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Effect of 1 Hz Repetitive Transcranial Magnetic Stimulation Over the Auditory Cortex on Audiometry and Otoacustic Emissions

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Abstract

Repetitive transcranial magnetic stimulation (rTMS) at low frequencies (≤1 Hz) delivered to the primary motor cortex for 15 min or longer has been shown to reduce motor cortex excitability. Over the visual cortex, 1 Hz rTMS led to increased phosphene thresholds and over the auditory cortex rTMS reduced auditory evoked potentials. rTMS above the auditory or temporo-parietal cortex has also been reported to reduce the severity of auditory hallucinations and the perception of tinnitus. However, possible unwanted effects on hearing function have not yet been investigated systematically. 12 right-handed normal hearing subjects (5 male, mean age 28.2 ± 4.3) received a single session of 18 min 1 Hz rTMS at 90% resting motor threshold intensity using an established coil positioning method targeting the Heschl’s area of the left superior temporal gyrus. Standard pure tone audiometry and distortion-products otoacustic emissions (DPOAE) were performed before and immediately after stimulation. The main finding was that one session of 1 Hz rTMS over the temporal cortex modified neither the auditory threshold meaningfully nor the presence of DPOAE in healthy subjects. In conclusion, we found in this pilot approach no obvious indication for auditory dysfunctions due to direct electromagnetic stimulation of the superior temporal gyrus after one session of rTMS in healthy controls that may be interpreted as unwanted side effects. Nevertheless monitoring of auditory functions is strongly recommended in future clinical trials stimulating the auditory cortex, as this has not been done systematically in the past.

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References

  • Aleman A, Sommer IE, Kahn RS (2007) Efficacy of slow repetitive transcranial magnetic stimulation in the treatment of resistant auditory hallucinations in schizophrenia: a meta-analysis. J Clin Psychiatry 68:416–421

    Article  PubMed  Google Scholar 

  • Al-Noury K (2011) Distortion product otoacoustic emission for the screening of cochlear damage in children treated with cisplatin. Laryngoscope 121(5):1081–1084

    Article  PubMed  Google Scholar 

  • Boroojerdi B, Prager A, Muellbacher W, Cohen LG (2000) Reduction of human visual cortex excitability using 1-Hz transcranial magnetic stimulation. Neurology 54:1529–1531

    Article  PubMed  CAS  Google Scholar 

  • Brunelin J, Poulet E, Bediou B, Kallel L, Dalery J, D’Amato T, Saoud M (2006) Low frequency repetitive transcranial magnetic stimulation improves source monitoring deficit in hallucinating patients with schizophrenia. Schizophr Res 81:41–45

    Article  PubMed  Google Scholar 

  • Burger J, Frank E, Kreuzer P, Kleinjung T, Vielsmeier V, Landgrebe M, Hajak G, Langguth B (2011) Transcranial magnetic stimulation for the treatment of tinnitus: 4-year follow-up in treatment responders-a retrospective analysis. Brain Stimul 4:222–227

    Article  PubMed  Google Scholar 

  • Cardenas-Morales L, Nowak DA, Kammer T, Wolf RC, Schönfeldt-Lecuona C (2010) Mechanisms and applications of theta-burst rTMS on the human motor cortex. Brain Topogr 22:294–306

    Article  PubMed  Google Scholar 

  • Chen R, Classen J, Gerloff C, Celnik P, Wassermann EM, Hallett M, Cohen LG (1997) Depression of motor cortex excitability by low-frequency transcranial magnetic stimulation. Neurology 48:1398–1403

    Article  PubMed  CAS  Google Scholar 

  • Counter SA, Borg E (1992) Analysis of the coil generated impulse noise in extracranial magnetic stimulation. Electroencephalogr Clin Neurophysiol 85:280–288

    Article  PubMed  CAS  Google Scholar 

  • De Ridder D, Verstraeten E, Van der Kelen K, De Mulder G, Sunaert S, Verlooy J, Van de Heyning P, Moller A (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 

  • Dierks T, Linden DE, Jandl M, Formisano E, Goebel R, Lanfermann H, Singer W (1999) Activation of Heschl’s gyrus during auditory hallucinations. Neuron 22:615–621

    Article  PubMed  CAS  Google Scholar 

  • Eichhammer P, Kleinjung T, Landgrebe M, Hajak G, Langguth B (2007) TMS for treatment of chronic tinnitus: neurobiological effects. Prog Brain Res 166:369–375

    Article  PubMed  CAS  Google Scholar 

  • Fierro B, Giglia G, Palermo A, Pecoraro C, Scalia S, Brighina F (2007) Modulatory effects of 1 Hz rTMS over the cerebellum on motor cortex excitability. Exp Brain Res 176:440–447

