Skip to main content
SpringerLink
Log in

Specific activation of operculum 3 (OP3) brain region during provoked tinnitus-related phantom auditory perceptions in humans

  • Original Article
  • Published:
Brain Structure and Function Aims and scope Submit manuscript

Abstract

The phantom sound perception mechanism by which a sound perception occurs without any external sound source is still enigmatic. According to our previous fMRI study, a small region in the parietal operculum 3 was hyperactivated as a function of tinnitus periodicity in subjects with acoustic trauma tinnitus sequelae. This region was localized in the vicinity of neural correlates of middle-ear tympano-ossicular chain movements due to pressure variations. Disturbed proprioceptors are known to trigger illusory perceptions; therefore, we hypothesized that a disturbance of middle-ear proprioceptors may originate phantom sound perceptions. We designed an fMRI study that aimed to stimulate middle-ear proprioceptors by repetitive vibrations using various rates of click trains. In this study, we report that exposure to specific rates of stimuli for a few minutes at comfortable intensity level in healthy subjects distinctly triggered transient tinnitus-like aftereffects. The fMRI neural correlates of the aftereffects were unequivocally localized in the same parietal region as in acoustic trauma tinnitus sufferers. Our results strongly suggest that a middle-ear kinesthetic/proprioceptive illusion exists at the origin of acoustic trauma tinnitus via a somatosensory pathway encompassing the trigeminal system.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Ashburner J (2007) A fast diffeomorphic image registration algorithm. Neuroimage 38(1):95–113. doi:10.1016/j.neuroimage.2007.07.007

    Article  PubMed  Google Scholar 

  • Babalian AL (2005) Synaptic influences of pontine nuclei on cochlear nucleus cells. Exp Brain Res 167(3):451–457. doi:10.1007/s00221-005-0178-8

    Article  PubMed  Google Scholar 

  • Baguley D, McFerran D, Hall D (2013) Tinnitus. Lancet 382(9904):1600–1607. doi:10.1016/S0140-6736(13)60142-7

    Article  PubMed  Google Scholar 

  • Burke D, Hagbarth KE, Lofstedt L, Wallin BG (1976) The responses of human muscle spindle endings to vibration of non-contracting muscles. J Physiol 261(3):673–693

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Burton H, Sinclair RJ (2000) Tactile-spatial and cross-modal attention effects in the primary somatosensory cortical areas 3b and 1-2 of rhesus monkeys. Somatosens Mot Res 17(3):213–228

    Article  CAS  PubMed  Google Scholar 

  • Burton H, Fabri M, Alloway K (1995) Cortical areas within the lateral sulcus connected to cutaneous representations in areas 3b and 1: a revised interpretation of the second somatosensory area in macaque monkeys. J Comp Neurol 355(4):539–562. doi:10.1002/cne.903550405

    Article  CAS  PubMed  Google Scholar 

  • Coghill RC, Talbot JD, Evans AC, Meyer E, Gjedde A, Bushnell MC, Duncan GH (1994) Distributed processing of pain and vibration by the human brain. J Neurosci 14(7):4095–4108

    CAS  PubMed  Google Scholar 

  • Collins DF, Refshauge KM, Todd G, Gandevia SC (2005) Cutaneous receptors contribute to kinesthesia at the index finger, elbow, and knee. J Neurophysiol 94(3):1699–1706. doi:10.1152/jn.00191.2005

    Article  CAS  PubMed  Google Scholar 

  • Da Costa S, van der Zwaag W, Marques JP, Frackowiak RS, Clarke S, Saenz M (2011) Human primary auditory cortex follows the shape of Heschl’s gyrus. J Neurosci 31(40):14067–14075. doi:10.1523/JNEUROSCI.2000-11.2011

    Article  PubMed  Google Scholar 

  • Devlin JT, Raley J, Tunbridge E, Lanary K, Floyer-Lea A, Narain C, Cohen I, Behrens T, Jezzard P, Matthews PM, Moore DR (2003) Functional asymmetry for auditory processing in human primary auditory cortex. J Neurosci 23(37):11516–11522 pii: 23/37/11516

    CAS  PubMed  Google Scholar 

  • Disbrow E, Roberts T, Krubitzer L (2000) Somatotopic organization of cortical fields in the lateral sulcus of Homo sapiens: evidence for SII and PV. J Comp Neurol 418(1):1–21

    Article  CAS  PubMed  Google Scholar 

  • Eickhoff SB, Schleicher A, Zilles K, Amunts K (2006) The human parietal operculum. I. Cytoarchitectonic mapping of subdivisions. Cereb Cortex 16(2):254–267. doi:10.1093/cercor/bhi105

    Article  PubMed  Google Scholar 

  • Eickhoff SB, Grefkes C, Zilles K, Fink GR (2007) The somatotopic organization of cytoarchitectonic areas on the human parietal operculum. Cereb Cortex 17(8):1800–1811. doi:10.1093/cercor/bhl090

    Article  PubMed  Google Scholar 

  • Eklund G (1972) General features of vibration-induced effects on balance. Ups J Med Sci 77(2):112–124

