Skip to main content

Advertisement

SpringerLink
Log in

The involvement of the left ventrolateral prefrontal cortex in tinnitus: a TMS study

  • Research Article
  • Published:
Experimental Brain Research Aims and scope Submit manuscript

Abstract

Tinnitus is an auditory phantom percept with a tone, hissing or buzzing sound in the absence of any objective physical sound source. Tinnitus is considered to be an auditory phantom phenomenon analogous to somatosensory phantom pain. Controllable versus uncontrollable pain is characterized by an increased activity in the ventrolateral prefrontal cortex (VLPFC), and activation in the VLPFC correlating with perceived control over pain results in a decrease in subjective pain intensity. Depressed individuals show less activation than healthy controls in the left VLPFC in response to sad autobiographical scripts, and greater relative left prefrontal activation is related to a greater disposition to approach-related, positive affect with a greater ability to regulate negative affect. Based on the theory that non-pulsatile tinnitus can be considered the auditory analogue for deafferentation pain, we hypothesize that the left VLPFC might also be involved in control of tinnitus. We conducted a transcranial magnetic stimulation (TMS) study verifying whether modulating the left VLPFC by TMS can modulate the loudness of tinnitus. We studied 60 patients with chronic tinnitus of which 21 patients received in random order sham and 1-Hz stimulation, while 39 patients received in random order sham and 10-Hz stimulation. Our results show that 10-Hz stimulation can modulate tinnitus loudness, while 1-Hz stimulation does not seem to exert the same effect. Our findings give further support to the fact that non-auditory areas are involved in tinnitus.

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

Similar content being viewed by others

References

  • Chen R (2000) Studies of human motor physiology with transcranial magnetic stimulation. Muscle Nerve Suppl 9:S26–S32

    Article  PubMed  CAS  Google Scholar 

  • Cohen LG, Roth BJ, Nilsson J et al (1990) Effects of coil design on delivery of focal magnetic stimulation. Technical considerations. Electroencephalogr Clin Neurophysiol 75:350–357

    Article  CAS  Google Scholar 

  • Davidson D (1995) Cerebral asymmetry, emotion and affective style. MIT, Cambridge

    Google Scholar 

  • De Ridder D, Verstraeten E, Van der Kelen K et al (2005) Transcranial magnetic stimulation for tinnitus : influence of tinnitus duration on stimulation parameter choice and maximal tinnitus suppression. Otol Neurotol 26:616–619

    Article  PubMed  Google Scholar 

  • De Ridder D, De Mulder G, Menovsky T, Sunaert S, Kovacs S (2007a) Electrical stimulation of auditory and somatosensory cortices for treatment of tinnitus and pain. Prog Brain Res 166:377–388

    Article  PubMed  Google Scholar 

  • De Ridder D, van der Loo E, Van der Kelen K, Menovsky T, van de Heyning P, Moller A (2007b) Do tonic and burst TMS modulate the lemniscal and extralemniscal system differentially? Int J Med Sci 4:242–246

    Article  PubMed  Google Scholar 

  • De Ridder D, van der Loo E, Van der Kelen K, Menovsky T, van de Heyning P, Moller A (2007c) Theta, alpha and beta burst transcranial magnetic stimulation: brain modulation in tinnitus. Int J Med Sci 4:237–241

    Article  PubMed  Google Scholar 

  • De Ridder D, Elgoyhen AB, Romo R, Langguth B (2011) Phantom percepts: tinnitus and pain as persisting aversive memory networks. Proc Natl Acad Sci USA. doi:10.1073/pnas.1018466108

    Google Scholar 

  • Hallett M (2000) Transcranial magnetic stimulation and the human brain. Nature 406:147–150. doi:10.1038/35018000

    Article  PubMed  CAS  Google Scholar 

  • Jastreboff PJ (1990) Phantom auditory perception (tinnitus): mechanisms of generation and perception. Neurosci Res 8:221–254

    Article  PubMed  CAS  Google Scholar 

  • Keedwell PA, Andrew C, Williams SC, Brammer MJ, Phillips ML (2005) A double dissociation of ventromedial prefrontal cortical responses to sad and happy stimuli in depressed and healthy individuals. Biol Psychiatry 58:495–503. doi:10.1016/j.biopsych.2005.04.035

    Article  PubMed  Google Scholar 

  • Khedr EM, Rothwell JC, Ahmed MA, El-Atar A (2008) Effect of daily repetitive transcranial magnetic stimulation for treatment of tinnitus: comparison of different stimulus frequencies. J Neurol Neurosurg Psychiatry 79:212–215. doi:10.1136/jnnp.2007.127712

