Skip to main content

Advertisement

Log in

Cerebellar metabolic involvement and its correlations with clinical parameters in vestibular neuritis

  • Original Communication
  • Published:
Journal of Neurology Aims and scope Submit manuscript

Abstract

Although vestibular neuritis (VN) cortical models are described in the literature, there is lack of knowledge regarding the exclusive cerebellar involvement. The aim of the present study was to analyze, by [18F] fluorodeoxyglucose-positron emission tomography (FDG-PET)/computer tomography, regional cerebellar FDG uptake in eight right-handed VN patients (five females; three males; mean age 48 ± 7 years) during the first few days (PET0) and after 1 month (PET1) since symptoms onset. At both phases, patients underwent otoneurological examination and filled in a battery of validated questionnaires. Twenty-six cerebellar volumes of interest (VOI) were identified by the automated anatomical labeling library and normalized to thalamus FDG-PET uptake. Mean intensity within VOIs was calculated in both phases and processed by within-subjects ANOVA. A significantly lower (p < 0.005) FDG uptake distribution was found in bilateral lobules III, VI and X and in vermis 1–2, 3, 6 and 10 at PET0 as compared to PET1 and a significant higher FDG uptake distribution was found in right crus I in the same comparison. Significant (p < 0.05) positive correlations were found between Anxiety and Bucket test scores, and normalized metabolism in right crus I (at PET0) and vermis 10 (at PET1), respectively. A negative correlation was found at PET0 between slow-phase velocity scores and normalized metabolism in right lobule X. These data show relevant changes in the pattern of cerebellar metabolism that might unravel additional central aspects of early and late VN associated to bilateral cortical responses to sensory conflict during the acute VN-related controversial inflow.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. Alessandrini M, Pagani M, Napolitano B, Micarelli A, Candidi M, Bruno E et al (2013) Early and phasic cortical metabolic changes in vestibular neuritis onset. PLoS One 8:e57596

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  2. Strupp M, Brandt T (2009) Vestibular neuritis. Semin Neurol 29:509–519

    Article  PubMed  Google Scholar 

  3. Pollak L, Klein C, Rafael S, Vera K, Rabey JM (2003) Anxiety in the first attack of vertigo. Otolaryngol Head Neck Surg 128:829–834

    Article  PubMed  Google Scholar 

  4. Tschan R, Wiltink J, Best C, Bense S, Dieterich M, Beutel ME et al (2008) German version of the Vertigo Symptom Scale (VSS) in patients with organic orsomatoform dizziness and healthy controls. J Neurol 255:1168–1175

    Article  CAS  PubMed  Google Scholar 

  5. Candidi M, Micarelli A, Viziano A, Aglioti SM, Minio-Paluello I, Alessandrini M (2013) Impaired mental rotation in benign paroxysmal positional vertigo and acute vestibular neuritis. Front Hum Neurosci 7:783. doi:10.3389/fnhum.2013.00783

    Article  PubMed Central  PubMed  Google Scholar 

  6. Brandt T, Bartenstein P, Janek A, Dieterich M (1998) Reciprocal inhibitory visual-vestibular interaction. Visual motion stimulation deactivates the parietoinsular vestibular cortex. Brain 121:1749–1758

    Article  PubMed  Google Scholar 

  7. 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 56:624–630

    Article  PubMed  Google Scholar 

  8. Dieterich M, Brandt T (2008) Functional brain imaging of peripheral and central vestibular disorders. Brain 131:2538–2552

    Article  PubMed  Google Scholar 

  9. Dieterich M, Brandt T (2010) Imaging cortical activity after vestibular lesions. Restor Neurol Neurosci 28:47–56

    PubMed  Google Scholar 

  10. Helmchen C, Klinkenstein J, Machner B, Rambold H, Mohr C, Sander T (2009) Structural changes in the human brain following vestibular neuritis indicate central vestibular compensation. Ann N Y Acad Sci 1164:104–115

    Article  PubMed  Google Scholar 

  11. Angelaki DE, Cullen KE (2008) Vestibular system: the many facets of a multimodal sense. Annu Rev Neurosci 31:125–150

    Article  CAS  PubMed  Google Scholar 

  12. Eulenburg P, Stoeter P, Dieterich M (2010) Voxel-based morphometry depicts central compensation after vestibular neuritis. Ann Neurol 68:241–249

