Brain Structure and Function

, Volume 219, Issue 4, pp 1355–1367 | Cite as

The differential effects of acute right- vs. left-sided vestibular failure on brain metabolism

  • Sandra Becker-BenseEmail author
  • Marianne Dieterich
  • Hans-Georg Buchholz
  • Peter Bartenstein
  • Mathias Schreckenberger
  • Thomas Brandt
Original Article


The human vestibular system is represented in the brain bilaterally, but it has functional asymmetries, i.e., a dominance of ipsilateral pathways and of the right hemisphere in right-handers. To determine if acute right- or left-sided unilateral vestibular neuritis (VN) is associated with differential patterns of brain metabolism in areas representing the vestibular network and the visual–vestibular interaction, patients with acute VN (right n = 9; left n = 13) underwent resting state 18F-FDG PET once in the acute phase and once 3 months later after central vestibular compensation. The contrast acute vs. chronic phase showed signal differences in contralateral vestibular areas and the inverse contrast in visual cortex areas, both more pronounced in VN right. In VN left additional regions were found in the cerebellar hemispheres and vermis bilaterally, accentuated in severe cases. In general, signal changes appeared more pronounced in patients with more severe vestibular deficits. Acute phase PET data of patients compared to that of age-matched healthy controls disclosed similarities to these patterns, thus permitting the interpretation that the signal changes in vestibular temporo-parietal areas reflect signal increases, and in visual areas, signal decreases. These data imply that brain activity in the acute phase of right- and left-sided VN exhibits different compensatory patterns, i.e., the dominant ascending input is shifted from the ipsilateral to the contralateral pathways, presumably due to the missing ipsilateral vestibular input. The visual–vestibular interaction patterns were preserved, but were of different prominence in each hemisphere and more pronounced in patients with right-sided failure and more severe vestibular deficits.


Vertigo Vestibular system PET Vestibular neuritis Visual–vestibular interaction 



Brodmann area


Fluoro-deoxyglucose positron emission tomography


Cerebral metabolic rate of glucose consumption


Subjective visual vertical


Vestibular neuritis


Volume of interest



The work was supported by the German Research Foundation (Deutsche Forschungsgemeinschaft: Di 379/4-3/4), the Foundation “Stiftung Rheinland-Pfalz für Innovation” (961-386261/759), the BMBF (01 GW 0642), and the Hertie-Foundation. Dr. Dieterich, Dr. Bartenstein, Dr. Brandt receive research support from Bundesministerium für Bildung und Forschung (BMBF). Dr. Dieterich serves on the editorial board of Annals of Neurology and received research support from Deutsche Forschungsgemeinschaft. Dr. Brandt receives support from the Hertie-Foundation. Dr. Becker-Bense, Mr. Buchholz, Dr. Schreckenberger report no disclosures.


