0
Article CAS PubMed Google Scholar
Hummel T, Haehner A, Hummel C, Croy I, Iannilli E (2013a) Lateralized differences in olfactory bulb volume relate to lateralized differences in olfactory function. Neuroscience 237:51–55. https://doi.org/10.1016/j.neuroscience.2013.01.044
Article CAS PubMed Google Scholar
Hummel T et al (2013b) Olfactory bulb volume in patients with temporal lobe epilepsy. J Neurology 260:1004–1008. https://doi.org/10.1007/s00415-012-6741-x
Article Google Scholar
Jones-Gotman M, Zatorre RJ (1988) Olfactory identification deficits in patients with focal cerebral excision. Neuropsychologia 26:387–400
Article CAS PubMed Google Scholar
Kaneko N et al (2010) New neurons clear the path of astrocytic processes for their rapid migration in the adult brain. Neuron 67:213–223. https://doi.org/10.1016/j.neuron.2010.06.018
Article CAS PubMed PubMed Central Google Scholar
Kornack DR, Rakic P (2001) The generation, migration, and differentiation of olfactory neurons in the adult primate brain. Proc Natl Acad Sci U S A 98:4752–4757. https://doi.org/10.1073/pnas.081074998
Article CAS PubMed PubMed Central Google Scholar
Kovacs T, Cairns NJ, Lantos PL (1999) Beta-amyloid deposition and neurofibrillary tangle formation in the olfactory bulb in ageing and Alzheimer's disease. Neuropathol Appl Neurobiol 25:481–491
Article CAS PubMed Google Scholar
Lazarini F, Lledo PM (2011) Is adult neurogenesis essential for olfaction? Trends Neurosci 34:20–30. https://doi.org/10.1016/j.tins.2010.09.006
Article CAS PubMed Google Scholar
Linster C, Cleland TA (2002) Cholinergic modulation of sensory representations in the olfactory bulb Neural networks : the official. J Int Neural Network Society 15:709–717
Article Google Scholar
Lledo PM, Gheusi G (2003) Olfactory processing in a changing brain. Neuroreport 14:1655–1663. https://doi.org/10.1097/01.wnr.0000092070.64779.76
Article PubMed Google Scholar
Lois C, Garcia-Verdugo JM, Alvarez-Buylla A (1996) Chain migration of neuronal precursors. Science 271:978–981
Article CAS PubMed Google Scholar
Lotsch J et al (2013) Functional genomics suggest neurogenesis in the adult human olfactory bulb. Brain Struct Funct. https://doi.org/10.1007/s00429-013-0618-3
Maresh A, Rodriguez GD, Whitman MC, Greer, CA (2008) Principles of glomerular organization in the human olfactory bulb – implications for odor processing Plos One 9;3(7):e2640 doi:https://doi.org/10.1371/journal.pone.0002640
McLean JH, Harley CW (2004) Olfactory learning in the rat pup: a model that may permit visualization of a mammalian memory trace. Neuroreport 15:1691–1697
Article CAS PubMed Google Scholar
Meisami E, Mikhail L, Baim D, Bhatnagar KP (1998) Human olfactory bulb: aging of glomeruli and mitral cells and a search for the accessory olfactory bulb. Ann N Y Acad Sci 855:708–715
Article CAS PubMed Google Scholar
Mineur YS, Belzung C, Crusio WE (2007) Functional implications of decreases in neurogenesis following chronic mild stress in mice. Neuroscience 150:251–259. https://doi.org/10.1016/j.neuroscience.2007.09.045
Article CAS PubMed Google Scholar
Ming GL, Song H (2011) Adult neurogenesis in the mammalian brain: significant answers and significant questions. Neuron 70:687–702. https://doi.org/10.1016/j.neuron.2011.05.001
Article CAS PubMed PubMed Central Google Scholar
Mizrahi A (2003) Dendritic stability in the adult olfactory bulb. Nat Neurosci 6(11):1201–1207
Article CAS PubMed Google Scholar