    Article  PubMed  Google Scholar 

  • Fitzgerald PB, Brown TL, Daskalakis ZJ, Chen R, Kulkarni J (2002) Intensity-dependent effects of 1 Hz rTMS on human corticospinal excitability. Clin Neurophysiol 113:1136–1141

    Article  PubMed  Google Scholar 

  • Fitzgerald PB, Benitez J, Daskalakis JZ, Brown TL, Marston NA, de Castella A, Kulkarni J (2005) A double-blind sham-controlled trial of repetitive transcranial magnetic stimulation in the treatment of refractory auditory hallucinations. J Clin Psychopharmacol 25:358–362

    Article  PubMed  Google Scholar 

  • Gorga MP, Neely ST, Bergman BM, Beauchaine KL, Kaminski JR, Peters J, Schulte L, Jesteadt W (1993) A comparison of transient-evoked and distortion product otoacoustic emissions in normal-hearing and hearing-impaired subjects. J Acoust Soc Am 94(5):2639–2648

    Article  PubMed  CAS  Google Scholar 

  • Gorga MP, Neely ST, Ohlrich B, Hoover B, Redner J, Peters J (1997) From laboratory to clinic: a large scale study of distortion product otoacoustic emissions in ears with normal hearing and ears with hearing loss. Ear Hear 18:440–455

    Article  PubMed  CAS  Google Scholar 

  • Herwig U, Bräuer K, Connemann B, Spitzer M, Schönfeldt-Lecuona C (2002) Intracortical excitability is modulated by a norepinephrine-reuptake inhibitor as measured with paired-pulse transcranial magnetic stimulation. Psychopharmacology 164(2):228–232

    Article  PubMed  CAS  Google Scholar 

  • Herwig U, Satrapi P, Schönfeldt-Lecuona C (2003) Using the international 10–20 EEG system for positioning of transcranial magnetic stimulation. Brain Topogr 16:95–99

    Article  PubMed  Google Scholar 

  • Hoffman RE, Cavus I (2002) Slow transcranial magnetic stimulation, long-term depotentiation, and brain hyperexcitability disorders. Am J Psychiatry 159:1093–1102

    Article  PubMed  Google Scholar 

  • Hoffman RE, Boutros NN, Berman RM, Roessler E, Belger A, Krystal JH, Charney DS (1999a) Transcranial magnetic stimulation of left temporoparietal cortex in three patients reporting hallucinated “voices”. Biol Psychiatry 46:130–132

    Article  PubMed  CAS  Google Scholar 

  • Hoffman RE, Rapaport J, Mazure CM, Quinlan DM (1999b) Selective speech perception alterations in schizophrenic patients reporting hallucinated “voices”. Am J Psychiatry 156:393–399

    PubMed  CAS  Google Scholar 

  • Hoffman RE, Boutros NN, Hu S, Berman RM, Krystal JH, Charney DS (2000) Transcranial magnetic stimulation and auditory hallucinations in schizophrenia. Lancet 355:1073–1075

    Article  PubMed  CAS  Google Scholar 

  • Hoffman RE, Gueorguieva R, Hawkins KA, Varanko M, Boutros NN, Wu YT, Carroll K, Krystal JH (2005) Temporoparietal transcranial magnetic stimulation for auditory hallucinations: safety, efficacy and moderators in a fifty patient sample. Biol Psychiatry 58:97–104

    Article  PubMed  Google Scholar 

  • Jasper HH (1958) The ten-twenty system of the International Federation. Electroencephalogr Clin Neurophysiol 10:371–375

    Google Scholar 

  • Kaffenberger T, Baumgartner T, Köneke S, Jäncke L, Herwig U (2008) Chronometric features of processing unpleasant stimuli—an fMRI-based TMS study. Neuroreport 19(7):777–781

    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

    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

    Article  PubMed  CAS  Google Scholar 

  • Khedr EM, Abo-Elfetoh N, Rothwell JC, El-Atar A, Sayed E, Khalifa H (2010) Contralateral versus ipsilateral rTMS of temporoparietal cortex for the treatment of chronic unilateral tinnitus: comparative study. Eur J Neurol 17:976–983

    Article  PubMed  CAS  Google Scholar 

  • Kleinjung T, Eichhammer P, Langguth B, Jacob P, Marienhagen J, Hajak G, Wolf SR, Strutz J (2005) Long-term effects of repetitive transcranial magnetic stimulation (rTMS) in patients with chronic tinnitus. Otolaryngol Head Neck Surg 132:566–569

    Article  PubMed  Google Scholar 

  • Langguth B, Zowe M, Landgrebe M, Sand P, Kleinjung T, Binder H, Hajak G, Eichhammer P (2006) Transcranial magnetic stimulation for the treatment of tinnitus: a new coil positioning method and first results. Brain Topogr 18:241–247