  1. Akbarian S, Grüsser OJ, Guldin WO (1994) Corticofugal connections between the cerebral cortex and brainstem vestibular nuclei in the macaque monkey. J Comp Neurol 339:421–437PubMedCrossRefGoogle Scholar
  2. Baier B, Suchan J, Karnath HO, Dieterich M (2012) Neural correlates of disturbed perception of verticality. Neurology 78:728–735PubMedCrossRefGoogle Scholar
  3. Baloh RW (2003) Clinical practice. Vestibular neuritis. N Engl J Med 348:1027–1032PubMedCrossRefGoogle Scholar
  4. Barmack NH (2003) Central vestibular system: vestibular nuclei and posterior cerebellum. Brain Res Bull 60(5–6):511–541PubMedCrossRefGoogle Scholar
  5. Bartenstein P, Minoshima S, Hirsch C, Buch K, Willoch F, Mosch D, Schad D, Schwaiger M, Kurz A (1997) Quantitative assessment of cerebral blood flow in patients with Alzheimer`s disease by SPECT. J Nucl Med 38:1095–1101PubMedGoogle Scholar
  6. Bartenstein P, Asenbaum S, Catafau A, Halldin C, Pilowski L, Tatsch K (2002) European association of nuclear medicine procedure guidelines for brain imaging using F-18 FDG. Eur J Nucl Med 29:43–48Google Scholar
  7. Bartlett EJ, Brodie JD, Wolf AP, Christmas DR, Laska E, Meissner M (1988) Reproducibility of cerebral glucose metabolic measurements in resting human subjects. J Cereb Blood Metab 8(4):502–512CrossRefGoogle Scholar
  8. Bense S, Stephan T, Yousry TA, Brandt T, Dieterich M (2001) Multisensory cortical increases and decreases during vestibular galvanic stimulation (fMRI). J Neurophysiol 85:886–899PubMedGoogle Scholar
  9. Bense S, Bartenstein P, Lutz S, Stephan T, Schwaiger M, Brandt Th, Dieterich M (2003) Three determinants of vestibular hemispheric dominance during caloric stimulation. Ann N Y Acad Sci 1004:440–445CrossRefGoogle Scholar
  10. Bense S, Bartenstein P, Lochmann M, Schlindwein P, Brandt T, Dieterich M (2004) Metabolic changes in vestibular and visual cortices in acute vestibular neuritis. Ann Neurol 56:624–630PubMedCrossRefGoogle Scholar
  11. Bense S, Buchholz HG, Zu Eulenburg P, Best C, Bartenstein P, Schreckenberger M, Dieterich M (2012) Ventral and dorsal streams processing visual motion perception (FDG-PET study). BMC Neurosci. doi: 10.1186/1471-2202-13-81 Google Scholar
  12. Brandt T, Dieterich M (1994) Vestibular syndromes in the roll plane: topographic diagnosis from brainstem to cortex. Ann Neurol 36:337–347PubMedCrossRefGoogle Scholar
  13. Brandt T, Bartenstein P, Janek A, Dieterich M (1998) Reciprocal inhibitory visual–vestibular interaction. Visual motion stimulation deactivates the parieto-insular vestibular cortex. Brain 121:1749–1758PubMedCrossRefGoogle Scholar
  14. Chen A, DeAngelis GC, Angelaki DE (2010) Macaque parieto-insular vestibular cortex: responses to self-motion and optic flow. J Neurosci 30:3022–3042PubMedCentralPubMedCrossRefGoogle Scholar
  15. Collignon O, Voss P, Lassonde M, Lepore F (2009) Cross-modal plasticity for the spatial processing of sound in visually deprived subjects. Exp Brain Res 193:343–358CrossRefGoogle Scholar
  16. Curthoys IS, Halmagyi GM (1994) Vestibular compensation: a review of the oculomotor, neural, and clinical consequences of unilateral vestibular loss. J Vest Res 5:67–107CrossRefGoogle Scholar
  17. Dieringer N (2003) Activity-related postlesional vestibular reorganization. Ann N Y Acad Sci 1004:50–60PubMedCrossRefGoogle Scholar
  18. Dieterich M, Bense S, Lutz S, Drzezga A, Stephan T, Brandt T, Bartenstein P (2003) Dominance for vestibular cortical function in the non-dominant hemisphere. Cereb Cortex 13:994–1007PubMedCrossRefGoogle Scholar
  19. Emri M, Kisely M, Lengyel Z, Balkay L, Marian T, Miko L, Berenyi E, Sziklai I, Tron L, Toth A (2003) Cortical projection of peripheral vestibular signaling. J Neurophysiol 89:2639–2646PubMedCrossRefGoogle Scholar