Mizrahi A (2007) Dendritic development and plasticity of adult-born neurons in the mouse olfactory bulb. Nat Neurosci 10(4):444–452
Article CAS PubMed Google Scholar
Moberg PJ, Doty RL, Mahr RN, Mesholam RI, Arnold SE, Turetsky BI, Gur RE (1997) Olfactory identification in elderly schizophrenia and Alzheimer's disease. Neurobiol Aging 18:163–167
Article CAS PubMed Google Scholar
Mombaerts P, Wang F, Dulac C, Chao SK, Nemes A, Mendelsohn M, Edmondson J, Axel R (1996) Visualizing an olfactory sensory map. Cell 87:675–686
Article CAS PubMed Google Scholar
Morizumi T, Tsukatani H, Miwa T (1994) Olfactory disturbance induced by deafferentation of serotoninergic fibers in the olfactory bulb. Neuroscience 61:733–738
Article Google Scholar
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 (Vienna) 112:1363–1370. https://doi.org/10.1007/s00702-005-0280-x
Article CAS Google Scholar
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 16:475–478
Article PubMed Google Scholar
Murphy C, Schubert CR, Cruickshanks KJ, Klein BE, Klein R, Nondahl DM (2002) Prevalence of olfactory impairment in older adults. JAMA 288:2307–2312
Article PubMed Google Scholar
Naessen R (1971) An enquiry on the morphological characteristics and possible changes with age in the olfactory region of man. Acta Otolaryngol 71:49–62
Article CAS PubMed Google Scholar
Nagayama S, Homma R, Imamura F (2014) Neuronal organization of olfactory bulb circuits. Front Neural Circuits 3(8):98. https://doi.org/10.3389/fncir.2014.00098
Article Google Scholar
Negoias S, Croy I, Gerber J, Puschmann S, Petrowski K, Joraschky P, Hummel T (2010) Reduced olfactory bulb volume and olfactory sensitivity in patients with acute major depression. Neuroscience 169:415–421. https://doi.org/10.1016/j.neuroscience.2010.05.012
Article CAS PubMed Google Scholar
Negoias S, Pietsch K, Hummel T (2017) Changes in olfactory bulb volume following lateralized olfactory training. Brain Imaging Behav 11:998–1005. https://doi.org/10.1007/s11682-016-9567-9
Article CAS PubMed Google Scholar
Nguyen AD, Pelavin PE, Shenton ME, Chilakamarri P, McCarley RW, Nestor PG, Levitt JJ (2011) Olfactory sulcal depth and olfactory bulb volume in patients with schizophrenia: an MRI study. Brain Imaging Behav 5:252–261. https://doi.org/10.1007/s11682-011-9129-0
Article PubMed Google Scholar
Pagano SF et al (2000) Isolation and characterization of neural stem cells from the adult human olfactory bulb. Stem Cells 18:295–300. https://doi.org/10.1634/stemcells.18-4-295
Article CAS PubMed Google Scholar
Paik SI, Lehman MN, Seiden AM, Duncan HJ, Smith DV (1992) Human olfactory biopsy. The influence of age and receptor distribution. Arc Otolaryngol Head Neck Surge 118:731–738
Article CAS Google Scholar
Paredes MF, Sorrells SF, Garcia-Verdugo JM, Alvarez-Buylla A (2016) Brain size and limits to adult neurogenesis. J Comp Neurol 524:646–664. https://doi.org/10.1002/cne.23896
Article PubMed Google Scholar
Pozzati E, Martinoni M, Marucci G, Bacci A (2014) Olfactory neuroblastoma and olfactory ventricle. A case report. Neuroradiol J 27:452–455. https://doi.org/10.15274/NRJ-2014-10060
Article PubMed PubMed Central Google Scholar
Rawson NE (2006) Olfactory loss in aging. Sci Aging knowledge Environ 2006(pe6). https://doi.org/10.1126/sageke.2006.5.pe6
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 116:436–439. https://doi.org/10.1097/01.MLG.0000195291.36641.1E
Article PubMed Google Scholar