    Article  PubMed  CAS  Google Scholar 

  • Khedr EM, Rothwell JC, El-Atar A (2009) One-year follow up of patients with chronic tinnitus treated with left temporoparietal rTMS. Eur J Neurol 16:404–408. doi:10.1111/j.1468-1331.2008.02522.x

    Article  PubMed  CAS  Google Scholar 

  • Kimbrell TA, Little JT, Dunn RT et al (1999) Frequency dependence of antidepressant response to left prefrontal repetitive transcranial magnetic stimulation (rTMS) as a function of baseline cerebral glucose metabolism. Biol Psychiatry 46:1603–1613

    Article  PubMed  CAS  Google Scholar 

  • Kimbrell TA, Dunn RT, George MS et al (2002) Left prefrontal-repetitive transcranial magnetic stimulation (rTMS) and regional cerebral glucose metabolism in normal volunteers. Psychiatry Res 115:101–113

    Article  PubMed  CAS  Google Scholar 

  • Kleinjung T, Eichhammer P, Langguth B et al (2005) Long-term effects of repetitive transcranial magnetic stimulation (rTMS) in patients with chronic tinnitus. Otolaryngol Head Neck Surg 132:566–569. doi:10.1016/j.otohns.2004.09.134

    Article  PubMed  Google Scholar 

  • Kleinjung T, Eichhammer P, Landgrebe M et al (2008) Combined temporal and prefrontal transcranial magnetic stimulation for tinnitus treatment: a pilot study. Otolaryngol Head Neck Surg 138:497–501. doi:10.1016/j.otohns.2007.12.022

    Article  PubMed  Google Scholar 

  • Landgrebe M, Langguth B, Rosengarth K et al (2009) Structural brain changes in tinnitus: grey matter decrease in auditory and non-auditory brain areas. Neuroimage 46:213–218. doi:10.1016/j.neuroimage.2009.01.069

    Article  PubMed  Google Scholar 

  • Langguth B, Zowe M, Landgrebe M et al (2006) Transcranial magnetic stimulation for the treatment of tinnitus: a new coil positioning method and first results. Brain Topogr 18:241–247. doi:10.1007/s10548-006-0002-1

    Article  PubMed  Google Scholar 

  • Langguth B, de Ridder D, Dornhoffer JL et al (2008) Controversy: does repetitive transcranial magnetic stimulation/transcranial direct current stimulation show efficacy in treating tinnitus patients? Brain Stimul 1:192–205. doi:10.1016/j.brs.2008.06.003

    Article  PubMed  Google Scholar 

  • Langguth B, Kleinjung T, Landgrebe M, de Ridder D, Hajak G (2010) rTMS for the treatment of tinnitus: the role of neuronavigation for coil positioning. Neurophysiol Clin 40:45–58. doi:10.1016/j.neucli.2009.03.001

    Article  PubMed  CAS  Google Scholar 

  • Lanting CP, de Kleine E, van Dijk P (2009) Neural activity underlying tinnitus generation: results from PET and fMRI. Hear Res 255:1–13. doi:10.1016/j.heares.2009.06.009

    Article  PubMed  CAS  Google Scholar 

  • Llinas RR, Ribary U, Jeanmonod D, Kronberg E, Mitra PP (1999) Thalamocortical dysrhythmia: a neurological and neuropsychiatric syndrome characterized by magnetoencephalography. Proc Natl Acad Sci USA 96:15222–15227

    Article  PubMed  CAS  Google Scholar 

  • Lockwood AH, Salvi RJ, Burkard RF, Galantowicz PJ, Coad ML, Wack DS (1999) Neuroanatomy of tinnitus. Scand Audiol Suppl 51:47–52

    PubMed  CAS  Google Scholar 

  • Moller AR (2000) Similarities between severe tinnitus and chronic pain. J Am Acad Audiol 11:115–124

    PubMed  CAS  Google Scholar 

  • Muhlnickel W, Elbert T, Taub E, Flor H (1998) Reorganization of auditory cortex in tinnitus. Proc Natl Acad Sci USA 95:10340–10343

    Article  PubMed  CAS  Google Scholar 

  • Nahas Z, Lomarev M, Roberts DR et al (2001) Unilateral left prefrontal transcranial magnetic stimulation (TMS) produces intensity-dependent bilateral effects as measured by interleaved BOLD fMRI. Biol Psychiatry 50:712–720

    Article  PubMed  CAS  Google Scholar 

  • Ochsner KN, Gross JJ (2005) The cognitive control of emotion. Trends Cogn Sci 9:242–249. doi:10.1016/j.tics.2005.03.010

    Article  PubMed  Google Scholar 

  • Rauschecker JP, Leaver AM, Muhlau M (2010) Tuning Out the Noise: limbic-Auditory Interactions in Tinnitus. Neuron 66:819–826