  20. Fasold O, von Brevern M, Kuhberg M, Ploner CJ, Villringer A, Lempert T, Wenzel R (2002) Human vestibular cortex as identified with caloric stimulation in functional magnetic resonance imaging. NeuroImage 7(3):1384–1393CrossRefGoogle Scholar
  21. Friston KJ, Frith CD, Liddle PF et al (1990) The relationship between global and local changes in PET scans. Hum Brain Mapp 13:1038–1040Google Scholar
  22. Friston KJ, Asburner J, Frith CD et al (1995a) Spatial registration and normalization of images. Hum Brain Mapp 2:165–189CrossRefGoogle Scholar
  23. Friston KJ, Holmes AP, Worsley KJ et al (1995b) Statistical parametric maps in functional imaging: a general linear approach. Hum Brain Mapp 2:189–210CrossRefGoogle Scholar
  24. Gispert JD, Pascau J, Reig S, Martínez-Lázaro R, Molina V, García-Barreno P, Desco M (2003) Influence of the normalization template on the outcome of statistical parametric mapping of PET scans. NeuroImage 19:601–612PubMedCrossRefGoogle Scholar
  25. Goto F, Straka H, Dieringer N (2001) Postlesional vestibular reorganization in frogs: evidence for a basic reaction pattern after nerve injury. J Neurophysiol 85(6):2643–6246PubMedGoogle Scholar
  26. Guilding C, Dutia MB (2005) Early and late changes in vestibular neuronal excitability after deafferentation. NeuroReport 16:1415–1418PubMedCrossRefGoogle Scholar
  27. Guldin WO, Grüsser OJ (1996) The anatomy of the vestibular cortices of primates. In: Collard M, Jeannerod M, Christen Y (eds) Le cortex vestibulaire. Editions IRVINN, Ipsen, pp 17–26Google Scholar
  28. Halmagyi GM, Weber KP, Curthoys IS (2010) Vestibular function after acute vestibular neuritis. Restor Neurol Neurosci 28(1):37–46PubMedGoogle Scholar
  29. Honrubia V (1994) Quantitative vestibular function tests and the clinical examination. In: Herdman SJ (ed) Vestibular rehabilitation. Davis, Philadelphia, pp 113–164Google Scholar
  30. Jongkees LBW, Maas JPM, Philipszoon AJ (1962) Clinical nystagmography: a detailed study of electro-nystagmography in 341 patients with vertigo. Pract Otorhinolaryngol 24:65–93Google Scholar
  31. Kleinschmidt A, Thilo KV, Büchel C, Gresty MA, Bronstein AM, Frackowiak RSJ (2002) Neuronal correlates of visual-motion perception as object- or self-motion. NeuroImage 16:873–882PubMedCrossRefGoogle Scholar
  32. Laurienti PJ, Burdette JH, Wallace MT, Yen YF, Field AS, Stein BE (2002) Deactivation of sensory-specific cortex by cross-modal stimuli. J Cogn Neurosci 14:420–429PubMedCrossRefGoogle Scholar
  33. Lobel E, Kleine JF, Le Bihan D, Leroy-Willig A, Berthoz A (1998) Functional MRI of galvanic vestibular stimulation. J Neurophysiol 80:2699–2709PubMedGoogle Scholar
  34. Lumer ED, Friston KJ, Rees G (1998) Neural correlates of perceptual rivalry in the human brain. Science 280:1930–1934PubMedCrossRefGoogle Scholar
  35. Maihöfner C, Handwerker HO, Birklein F (2006) Functional imaging of allodynia in complex regional pain syndrome. Neurology 66(5):711–717PubMedCrossRefGoogle Scholar
  36. Mast FW, Merfeld DM, Kosslyn SM (2006) Visual mental imagery during caloric vestibular stimulation. Neuropsychologia 44(1):101–109PubMedCentralPubMedCrossRefGoogle Scholar
  37. Merabet LB, Swisher JD, McMains SA, Halko MA, Amedi A, Pascual-Leone A, Somers DC (2007) Combined activation and deactivation of visual cortex during tactile sensory processing. J Neurophysiol 97:633–1641Google Scholar
  38. Miyamato T, Fukushima K, Takada T, de Waele C, Vidal PP (2007) Saccular stimulation of the human cortex: a functional magnetic resonance imaging study. Neurosci Lett 423(1):68–72CrossRefGoogle Scholar
