Head-to-Head Comparison of Transcranial Random Noise Stimulation, Transcranial AC Stimulation, and Transcranial DC Stimulation for Tinnitus

Sven Vanneste, Felipe Fregni, Dirk De Ridder, Sven Vanneste, Felipe Fregni, Dirk De Ridder

Abstract

Tinnitus is the perception of a sound in the absence of an external sound stimulus. This phantom sound has been related to plastic changes and hyperactivity in the auditory cortex. Different neuromodulation techniques such as transcranial magnetic stimulation and transcranial direct current stimulation (tDCS) have been used in an attempt to modify local and distant neuroplasticity as to reduce tinnitus symptoms. Recently, two techniques of pulsed electrical stimulation using weak electrical currents - transcranial alternating current stimulation (tACS) and transcranial random noise stimulation (tRNS) - have also shown significant neuromodulatory effects. In the present study we conducted the first head-to-head comparison of three different transcranial electrical stimulation (tES) techniques, namely tDCS, tACS, and tRNS in 111 tinnitus patients by placing the electrodes overlying the auditory cortex bilaterally. The results demonstrated that tRNS induced the larger transient suppressive effect on the tinnitus loudness and the tinnitus related distress as compared to tDCS and tACS. Both tDCS and tACS induced small and non-significant effects on tinnitus symptoms, supporting the superior effects of tRNS as a method for tinnitus suppression.

Keywords: distress; loudness; tACS; tDCS; tRNS; tinnitus.

Figures

Figure 1
Figure 1
Pre- and post-stimulation numeric rating scales for tinnitus loudness (A) and tinnitus distress (B) for bilateral auditory cortex tDCS, tACS, and tRNS. Only tRNS exerts a suppressive effect both tinnitus loudness and tinnitus distress. (***p < 0.001).
Figure 2
Figure 2
Amount of tinnitus suppression (pre – post-stimulation) for tinnitus loudness and tinnitus distress by bilateral auditory cortex tDCS, tACS, and tRNS. tRNS significantly improves both tinnitus loudness and tinnitus distress in comparison to tDCS and tACS.