    Article  PubMed  Google Scholar 

  13. Cooper CW (1993) Vestibular neuronitis: a review of a common cause of vertigo in general practice. Br J Gen Pract 43:164–167

    PubMed Central  CAS  PubMed  Google Scholar 

  14. Varrone A, Asenbaum S, Vander Borght T, Booij J, Nobili F, Någren K, European Association of Nuclear Medicine Neuroimaging Committee et al (2009) EANM procedure guidelines for PET brain imaging using [18F]FDG, version 2. Eur J Nucl Med Mol Imaging 36:2103–2110

    Article  PubMed  Google Scholar 

  15. Honrubia V (1994) Quantitative vestibular function tests and the clinical examination. In: Herdman SJ (ed) Vestibular rehabilitation. Davis, Philadelphia, pp 113–164

    Google Scholar 

  16. Zwergal A, Rettinger N, Frenzel C, Dieterich M, Brandt T, Strupp M (2009) A bucket of static vestibular function. Neurology 72:1689–1692

    Article  CAS  PubMed  Google Scholar 

  17. Gomez-Alvarez FB, Jauregui-Renaud K (2011) Psychological symptoms and spatial orientation during the first 3 months after acute unilateral vestibular lesion. Arch Med Res 42:97–103

    Article  PubMed  Google Scholar 

  18. Zung WK (1971) A rating instrument for anxiety disorders. Psychosomatics 12:371–379

    Article  CAS  PubMed  Google Scholar 

  19. Cox BJ, Swinson RP (2002) Instrument to assess depersonalization/derealization in panic disorder. Depress Anxiety 15:172–175

    Article  PubMed  Google Scholar 

  20. Pagani M, Chiò A, Valentini MC, Öberg J, Nobili F, Calvo A et al (2014) Functional pattern of brain FDG-PET in amyotrophic lateral sclerosis. Neurology (in press)

  21. Tzourio-Mazoyer N, Landeau B, Papathanassiou D, Crivello F, Etard O, Delcroix N et al (2002) Automated anatomical labelling of activations in spm using a macroscopic anatomical parcellation of the MNI MRI single subject brain. Neuroimage 15:273–289

    Article  CAS  PubMed  Google Scholar 

  22. Schmahmann JD, Doyon J, McDonald D, Holmes C, Lavoie K, Hurwitz AS et al (1999) Three-dimensional MRI atlas of the human cerebellum in proportional stereotaxic space. Neuroimage 10:233–260

    Article  CAS  PubMed  Google Scholar 

  23. Schmahmann JD (2010) The role of the cerebellum in cognition and emotion: personal reflections since 1982 on the dysmetria of thought hypothesis, and its historical evolution from theory to therapy. Neuropsychol Rev 20:236–260

    Article  PubMed  Google Scholar 

  24. Diedrichsen J (2006) A spatially unbiased atlas template of the human cerebellum. Neuroimage 33:127–138

    Article  PubMed  Google Scholar 

  25. Diedrichsen J, Balsters JH, Flavell J, Cussans E, Ramnani N (2009) A probabilistic MR atlas of the human cerebellum. Neuroimage 46:39–46

    Article  PubMed  Google Scholar 

  26. Stoodley CJ, Schmahmann JD (2009) Functional topography in the human cerebellum: a meta-analysis of neuroimaging studies. Neuroimage 44:489–501

    Article  PubMed  Google Scholar 

  27. Stoodley CJ, Valera EM, Schmahmann JD (2012) Functional topography of the cerebellum for motor and cognitive tasks: an fMRI study. Neuroimage 59:1560–1570

    Article  PubMed Central  PubMed  Google Scholar 

  28. Stoodley CJ, Schmahmann JD (2010) Evidence for topographic organization in the cerebellum of motor control versus cognitive and affective processing. Cortex 46:831–844

    Article  PubMed Central  PubMed  Google Scholar 

  29. Schmahmann JD, Macmore J, Vangel M (2009) Cerebellar stroke without motor deficit: clinical evidence for motor and non-motor domains within the human cerebellum. Neuroscience 162:852–861