    Article  CAS  PubMed  Google Scholar 

  • Goodwin GM, McCloskey DI, Matthews PB (1972) Proprioceptive illusions induced by muscle vibration: contribution by muscle spindles to perception? Science 175(4028):1382–1384

    Article  CAS  PubMed  Google Scholar 

  • Grassi C, Deriu F, Passatore M (1993) Effect of sympathetic nervous system activation on the tonic vibration reflex in rabbit jaw closing muscles. J Physiol 469:601–613

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hugdahl K (2000) Lateralization of cognitive processes in the brain. Acta Psychol (Amst) 105(2–3):211–235

    Article  CAS  Google Scholar 

  • Itoh K, Kamiya H, Mitani A, Yasui Y, Takada M, Mizuno N (1987) Direct projections from the dorsal column nuclei and the spinal trigeminal nuclei to the cochlear nuclei in the cat. Brain Res 400(1):145–150 pii: 0006-8993(87)90662-7

    Article  CAS  PubMed  Google Scholar 

  • Jain R, Shore S (2006) External inferior colliculus integrates trigeminal and acoustic information: unit responses to trigeminal nucleus and acoustic stimulation in the guinea pig. Neurosci Lett 395(1):71–75

    Article  CAS  PubMed  Google Scholar 

  • Job A, Paucod J-C, O’Beirne GA, Delon-Martin C (2011) Cortical representation of tympanic membrane movements due to pressure variation: a fMRI study. Hum Brain Mapp 32:744–749

    Article  PubMed  Google Scholar 

  • Job A, Pons Y, Lamalle L, Jaillard A, Buck K, Segebarth C, Delon-Martin C (2012) Abnormal cortical sensorimotor activity during “Target” sound detection in subjects with acute acoustic trauma sequelae: an fMRI study. Brain Behav 2(2):187–199. doi:10.1002/brb3.21

    Article  PubMed  PubMed Central  Google Scholar 

  • Kemp DT, Ryan S, Bray P (1990) A guide to the effective use of otoacoustic emissions. Ear Hear 11(2):93–105

    Article  CAS  PubMed  Google Scholar 

  • Kierner AC, Zelenka I, Lukas JR, Aigner M, Mayr R (1999) Observations on the number, distribution and morphological peculiarities of muscle spindles in the tensor tympani and stapedius muscle of man. Hear Res 135(1–2):71–77 pii: S0378-5955(99)00092-1

    Article  CAS  PubMed  Google Scholar 

  • Klein A, Andersson J, Ardekani BA, Ashburner J, Avants B, Chiang MC, Christensen GE, Collins DL, Gee J, Hellier P, Song JH, Jenkinson M, Lepage C, Rueckert D, Thompson P, Vercauteren T, Woods RP, Mann JJ, Parsey RV (2009) Evaluation of 14 nonlinear deformation algorithms applied to human brain MRI registration. Neuroimage 46(3):786–802. doi:10.1016/j.neuroimage.2008.12.037

    Article  PubMed  PubMed Central  Google Scholar 

  • Krubitzer L, Clarey J, Tweedale R, Elston G, Calford M (1995) A redefinition of somatosensory areas in the lateral sulcus of macaque monkeys. J Neurosci 15(5 Pt 2):3821–3839

    CAS  PubMed  Google Scholar 

  • Ledberg A, O’Sullivan BT, Kinomura S, Roland PE (1995) Somatosensory activations of the parietal operculum of man. A PET study. Eur J Neurosci 7(9):1934–1941

    Article  CAS  PubMed  Google Scholar 

  • Matsuo R, Ikehara A, Nokubi T, Morimoto T (1995) Inhibitory effect of sympathetic stimulation on activities of masseter muscle spindles and the jaw jerk reflex in rats. J Physiol 483(Pt 1):239–250

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Maudoux A, Lefebvre P, Cabay JE, Demertzi A, Vanhaudenhuyse A, Laureys S, Soddu A (2012) Auditory resting-state network connectivity in tinnitus: a functional MRI study. PLoS One 7(5):e36222. doi:10.1371/journal.pone.0036222

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mazzola L, Faillenot I, Barral FG, Mauguiere F, Peyron R (2012) Spatial segregation of somato-sensory and pain activations in the human operculo-insular cortex. Neuroimage 60(1):409–418. doi:10.1016/j.neuroimage.2011.12.072

    Article  PubMed  Google Scholar 

  • Naito E, Ehrsson HH, Geyer S, Zilles K, Roland PE (1999) Illusory arm movements activate cortical motor areas: a positron emission tomography study. J Neurosci 19(14):6134–6144

    CAS  PubMed  Google Scholar 

  • Passatore M, Deriu F, Grassi C, Roatta S (1996) A comparative study of changes operated by sympathetic nervous system activation on spindle afferent discharge and on tonic vibration reflex in rabbit jaw muscles. J Auton Nerv Syst 57(3):163–167 pii: 0165183895000747