References

    1. Jastreboff PJ. Phantom auditory perception (tinnitus): mechanisms of generation and perception. Neurosci Res (1990) 8:221–5410.1016/0168-0102(90)90031-9
    1. Eggermont JJ, Roberts LE. The neuroscience of tinnitus. Trends Neurosci (2004) 27:676–8210.1016/j.tins.2004.08.010
    1. Axelsson A, Ringdahl A. Tinnitus – a study of its prevalence and characteristics. Br J Audiol (1989) 23:53–6210.3109/03005368909077819
    1. Scott B, Lindberg P. Psychological profile and somatic complaints between help-seeking and non-help-seeking tinnitus subjects. Psychosomatics (2000) 41:347–5210.1176/appi.psy.41.4.347
    1. Muhlnickel W, Elbert T, Taub E, Flor H. Reorganization of auditory cortex in tinnitus. Proc Natl Acad Sci U S A (1998) 95:10340–310.1073/pnas.95.17.10340
    1. De Ridder D, Elgoyhen AB, Romo R, Langguth B. Phantom percepts: tinnitus and pain as persisting aversive memory networks. Proc Natl Acad Sci U S A (2011) 108:8075–8010.1073/pnas.1018466108
    1. De Ridder D, Vanneste S, Freeman W. The Bayesian brain: phantom percepts resolve sensory uncertainty. Neurosci Biobehav Rev (in press).10.1016/j.neubiorev.2012.04.001
    1. Weisz N, Muller S, Schlee W, Dohrmann K, Hartmann T, Elbert T. The neural code of auditory phantom perception. J Neurosci (2007) 27:1479–8410.1523/JNEUROSCI.3711-06.2007
    1. Salvi RJ, Wang J, Ding D. Auditory plasticity and hyperactivity following cochlear damage. Hear Res (2000) 147:261–7410.1016/S0378-5955(00)00136-2
    1. Lockwood AH, Salvi RJ, Coad ML, Towsley ML, Wack DS, Murphy BW. The functional neuroanatomy of tinnitus: evidence for limbic system links and neural plasticity. Neurology (1998) 50:114–20
    1. Smits M, Kovacs S, De Ridder D, Peeters RR, van Hecke P, Sunaert S. Lateralization of functional magnetic resonance imaging (fMRI) activation in the auditory pathway of patients with lateralized tinnitus. Neuroradiology (2007) 49:669–7910.1007/s00234-007-0231-3
    1. Joliot M, Ribary U, Llinas R. Human oscillatory brain activity near 40 Hz coexists with cognitive temporal binding. Proc Natl Acad Sci U S A (1994) 91:11748–5110.1073/pnas.91.24.11748
    1. Steriade M. Grouping of brain rhythms in corticothalamic systems. Neuroscience (2006) 137:1087–10610.1016/j.neuroscience.2005.10.029
    1. Llinas R, Urbano FJ, Leznik E, Ramirez RR, van Marle HJ. Rhythmic and dysrhythmic thalamocortical dynamics: GABA systems and the edge effect. Trends Neurosci (2005) 28:325–3310.1016/j.tins.2005.04.006
    1. Llinás RR, Ribary U, Jeanmonod D, Kronberg E, Mitra PP. Thalamocortical dysrhythmia: a neurological and neuropsychiatric syndrome characterized by magnetoencephalography. Proc Natl Acad Sci U S A (1999) 96:15222–710.1073/pnas.96.26.15222
    1. Lorenz I, Muller N, Schlee W, Hartmann T, Weisz N. Loss of alpha power is related to increased gamma synchronization-A marker of reduced inhibition in tinnitus? Neurosci Lett (2009) 453:225–810.1016/j.neulet.2009.02.028
    1. van der Loo E, Gais S, Congedo M, Vanneste S, Plazier M, Menovsky T, et al. Tinnitus intensity dependent gamma oscillations of the contralateral auditory cortex. PLoS One (2009) 4:e7396.10.1371/journal.pone.0007396
    1. De Ridder D, van der Loo E, Vanneste S, Gais S, Plazier M, Kovacs S, et al. Theta-gamma dysrhythmia and auditory phantom perception. J Neurosurg (2011) 114:912–2110.3171/2010.11.JNS10335
    1. Bravo L, Mico JA, Rey-Brea R, Perez-Nievas B, Leza JC, Berrocoso E. Depressive-like states heighten the aversion to painful stimuli in a rat model of comorbid chronic pain and depression. Anesthesiology (2012) 117:613–2510.1097/ALN.0b013e3182657b3e
    1. Nguyen JP, Lefaucher JP, Le Guerinel C, Eizenbaum JF, Nakano N, Carpentier A, et al. Motor cortex stimulation in the treatment of central and neuropathic pain. Arch Med Res (2000) 31:263–510.1016/S0188-4409(00)00078-3
    1. De Ridder D, de Mulder G, Verstraeten E, Seidman M, Elisevich K, Sunaert S, et al. Auditory cortex stimulation for tinnitus. Acta Neurochir Suppl (2007) 97:451–62
    1. Ramirez RR, Kopell BH, Butson CR, Gaggl W, Friedland DR, Baillet S. Neuromagnetic source imaging of abnormal spontaneous activity in tinnitus patient modulated by electrical cortical stimulation. Conf Proc IEEE Eng Med Biol Soc (2009) 1:1940–410.1109/IEMBS.2009.5333457
    1. Langguth B, Schecklmann M, Lehner A, Landgrebe M, Poeppl TB, Kreuzer PM, et al. Neuroimaging and neuromodulation: complementary approaches for identifying the neuronal correlates of tinnitus. Front Syst Neurosci (2012) 6:15.10.3389/fnsys.2012.00015