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 116:901–905. https://doi.org/10.1097/01.mlg.0000217533.60311.e7
Article PubMed Google Scholar
Rombaux P, Potier H, Bertrand B, Duprez T, Hummel T (2008) Olfactory bulb volume in patients with sinonasal disease. Am J Rhinol 22:598–601. https://doi.org/10.2500/ajr.2008.22.3237
Article PubMed Google Scholar
Rombaux P, Grandin C, Duprez T (2009) How to measure olfactory bulb volume and olfactory sulcus depth? B-Ent 5(Suppl 13):53–60
PubMed Google Scholar
Rombaux P, Huart C, De Volder AG, Cuevas I, Renier L, Duprez T, Grandin C (2010a) Increased olfactory bulb volume and olfactory function in early blind subjects. Neuroreport 21:1069–1073. https://doi.org/10.1097/WNR.0b013e32833fcb8a
Article PubMed Google Scholar
Rombaux P, Potier H, Markessis E, Duprez T, Hummel T (2010b) Olfactory bulb volume and depth of olfactory sulcus in patients with idiopathic olfactory loss. Eur Arch Otorhinolaryngol 267:1551–1556. https://doi.org/10.1007/s00405-010-1230-2
Article PubMed Google Scholar
Rottstadt F et al (2018) Reduced olfactory bulb volume in depression-a structural moderator analysis. Hum Brain Mapp 39:2573–2582. https://doi.org/10.1002/hbm.24024
Article PubMed Google Scholar
Samaulhaq MT, Lone KP (2008) Age and gender related differences in olfactory bulb glomeruli in human. Biomedica 24:12–17
Google Scholar
Sanai N et al (2004) Unique astrocyte ribbon in adult human brain contains neural stem cells but lacks chain migration. Nature 427:740–744. https://doi.org/10.1038/nature02301
Article CAS PubMed Google Scholar
Sanai N et al (2011) Corridors of migrating neurons in the human brain and their decline during infancy. Nature 478:382–386. https://doi.org/10.1038/nature10487
Article CAS PubMed PubMed Central Google Scholar
Schwob JE (2002) Neural regeneration and the peripheral olfactory system. Anat Rec 269:33–49
Article PubMed Google Scholar
Shiga H et al (2013) Assessment of olfactory nerve by SPECT-MRI image with nasal thallium-201 administration in patients with olfactory impairments in comparison to healthy volunteers. PloS One 8:e57671. https://doi.org/10.1371/journal.pone.0057671
Article CAS PubMed PubMed Central Google Scholar
Smitka M et al (2009) Olfactory bulb ventricles as a frequent finding in magnetic resonance imaging studies of the olfactory system. Neuroscience 162:482–485. https://doi.org/10.1016/j.neuroscience.2009.04.058
Article CAS PubMed Google Scholar
Sorokowska A, Sorokowski P, Karwowski M, Larsson M, Hummel T (2018) Olfactory perception and blindness: a systematic review and meta-analysis. Psychol Res. https://doi.org/10.1007/s00426-018-1035-2
Tanik N, Serin HI, Celikbilek A, Inan LE, Gundogdu F (2015) Olfactory bulb and olfactory sulcus depths are associated with disease duration and attack frequency in multiple sclerosis patients. J Neuro Sci 358:304–307. https://doi.org/10.1016/j.jns.2015.09.016
Article Google Scholar
Thomann PA, Dos Santos V, Toro P, Schonknecht P, Essig M, Schroder J (2009) Reduced olfactory bulb and tract volume in early Alzheimer's disease--a MRI study. Neurobiol Aging 30:838–841. https://doi.org/10.1016/j.neurobiolaging.2007.08.001
Article PubMed Google Scholar
Turetsky BI, Moberg PJ, Yousem DM, Doty RL, Arnold SE, Gur RE (2000) Reduced olfactory bulb volume in patients with schizophrenia. Am J Psychiatry 157:828–830. https://doi.org/10.1176/appi.ajp.157.5.828
Article CAS PubMed Google Scholar