    Article  CAS  PubMed  Google Scholar 

  • Pilati N, Ison MJ, Barker M, Mulheran M, Large CH, Forsythe ID, Matthias J, Hamann M (2012) Mechanisms contributing to central excitability changes during hearing loss. Proc Natl Acad Sci USA 109(21):8292–8297. doi:10.1073/pnas.1116981109

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Proske U, Gandevia SC (2009) The kinaesthetic senses. J Physiol 587(Pt 17):4139–4146. doi:10.1113/jphysiol.2009.175372

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Roatta S, Windhorst U, Ljubisavljevic M, Johansson H, Passatore M (2002) Sympathetic modulation of muscle spindle afferent sensitivity to stretch in rabbit jaw closing muscles. J Physiol 540(Pt 1):237–248 pii:PHY_14316

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Roll JP, Vedel JP (1982) Kinaesthetic role of muscle afferents in man, studied by tendon vibration and microneurography. Exp Brain Res 47(2):177–190

    Article  CAS  PubMed  Google Scholar 

  • Roll JP, Vedel JP, Ribot E (1989) Alteration of proprioceptive messages induced by tendon vibration in man: a microneurographic study. Exp Brain Res 76(1):213–222

    Article  CAS  PubMed  Google Scholar 

  • Rosenblith WA, Miller GA, Egan JP, Hirsh IJ, Thomas GJ (1947) An auditory afterimage? Science 106(2754):333–335. doi:10.1126/science.106.2754.333

    Article  CAS  PubMed  Google Scholar 

  • Shore SE, Vass Z, Wys NL, Altschuler RA (2000) Trigeminal ganglion innervates the auditory brainstem. J Comp Neurol 419(3):271–285

    Article  CAS  PubMed  Google Scholar 

  • Taylor A, Ellaway PH, Durbaba R (1999) Why are there three types of intrafusal muscle fibers? Prog Brain Res 123:121–131

    Article  CAS  PubMed  Google Scholar 

  • Vanneste S, De Ridder D (2013) Brain areas controlling heart rate variability in tinnitus and tinnitus-related distress. PLoS One 8(3):e59728. doi:10.1371/journal.pone.0059728

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vass Z, Shore SE, Nuttall AL, Miller JM (1998) Direct evidence of trigeminal innervation of the cochlear blood vessels. Neuroscience 84(2):559–567 pii: S0306-4522(97)00503-4

    Article  CAS  PubMed  Google Scholar 

  • Weerakkody NS, Mahns DA, Taylor JL, Gandevia SC (2007) Impairment of human proprioception by high-frequency cutaneous vibration. J Physiol 581(Pt 3):971–980. doi:10.1113/jphysiol.2006.126854

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Westcott M, Sanchez TG, Diges I, Saba C, Dineen R, McNeill C, Chiam A, O’Keefe M, Sharples T (2013) Tonic tensor tympani syndrome in tinnitus and hyperacusis patients: a multi-clinic prevalence study. Noise Health 15(63):117–128. doi:10.4103/1463-1741.110295

    Article  PubMed  Google Scholar 

  • Zhou J, Shore S (2004) Projections from the trigeminal nuclear complex to the cochlear nuclei: a retrograde and anterograde tracing study in the guinea pig. J Neurosci Res 78(6):901–907. doi:10.1002/jnr.20343

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We are grateful to Alain Roux and Hervé Mathieu for their technical assistance and the NATO group HFM-229 for their precious advises. This work was supported by Grants from Délégation Générale de l’Armement (DGA) under number 11 CA 801 (to A. J.). We thank the Grenoble MRI facility, partially funded by the French national program “Investissement d’Avenir” run by the ‘Agence Nationale pour la Recherche’ Grant No- ANR-11-INBS-0006.

Conflict of interest

The authors declare no competing financial interest.

Author information

Authors and Affiliations

  1. IRBA, Institut de Recherche Biomédicale des Armées, Bretigny Sur Orge, France

    Agnès Job

  2. INSERM, U836, Grenoble, France

    Agnès Job & Chantal Delon-Martin

  3. Univ. Grenoble Alpes, GIN-eq5, Grenoble, France

    Agnès Job & Chantal Delon-Martin

  4. Bundeswherzentralkrankenhaus, Abt V HNO, Koblenz, Germany

    Roland Jacob

  5. Service ORL, Hopital d’Instruction des Armées, HIA Percy, Clamart, France

    Yoann Pons, Marc Raynal & Michel Kossowski

  6. Service ORL, Hopital d’Instruction des Armées, HIA Desgenettes, Lyon, France

    Jérôme Gauthier & Bertrand Lombard

Authors
  1. Agnès Job
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Roland Jacob
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yoann Pons
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Marc Raynal
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Michel Kossowski
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Jérôme Gauthier
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Bertrand Lombard
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Chantal Delon-Martin
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Agnès Job.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Job, A., Jacob, R., Pons, Y. et al. Specific activation of operculum 3 (OP3) brain region during provoked tinnitus-related phantom auditory perceptions in humans. Brain Struct Funct 221, 913–922 (2016). https://doi.org/10.1007/s00429-014-0944-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00429-014-0944-0

Keywords

Search

Navigation