    1. De Ridder D, de Mulder G, Walsh V, Muggleton N, Sunaert S, Moller A. Magnetic and electrical stimulation of the auditory cortex for intractable tinnitus. Case report. J Neurosurg (2004) 100:560–4
    1. Burger J, Frank E, Kreuzer P, Kleinjung T, Vielsmeier V, Landgrebe M, et al. Transcranial magnetic stimulation for the treatment of tinnitus: 4-year follow-up in treatment responders – a retrospective analysis. Brain Stimul (2011) 4:222–710.1016/j.brs.2010.11.003
    1. De Ridder D, Verstraeten E, van der Kelen K, de Mulder G, Sunaert S, Verlooy J, et al. Transcranial magnetic stimulation for tinnitus: influence of tinnitus duration on stimulation parameter choice and maximal tinnitus suppression. Otol Neurotol (2005) 26:616–910.1097/01.mao.0000194897.56592.11
    1. Fregni F, Marcondes R, Boggio PS, Marcolin MA, Rigonatti SP, Sanchez TG, et al. Transient tinnitus suppression induced by repetitive transcranial magnetic stimulation and transcranial direct current stimulation. Eur J Neurol (2006) 13:996–100110.1111/j.1468-1331.2006.01414.x
    1. Khedr EM, Rothwell JC, El-Atar A. One-year follow up of patients with chronic tinnitus treated with left temporoparietal rTMS. Eur J Neurol (2009) 16:404–810.1111/j.1468-1331.2008.02522.x
    1. Vanneste S, Plazier M, van de Heyning P, De Ridder D. Repetitive transcranial magnetic stimulation frequency dependent tinnitus improvement by double cone coil prefrontal stimulation. J Neurol Neurosurg Psychiatry (2011) 82:1160–410.1136/jnnp.2010.213959
    1. Vanneste S, Plazier M, van der Loo E, Ost J, van de Heyning P, De Ridder D. Burst transcranial magnetic stimulation: which tinnitus characteristics influence the amount of transient tinnitus suppression? Eur J Neurol (2010) 17:1141–710.1111/j.1468-1331.2010.02987.x
    1. Frank E, Schecklmann M, Landgrebe M, Burger J, Kreuzer P, Poeppl TB, et al. Treatment of chronic tinnitus with repeated sessions of prefrontal transcranial direct current stimulation: outcomes from an open-label pilot study. J Neurol (2012) 259:327–3310.1007/s00415-011-6189-4
    1. Faber M, Vanneste S, Fregni F, De Ridder D. Top down prefrontal affective modulation of tinnitus with multiple sessions of tDCS of dorsolateral prefrontal cortex. Brain Stimul (2011) 5(4):492–810.1016/j.brs.2011.09.003
    1. Vanneste S, Plazier M, Ost J, van der Loo E, van de Heyning P, De Ridder D. Bilateral dorsolateral prefrontal cortex modulation for tinnitus by transcranial direct current stimulation: a preliminary clinical study. Exp Brain Res (2010) 202:779–8510.1007/s00221-010-2183-9
    1. Miranda PC, Lomarev M, Hallett M. Modeling the current distribution during transcranial direct current stimulation. Clin Neurophysiol (2006) 117:1623–910.1016/j.clinph.2006.04.009
    1. George MS, Aston-Jones G. Noninvasive techniques for probing neurocircuitry and treating illness: vagus nerve stimulation (VNS), transcranial magnetic stimulation (TMS) and transcranial direct current stimulation (tDCS). Neuropsychopharmacology (2010) 35:301–1610.1038/npp.2009.87
    1. Dymond AM, Coger RW, Serafetinides EA. Intracerebral current levels in man during electrosleep therapy. Biol Psychiatry (1975) 10:101–4
    1. Monte-Silva K, Kuo MF, Hessenthaler S, Fresnoza S, Liebetanz D, Paulus W, et al. Induction of late LTP-like plasticity in the human motor cortex by repeated non-invasive brain stimulation. Brain Stimul (2012) 6(3):424–3210.1016/j.brs.2012.04.011
    1. Antal A, Kincses TZ, Nitsche MA, Bartfai O, Paulus W. Excitability changes induced in the human primary visual cortex by transcranial direct current stimulation: direct electrophysiological evidence. Invest Ophthalmol Vis Sci (2004) 45:702–710.1167/iovs.03-0688
    1. Zaghi S, de Freitas Rezende L, de Oliveira LM, El-Nazer R, Menning S, Tadini L, et al. Inhibition of motor cortex excitability with 15Hz transcranial alternating current stimulation (tACS). Neurosci Lett (2010) 479:211–410.1016/j.neulet.2010.05.060
    1. Zaehle T, Rach S, Herrmann CS. Transcranial alternating current stimulation enhances individual alpha activity in human EEG. PLoS One (2010) 5:e13766.10.1371/journal.pone.0013766
    1. Datta A, Dmochowski JP, Guleyupoglu B, Bikson M, Fregni F. Cranial electrotherapy stimulation and transcranial pulsed current stimulation: a computer based high-resolution modeling study. Neuroimage (2013) 65:280–710.1016/j.neuroimage.2012.09.062
    1. Terney D, Chaieb L, Moliadze V, Antal A, Paulus W. Increasing human brain excitability by transcranial high-frequency random noise stimulation. J Neurosci (2008) 28:14147–5510.1523/JNEUROSCI.4248-08.2008