  39. Naidich TP, Brightbill TC (2003) Vascular territories and watersheds: a zonal frequency analysis of the gyral and sulcal extent of cerebral infarcts. Part I: the anatomic template. Neuroradiology 45:536–540PubMedCrossRefGoogle Scholar
  40. Naito Y, Tateya I, Hirano S, Inoue M, Funabiki K, Toyoda H, Ueno M, Ishizu K, Nagahama Y, Fukuyama H, Ito J (2003) Cortical correlates of vestibulo-ocular reflex modulation: a PET study. Brain 126:1562–1578PubMedCrossRefGoogle Scholar
  41. Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9:97–113PubMedCrossRefGoogle Scholar
  42. Ptito M, Matteau I, Zhi Wang A, Paulson OB, Siebner HR, Kupers R (2012) Crossmodal recruitment of the ventral stream in congenital blindness. Neural Plat. doi: 10.1155/2012/304045 Google Scholar
  43. Schlindwein P, Mueller M, Bauermann T, Brandt T, Stoeter P, Dieterich M (2008) Cortical representation of saccular vestibular stimulation: VEMPs in fMRI. NeuroImage 39(1):19–31PubMedCrossRefGoogle Scholar
  44. Stephan T, Deutschländer A, Nolte A, Schneider E, Wiesmann M, Brandt T, Dieterich M (2005) Functional MRI of galvanic vestibular stimulation with alternating currents at different frequencies. Neuroimage 26:721–732PubMedCrossRefGoogle Scholar
  45. Talairach J, Tournoux P (1988) Co-planar Stereotaxic Atlas of the Human Brain. Georg Thieme Verlag, StuttgartGoogle Scholar
  46. Théoret H, Merabet L, Pasqual-Leone A (2004) Behavioural and neuroplastic changes in the blind: evidence for functionally relevant cross-modal interactions. J Physiol Paris 98:221–233PubMedCrossRefGoogle Scholar
  47. Wenzel R, Bartenstein P, Dieterich M, Danek A, Weindl A, Minoshima S, Ziegler S, Schwaiger M, Brandt T (1996) Deactivation of human visual cortex during involuntary ocular oscillations. A PET activation study. Brain 119:101–110PubMedCrossRefGoogle Scholar
  48. Wienhard K, Eriksson L, Grootoonk S, Casey M, Pietrzyk U, Heiss WD (1992) Performance evaluation of the positron scanner ECAT EXACT. J Comput Assist Tomogr 16:804–813PubMedCrossRefGoogle Scholar
  49. Worsley KJ, Evans AC, Marrett S, Neelin P (1992) A three-dimensional statistical analysis for CBF activation studies in human brain. J Cereb Blood Flow Metab 12:900–918PubMedCrossRefGoogle Scholar
  50. Yamanaka T, Him A, Cameron SA, Dutia MB (2000) Rapid compensatory changes in GABA receptor efficacy in rat vestibular neurons after unilateral labyrinthectomy. J Physiol 523:413–424PubMedCentralPubMedCrossRefGoogle Scholar
  51. Yousry TA, Schmid UD, Alkadhi H, Schmidt D, Peraud A, Büttner A, Winkler P (1997) Localization of the motor hand area to a knob on the precentral gyrus. A new landmark. Brain 120:141–157PubMedCrossRefGoogle Scholar
  52. Zu Eulenburg P, Caspers S, Roski C, Eickhoff SB (2012) Meta-analytical definition and functional connectivity of the human vestibular cortex. Neuroimage 60:162–169PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Sandra Becker-Bense
    • 1
    • 2
    Email author
  • Marianne Dieterich
    • 1
    • 2
    • 5
  • Hans-Georg Buchholz
    • 6
  • Peter Bartenstein
    • 2
    • 3
    • 5
  • Mathias Schreckenberger
    • 6
  • Thomas Brandt
    • 2
    • 4
  1. 1.Department of NeurologyLudwig-Maximilians-University MunichMunichGermany
  2. 2.The German Center for Vertigo and Balance Disorders (IFB-LMU)University of Munich HospitalMunichGermany
  3. 3.Department of Nuclear MedicineLudwig-Maximilians-University MunichMunichGermany
  4. 4.Institute of Clinical NeuroscienceLudwig-Maximilians-University MunichMunichGermany
  5. 5.Munich Cluster for Systems Neurology (SyNergy)MunichGermany
  6. 6.Department of Nuclear MedicineJohannes Gutenberg-UniversityMainzGermany

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