    Article  PubMed  Google Scholar 

  • Langguth B, Kleinjung T, Marienhagen J, Binder H, Sand PG, Hajak G, Eichhammer P (2007) Transcranial magnetic stimulation for the treatment of tinnitus: effects on cortical excitability. BMC Neurosci 8:45

    Article  PubMed  Google Scholar 

  • Langguth B, Kleinjung T, Frank E, Landgrebe M, Sand P, Dvorakova J, Frick U, Eichhammer P, Hajak G (2008) High-frequency priming stimulation does not enhance the effect of low-frequency rTMS in the treatment of tinnitus. Exp Brain Res 184:587–591

    Article  PubMed  Google Scholar 

  • Lockwood AH, Salvi RJ, Coad ML, Towsley ML, Wack DS, Murphy BW (1998) The functional neuroanatomy of tinnitus: evidence for limbic system links and neural plasticity. Neurology 50(1):114–120

    Article  PubMed  CAS  Google Scholar 

  • Lorenz I, Müller N, Schlee W, Langguth B, Weisz N (2010) Short-term effects of single repetitive TMS sessions on auditory evoked activity in patients with chronic tinnitus. J Neurophysiol 104:1497–1505

    Article  PubMed  Google Scholar 

  • May A, Hajak G, Gänssbauer S, Steffens T, Langguth B, Kleinjung T, Eichhammer P (2007) Structural brain alterations following 5 days of intervention: dynamic aspects of neuroplasticity. Cereb Cortex 17:205–210

    Article  PubMed  CAS  Google Scholar 

  • McGuire PK, Silbersweig DA, Wright I, Murray RM, David AS, Frackowiak RS, Frith CD (1995) Abnormal monitoring of inner speech: a physiological basis for auditory hallucinations. Lancet 346:596–600

    Article  PubMed  CAS  Google Scholar 

  • Muellbacher W, Ziemann U, Boroojerdi B, Hallett M (2000) Effects of low-frequency transcranial magnetic stimulation on motor excitability and basic motor behavior. Clin Neurophysiol 111:1002–1007

    Article  PubMed  CAS  Google Scholar 

  • Pascual-Leone A, Cohen LG, Shotland LI, Dang N, Pikus A, Wassermann EM, Brasil-Neto JP, Valls-Sole J, Hallett M (1992) No evidence of hearing loss in humans due to transcranial magnetic stimulation. Neurology 42:647–651

    Article  PubMed  CAS  Google Scholar 

  • Pascual-Leone A, Houser CM, Reese K, Shotland LI, Grafman J, Sato S, Valls-Sole J, Brasil-Neto JP, Wassermann EM, Cohen LG et al (1993) Safety of rapid-rate transcranial magnetic stimulation in normal volunteers. Electroencephalogr Clin Neurophysiol 89:120–130

    Article  PubMed  CAS  Google Scholar 

  • Plewnia C, Reimold M, Najib A, Reischl G, Plontke SK, Gerloff C (2007) Moderate therapeutic efficacy of positron emission tomography-navigated repetitive transcranial magnetic stimulation for chronic tinnitus: a randomised, controlled pilot study. J Neurol Neurosurg Psychiatry 78:152–156

    Article  PubMed  CAS  Google Scholar 

  • Prasher D, Sulkowski W (1999) The role of otoacoustic emissions in screening and evaluation of noise damage. Int J Occup Med Environ Health 12:183–192

    PubMed  CAS  Google Scholar 

  • Probst R, Harris FP (1993) Transiently evoked and distortion-product otoacoustic emissions. Comparison of results from normally hearing and hearing-impaired human ears. Arch Otolaryngol Head Neck Surg 119(8):858–860

    Article  PubMed  CAS  Google Scholar 

  • Rosa MO, Gattaz WF, Rosa MA, Rumi DO, Tavares H, Myczkowski M, Sartorelli MC, Rigonatti SP, Elkis H, Cabral SB, Teixeira MJ, Marcolin MA (2007) Effects of repetitive transcranial magnetic stimulation on auditory hallucinations refractory to clozapine. J Clin Psychiatry 68:1528–1532

    Article  PubMed  CAS  Google Scholar 

  • Rossi S, Hallett M, Rossini PM, Pascual-Leone A (2009) Safety, ethical considerations, and application guidelines for the use of transcranial magnetic stimulation in clinical practice and research. Clin Neurophysiol 120:2008–2039