    1. Nitsche MA, Boggio PS, Fregni F, Pascual-Leone A. Treatment of depression with transcranial direct current stimulation (tDCS): a review. Exp Neurol (2009) 219:14–9
    1. Fertonani A, Pirulli C, Miniussi C. Random noise stimulation improves neuroplasticity in perceptual learning. J Neurosci (2011) 31:15416–2310.1523/JNEUROSCI.2002-11.2011
    1. Garin P, Gilain C, Van Damme JP, de Fays K, Jamart J, Ossemann M, et al. Short- and long-lasting tinnitus relief induced by transcranial direct current stimulation. J Neurol (2011) 258(11):1940–810.1007/s00415-011-6037-6
    1. Langguth B, De Ridder D, Dornhoffer JL, Eichhammer P, Folmer RL, Frank E, et al. Controversy: does repetitive transcranial magnetic stimulation/transcranial direct current stimulation show efficacy in treating tinnitus patients? Brain Stimul (2008) 1:192–20510.1016/j.brs.2008.06.003
    1. Vanneste S, De Ridder D. Bifrontal transcranial direct current stimulation modulates tinnitus intensity and tinnitus-distress-related brain activity. Eur J Neurosci (2011) 34:605–1410.1111/j.1460-9568.2011.07778.x
    1. Vanneste S, Focquaert F, van de Heyning P, De Ridder D. Different resting state brain activity and functional connectivity in patients who respond and not respond to bifrontal tDCS for tinnitus suppression. Exp Brain Res (2011) 210:217–2710.1007/s00221-011-2617-z
    1. Vanneste S, Langguth B, De Ridder D. Do tDCS and TMS influence tinnitus transiently via a direct cortical and indirect somatosensory modulating effect? A combined TMS-tDCS and TENS study. Brain Stimulat (2011) 4:242–5210.1016/j.brs.2010.12.001
    1. Zaghi S, Acar M, Hultgren B, Boggio PS, Fregni F. Noninvasive brain stimulation with low-intensity electrical currents: putative mechanisms of action for direct and alternating current stimulation. Neuroscientist (2010) 16:285–30710.1177/1073858409336227
    1. Llinas RR, Ribary U, Jeanmonod D, Kronberg E, Mitra PP. Thalamocortical dysrhythmia: a neurological and neuropsychiatric syndrome characterized by magnetoencephalography. Proc Natl Acad Sci U S A (1999) 96:15222–710.1073/pnas.96.26.15222
    1. Tass PA, Adamchic I, Freund HJ, von Stackelberg T, Hauptmann C. Counteracting tinnitus by acoustic coordinated reset neuromodulation. Restor Neurol Neurosci (2012) 30(2):137–59
    1. Klimesch W, Doppelmayr M, Schwaiger J, Auinger P, Winkler T. ‘Paradoxical’ alpha synchronization in a memory task. Brain Res Cogn Brain Res (1999) 7:493–50110.1016/S0926-6410(98)00056-1
    1. Plazier M, Joos K, Vanneste S, Ost J, De Ridder D. Bifrontal and bioccipital transcranial direct current stimulation (tDCS) does not induce mood changes in healthy volunteers: a placebo controlled study. Brain Stimulat (2011) 5(4):454–6110.1016/j.brs.2011.07.005
    1. Boggio PS, Rigonatti SP, Ribeiro RB, Myczkowski ML, Nitsche MA, Pascual-Leone A, et al. A randomized, double-blind clinical trial on the efficacy of cortical direct current stimulation for the treatment of major depression. Int J Neuropsychopharmacol (2008) 11:249–5410.1017/S1461145707007833
    1. Siebert WM. Some implications of the stochastic behavior of primary auditory neurons. Kybernetik (1965) 2:206–1510.1007/BF00306416
    1. Rodieck RW, Kiang NY, Gerstein GL. Some quantitative methods for the study of spontaneous activity of single neurons. Biophys J (1962) 2:351–6810.1016/S0006-3495(62)86860-X
    1. Luczak A, Bartho P, Harris KD. Spontaneous events outline the realm of possible sensory responses in neocortical populations. Neuron (2009) 62:413–2510.1016/j.neuron.2009.03.014
    1. Ochi K, Eggermont JJ. Effects of quinine on neural activity in cat primary auditory cortex. Hear Res (1997) 105:105–1810.1016/S0378-5955(96)00201-8
    1. Parazzini M, Fiocchi S, Ravazzani P. Electric field and current density distribution in an anatomical head model during transcranial direct current stimulation for tinnitus treatment. Bioelectromagnetics (2012) 33:476–8710.1002/bem.21708
    1. Mendonca ME, Santana MB, Baptista AF, Datta A, Bikson M, Fregni F, et al. Transcranial DC stimulation in fibromyalgia: optimized cortical target supported by high-resolution computational models. J Pain (2011) 12:610–710.1016/j.jpain.2010.12.015
    1. Fregni F, Boggio PS, Lima MC, Ferreira MJ, Wagner T, Rigonatti SP, et al. A sham-controlled, phase II trial of transcranial direct current stimulation for the treatment of central pain in traumatic spinal cord injury. Pain (2006) 122:197–20910.1016/j.pain.2006.02.023

Source: PubMed

Подписаться