    Article  PubMed  CAS  Google Scholar 

  • Romanski LM, Goldman-Rakic PS (2002) An auditory domain in primate prefrontal cortex. Nat Neurosci 5:15–16. doi:10.1038/nn781

    Article  PubMed  CAS  Google Scholar 

  • Salomons TV, Johnstone T, Backonja MM, Shackman AJ, Davidson RJ (2007) Individual differences in the effects of perceived controllability on pain perception: critical role of the prefrontal cortex. J Cogn Neurosci 19:993–1003. doi:10.1162/jocn.2007.19.6.993

    Article  PubMed  Google Scholar 

  • Speer AM, Kimbrell TA, Wassermann EM, Repell JD, Willis MW, Herscovitch P, Post RM (2000) Opposite effects of high and low frequency rTMS on regional brain activity in depressed patients. Biol Psychiatry 48:1133–1141

    Article  PubMed  CAS  Google Scholar 

  • Speer AM, Willis MW, Herscovitch P et al (2003) Intensity-dependent regional cerebral blood flow during 1-Hz repetitive transcranial magnetic stimulation (rTMS) in healthy volunteers studied with H215O positron emission tomography: II. Effects of prefrontal cortex rTMS. Biol Psychiatry 54:826–832

    Article  PubMed  Google Scholar 

  • Tomarken AJ, Davidson RJ, Wheeler RE, Doss RC (1992) Individual differences in anterior brain asymmetry and fundamental dimensions of emotion. J Pers Soc Psychol 62:676–687

    Article  PubMed  CAS  Google Scholar 

  • Tonndorf J (1987) The analogy between tinnitus and pain: a suggestion for a physiological basis of chronic tinnitus. Hear Res 28:271–275

    Article  PubMed  CAS  Google Scholar 

  • van der Loo E, Gais S, Congedo M et al (2009) Tinnitus intensity dependent gamma oscillations of the contralateral auditory cortex. PLoS One 4:e7396 (7391–7395). doi:10.1371/journal.pone.0007396

    Article  PubMed  Google Scholar 

  • Vanneste S, Plazier M, Ost J, van der Loo E, Van de Heyning P, De Ridder D (2010a) Bilateral dorsolateral prefrontal cortex modulation for tinnitus by transcranial direct current stimulation: a preliminary clinical study. Exp Brain Res 202:779–785. doi:10.1007/s00221-010-2183-9

    Article  PubMed  Google Scholar 

  • Vanneste S, Plazier M, van der Loo E, Van de Heyning P, De Ridder D (2010b) The difference between uni-and bilateral auditory phantom percept. Clin Neurophysiol. doi:10.1016/j.clinph.2010.07.022

    PubMed  Google Scholar 

  • Wager TD, Davidson ML, Hughes BL, Lindquist MA, Ochsner KN (2008) Prefrontal-subcortical pathways mediating successful emotion regulation. Neuron 59:1037–1050. doi:10.1016/j.neuron.2008.09.006

    Article  PubMed  CAS  Google Scholar 

  • Weisz N, Muller S, Schlee W, Dohrmann K, Hartmann T, Elbert T (2007) The neural code of auditory phantom perception. J Neurosci 27:1479–1484

    Article  PubMed  CAS  Google Scholar 

  • Wiech K, Kalisch R, Weiskopf N, Pleger B, Stephan KE, Dolan RJ (2006) Anterolateral prefrontal cortex mediates the analgesic effect of expected and perceived control over pain. J Neurosci 26:11501–11509. doi:10.1523/JNEUROSCI.2568-06.2006

    Article  PubMed  CAS  Google Scholar 

  • Wiech K, Ploner M, Tracey I (2008) Neurocognitive aspects of pain perception. Trends Cogn Sci 12:306–313. doi:10.1016/j.tics.2008.05.005

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

The authors thank Jan Ost, Bram Van Achteren, Bjorn Devree and Pieter van Looy for their help in preparing this manuscript.

Author information

Authors and Affiliations

  1. Brai²n, Tinnitus Research Initiative Clinic Antwerp, Department of Neurosurgery, University Hospital Antwerp, Wilrijkstraat 10, 2650, Edegem, Belgium

    Sven Vanneste & Dirk De Ridder

Authors
  1. Sven Vanneste
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Dirk De Ridder
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Sven Vanneste.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Vanneste, S., De Ridder, D. The involvement of the left ventrolateral prefrontal cortex in tinnitus: a TMS study. Exp Brain Res 221, 345–350 (2012). https://doi.org/10.1007/s00221-012-3177-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00221-012-3177-6

Keywords

Search

Navigation