    Article  PubMed  Google Scholar 

  • Rossini PM, Barker AT, Berardelli A, Caramia MD, Caruso G, Cracco RQ, Dimitrijevic MR, Hallett M, Katayama Y, Lucking CH et al (1994) Non-invasive electrical and magnetic stimulation of the brain, spinal cord and roots: basic principles and procedures for routine clinical application. Report of an IFCN committee. Electroencephalogr Clin Neurophysiol 91:79–92

    Article  PubMed  CAS  Google Scholar 

  • Schönfeldt-Lecuona C, Gron G, Walter H, Buchler N, Wunderlich A, Spitzer M, Herwig U (2004) Stereotaxic rTMS for the treatment of auditory hallucinations in schizophrenia. Neuroreport 15:1669–1673

    Article  PubMed  Google Scholar 

  • Seixas N, Kujawa SG, Norton S, Sheppard L, Neitzel R, Slee A (2004) Predictors of hearing threshold levels and distortion product otoacoustic emissions among noise exposed young adults. Occup Environ Med 61:899–907

    Article  PubMed  CAS  Google Scholar 

  • Siebner HR, Lang N, Rizzo V, Nitsche MA, Paulus W, Lemon RN, Rothwell JC (2004) Preconditioning of low-frequency repetitive transcranial magnetic stimulation with transcranial direct current stimulation: evidence for homeostatic plasticity in the human motor cortex. J Neurosci 24:3379–3385

    Article  PubMed  CAS  Google Scholar 

  • Slotema CW, Blom JD, Hoek HW, Sommer IE (2010) Should we expand the toolbox of psychiatric treatment methods to include Repetitive Transcranial Magnetic Stimulation (rTMS)? A meta-analysis of the efficacy of rTMS in psychiatric disorders. J Clin Psychiatry 71:873–884

    Article  PubMed  Google Scholar 

  • Slotema CW, Blom JD, de Weijer AD, Diederen KM, Goekoop R, Looijestijn J, Daalman K, Rijkaart A-M, Kahn RS, Hoek HW, Sommer IEC (2011) Can low-frequency repetitive transcranial magnetic stimulation really relieve medication-resistant auditory verbal hallucinations? Negative results from a large randomized controlled trial. Biol Psychiatry 69:450–456

    Article  PubMed  Google Scholar 

  • Smoorenburg GF (1993) Risk of noise-induced hearing loss following exposure to Chinese firecrackers. Int J Audiol 32:333–343

    Article  CAS  Google Scholar 

  • Tringali S, Perrot X, Collet L, Moulin A (2011) Repetitive transcranial magnetic stimulation: hearing safety considerations. Brain Stimul. doi:10.1016/j.brs.2011.06.005

  • Wassermann EM (1998) Risk and safety of repetitive transcranial magnetic stimulation: report and suggested guidelines from the International Workshop on the Safety of Repetitive Transcranial Magnetic Stimulation, June 5–7, 1996. Electroencephalogr Clin Neurophysiol 108:1–16

    Article  PubMed  CAS  Google Scholar 

  • Weiss SR, Li XL, Rosen JB, Li H, Heynen T, Post RM (1995) Quenching: inhibition of development and expression of amygdala kindled seizures with low frequency stimulation. Neuroreport 6:2171–2176

    Article  PubMed  CAS  Google Scholar 

  • Zahnert T (2010) Hearing impairment—aetiology, diagnostik and auditive rehabilitation. Laryngorhinootologie 89:669–691; quiz 692–663

    Google Scholar 

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Authors and Affiliations

  1. Department of Psychiatry and Psychotherapy III, University of Ulm, Leimgrubenweg 12–14, 89075, Ulm, Germany

    C. Schönfeldt-Lecuona, L. Cárdenas-Morales, T. Kammer & U. Herwig

  2. Department of Human Communication, University of Morelos, Cuernavaca, Mexico

    A. Moreno-Aguirre

  3. Practice for Otolaryngology, Leonberg, Germany

    K. Dorn

  4. Department of Psychiatry and Psychotherapy, University of Regensburg, Regensburg, Germany

    B. Langguth

  5. Psychiatric University Hospital, University of Zürich, Zürich, Switzerland

    A. B. Brühl & U. Herwig

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  1. C. Schönfeldt-Lecuona
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  2. L. Cárdenas-Morales
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  3. A. Moreno-Aguirre
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  4. K. Dorn
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Correspondence to C. Schönfeldt-Lecuona.

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Schönfeldt-Lecuona, C., Cárdenas-Morales, L., Moreno-Aguirre, A. et al. Effect of 1 Hz Repetitive Transcranial Magnetic Stimulation Over the Auditory Cortex on Audiometry and Otoacustic Emissions. Brain Topogr 25, 241–247 (2012). https://doi.org/10.1007/s10548-012-0218-1

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  • DOI: https://doi.org/10.1007/s10548-012-0218-1

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