Veyseller B, Aksoy F, Yildirim YS, Bayraktar FG, Gurbuz D, Savas Y, Ozturan O (2011) Reduced olfactory bulb volume in total laryngectomy patients: a magnetic resonance imaging study. Rhinology 49:112–116. https://doi.org/10.4193/Rhino10.001
CAS Article PubMed Google Scholar
von Gudden B (1870) Experimentaluntersuchungen ueber das periphere und zentrale. Nervensystem Archiv f Psychiatrie u Nervenkrankheiten 2:693–723
Article Google Scholar
Wang C et al (2011a) Identification and characterization of neuroblasts in the subventricular zone and rostral migratory stream of the adult human brain. Cell Res 21:1534–1550. https://doi.org/10.1038/cr.2011.83
Article CAS PubMed PubMed Central Google Scholar
Wang J, You H, Liu JF, Ni DF, Zhang ZX, Guan J (2011b) Association of olfactory bulb volume and olfactory sulcus depth with olfactory function in patients with Parkinson disease. AJNR Am J Neuroradiol 32:677–681. https://doi.org/10.3174/ajnr.A2350
Article CAS PubMed Google Scholar
Wilson DA, Fletcher ML, Sullivan RM (2004) Acetylcholine and olfactory perceptual learning. Learn Mem 11:28–34
Article PubMed PubMed Central Google Scholar
Yaldizli O et al (2016) The association between olfactory bulb volume, cognitive dysfunction, physical disability and depression in multiple sclerosis. Eur J Neurol 23:510–519. https://doi.org/10.1111/ene.12891
Article CAS PubMed Google Scholar
Yousem DM, Geckle RJ, Bilker WB, McKeown DA, Doty RL (1996) Posttraumatic olfactory dynfunction: MR and clinical evaluation. AJNR 17:1171–1179
CAS PubMed Google Scholar
Yousem DM, Geckle RJ, Doty RL, Bulker WB (1997) Reproducibility and reliability of volumetric measurements of olfactory eloquent structures. Acad Radiol 4(4):264–269
Article CAS PubMed Google Scholar
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 855:546–555
Article CAS PubMed Google Scholar
Yousem DM, Geckle RJ, Bilker WB, Kroger H, Doty RL (1999) Posttraumatic smell loss: Relationship of psychophysical tests and volumes of the olfactory bulbs and tracts and the temporal lobes. Acad Radiol 6:264–272
Article CAS PubMed Google Scholar
Yuan Q, Harley CW, McLean JH (2003) Mitral cell a1 and 5-HT2A receptor colocalization and cAMP coregulation: a new model of norepinephrine-induced learning in the olfactory bulb. Learn Mem 10:5–15
Article PubMed PubMed Central Google Scholar
Zhang K, Yu C, Zhang Y, Wu X, Zhu C, Chan P, Li K (2011) Voxel-based analysis of diffusion tensor indices in the brain in patients with Parkinson's disease. Eur J Radiol 77:269–273. https://doi.org/10.1016/j.ejrad.2009.07.032
Article PubMed Google Scholar

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Department of Otorhinolaryngology, Cliniques universitaires Saint-Luc, Brussels, Belgium
C. Huart & Ph Rombaux
Institute of Neuroscience, Université catholique de Louvain, Brussels, Belgium
C. Huart & Ph Rombaux
Smell and Taste Clinic, Department of Otorhinolaryngology, TU Dresden, Fetscherstrasse 74, 01307, Dresden, Germany
T. Hummel

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Huart, C., Rombaux, P. & Hummel, T. Neural plasticity in developing and adult olfactory pathways – focus on the human olfactory bulb. J Bioenerg Biomembr 51, 77–87 (2019). https://doi.org/10.1007/s10863-018-9780-x

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Received: 12 July 2018
Accepted: 23 November 2018
Published: 03 January 2019
Issue Date: 15 February 2019
DOI: https://doi.org/10.1007/s10863-018-9780-x

Keywords

Smell
Anosmia
Nose
Plasticity
Neuroregeneration