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  30. Keren-Happuch E, Chen SH, Ho MH, Desmond JE (2014) A meta-analysis of cerebellar contributions to higher cognition from PET and fMRI studies. Hum Brain Mapp 35:593–615

    Article  PubMed Central  Google Scholar 

  31. Habas C, Kamdar N, Nguyen D, Prater K, Beckmann CF, Menon V et al (2009) Distinct cerebellar contributions to intrinsic connectivity networks. J Neurosci 29:8586–8594

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  32. Manni E, Petrosini L (2004) A century of cerebellar somatotopy: a debated representation. Nat Rev Neurosci 5:241–249

    Article  CAS  PubMed  Google Scholar 

  33. Krienen FM, Buckner RL (2009) Segregated fronto-cerebellar circuits revealed by intrinsic functional connectivity. Cereb Cortex 19:2485–2497

    Article  PubMed Central  PubMed  Google Scholar 

  34. O’Reilly JX, Beckmann CF, Tomassini V, Ramnani N, Johansen-Berg H (2010) Distinct and overlapping functional zones in the cerebellum defined by resting state functional connectivity. Cereb Cortex 20:953–965

    Article  PubMed Central  PubMed  Google Scholar 

  35. Martin TA, Keating JG, Goodkin HP, Bastian AJ, Thach WT (1996) Throwing while looking through prisms. II. Specificity and storage of multiple gaze-throw calibrations. Brain 119:1199–1211

    Article  PubMed  Google Scholar 

  36. Glickstein M (2000) How are visual areas of the brain connected to motor areas for the sensory guidance of movement? Trends Neurosci 23:613–617

    Article  CAS  PubMed  Google Scholar 

  37. Bauswein E, Kolb FP, Leimbeck B, Rubia FJ (1983) Simple and complex spike activity of cerebellar Purkinje cells during active and passive movements in the awake monkey. J Physiol 339:379–394

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  38. Donga R, Dessem D (1993) An unrelayed projection of jaw-muscle spindle afferents to the cerebellum. Brain Res 626:347–350

    Article  CAS  PubMed  Google Scholar 

  39. Wolpert DM, Miall RC, Kawato M (1998) Internal models in the cerebellum. Trends Cogn Sci 2:338–347

    Article  CAS  PubMed  Google Scholar 

  40. Ito M (2001) Cerebellar long-term depression: characterization, signal transduction, and functional roles. Physiol Rev 81:1143–1195

    CAS  PubMed  Google Scholar 

  41. Bays PM, Wolpert DM (2007) Computational principles of sensorimotor control that minimize uncertainty and variability. J Physiol 578:387–396

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  42. Glickstein M, Sultan F, Voogd J (2011) Functional localization in the cerebellum. Cortex 47:59–80

    Article  PubMed  Google Scholar 

  43. Voogd J, Barmack NH (2006) Oculomotor cerebellum. Prog Brain Res 151:231–268

    Article  PubMed  Google Scholar 

  44. Voogd J, Schraa-Tam CK, van der Geest JN, De Zeeuw CI (2012) Visuomotor cerebellum in human and nonhuman primates. Cerebellum 11:392–410

    Article  PubMed Central  PubMed  Google Scholar 

  45. Angelaki DE, Yakusheva TA, Green AM, Dickman JD, Blazquez PM (2010) Computation of egomotion in the macaque cerebellar vermis. Cerebellum 9:174–182

    Article  PubMed Central  PubMed  Google Scholar 

  46. Yakusheva TA, Shaikh AG, Green AM, Blazquez PM, Dickman JD, DE Angelaki (2007) Purkinje cells in posterior cerebellar vermis encode motion in an inertial reference frame. Neuron 54:973–985

    Article  CAS  PubMed  Google Scholar 

  47. Barmack NH (2003) Central vestibular system: vestibular nuclei and posterior cerebellum. Brain Res Bull 60:511–541

    Article  PubMed  Google Scholar 

  48. du Lac S, Raymond JL, Sejnowski TJ, Lisberger SG (1995) Learning and memory in the vestibulo-ocular reflex. Annu Rev Neurosci 18:409–441

    Article  PubMed  Google Scholar 

  49. du Lac S (1996) Candidate cellular mechanisms of vestibulo-ocular reflex plasticity. Ann NY Acad Sci 781:489–498

    Article  PubMed  Google Scholar 

  50. Hirata Y, Highstein SM (2000) Analysis of the discharge pattern of floccular Purkinje cells in relation to vertical head and eye movement in the squirrel monkey. Prog Brain Res 124:221–332

    Article  CAS  PubMed  Google Scholar 

  51. Blazquez PM, Hirata Y, Heiney SA, Green AM, Highstein SM (2003) Cerebellar signatures of vestibulo-ocular reflex motor learning. J Neurosci 29:9742–9751

    Google Scholar 

  52. Partsalis AM, Zhang Y, Highstein SM (1995) Dorsal Y group in the squirrel monkey. II. Contribution of the cerebellar flocculus to neuronal responses in normal and adapted animals. J Neurophysiol 73:632–650

    CAS  PubMed  Google Scholar 

  53. Rambold H, Churchland A, Selig Y, Jasmin L, Lisberger SG (2002) Partial ablations of the flocculus and ventral paraflocculus in monkeys cause linked deficits in smooth pursuit eye movements and adaptive modification of the VOR. J Neurophysiol 87:912–924

    PubMed Central  CAS  PubMed  Google Scholar 

  54. Clower DM, West RA, Lynch JC, Strick PL (2001) The inferior parietal lobule is the target of output from the superior colliculus, hippocampus, and cerebellum. J Neurosci 21:6283–6291

    CAS  PubMed  Google Scholar 

  55. Block HJ, Bastian AJ (2012) Cerebellar involvement in motor but not sensory adaptation. Neuropsychologia 50:1766–1775

    Article  PubMed Central  PubMed  Google Scholar 

  56. Alessandrini M, D’Erme G, Bruno E, Napolitano B, Magrini A (2003) Vestibular compensation: analysis of postural re-arrangement as a control index for unilateral vestibular deficit. NeuroReport 14:1075–1079

    PubMed  Google Scholar 

  57. Kipping JA, Grodd W, Kumar V, Taubert M, Villringer A, Margulies DS (2013) Overlapping and parallel cerebello-cerebral networks contributing to sensorimotor control: an intrinsic functional connectivity study. Neuroimage 83:837–848

    Article  PubMed  Google Scholar 

  58. Seeley WW, Menon V, Schatzberg AF, Keller J, Glover GH, Kenna H et al (2007) Dissociable intrinsic connectivity networks for salience processing and executive control. J Neurosci 27:2349–2356

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  59. Dimitrova A, Kolb FP, Elles FP, Maschke M, Forsting M, Diener HC et al (2003) Cerebellar responses evoked by nociceptive leg withdrawal reflex as revealed by event-related FMRI. J Neurophysiol 90:1877–1886

    Article  CAS  PubMed  Google Scholar 

  60. Wang D, Buckner RL, Liu H (2013) Cerebellar asymmetry and its relation to cerebral asymmetry estimated by intrinsic functional connectivity. J Neurophysiol 109:46–57

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  61. Fox MD, Raichle ME (2007) Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging. Nat Rev Neurosci 8:700–711

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

MichelAngela Studio generated Fig. 2 with airbrush simulation technique by using Photoshop Package for iOS and modified Fig. 3 by using the same software. The authors express sincerely thanks to MichelAngela Studio for skillful and creative craftsmanship in preparing illustrations.

Conflicts of interest

On behalf of all authors, the corresponding author states that there are no conflicts of interest.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Alessandro Micarelli.

Additional information

M. Alessandrini, A. Micarelli, O. Schillaci and M. Pagani contributed equally to this work.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Alessandrini, M., Micarelli, A., Chiaravalloti, A. et al. Cerebellar metabolic involvement and its correlations with clinical parameters in vestibular neuritis. J Neurol 261, 1976–1985 (2014). https://doi.org/10.1007/s00415-014-7449-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00415-014-7449-x

Keywords

Navigation