Anterior cingulate implants for tinnitus: report of 2 cases

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Tinnitus can be distressful, and tinnitus distress has been linked to increased beta oscillatory activity in the dorsal anterior cingulate cortex (dACC). The amount of distress is linked to alpha activity in the medial temporal lobe (amygdala and parahippocampal area), as well as the subgenual (sg)ACC and insula, and the functional connectivity between the parahippocampal area and the sgACC at 10 and 11.5 Hz.

The authors describe 2 patients with very severely distressing intractable tinnitus who underwent transcranial magnetic stimulation (TMS) with a double-cone coil targeting the dACC and subsequent implantation of electrodes on the dACC. One of the patients responded to the implant and one did not, even though phenomenologically they both expressed the same tinnitus loudness and distress.

The responder has remained dramatically improved for more than 2 years with 6-Hz burst stimulation of the dACC. The 2 patients differed in functional connectivity between the area of the implant and a tinnitus network consisting of the parahippocampal area as well as the sgACC and insula; that is, the responder had increased functional connectivity between these areas, whereas the nonresponder had decreased functional connectivity between these areas. Only the patient with increased functional connectivity linked to the target area of repetitive TMS or implantation might transmit the stimulation current to the entire tinnitus network and thus clinically improve.

ABBREVIATIONSACC = anterior cingulate cortex; BA = Brodmann area; BOLD = blood oxygen level-dependent; d = dorsal; DLPFC = dorsolateral prefrontal cortex; EEG = electroencephalography; fMRI = functional MRI; HADS = Hospital Anxiety Depression Scale; MEG = magnetoencephalography; NRS = numeric rating scale; r = repetitive; sg = subgenual; sLORETA = standardized low-resolution electromagnetic tomography; tDCS = transcranial direct current stimulation; TENS = transcutaneous electrical nerve stimulation; TMS = transcranial magnetic stimulation; TQ = tinnitus questionnaire.
Article Information

Contributor Notes

Correspondence Dirk De Ridder, Department of Surgical Sciences, Section of Neurosurgery, Dunedin School of Medicine, University of Otago, P.O. Box 56, Leith St., Dunedin 9054, New Zealand. email: dirk.deridder@otago.ac.nz.INCLUDE WHEN CITING Published online August 28, 2015; DOI: 10.3171/2015.3.JNS142880.Disclosure Dr. De Ridder is a consultant for, holds a patent with, has received clinical or research support for the study described, and has received support for non-study-related clinical or research effort from St. Jude Medical.

© AANS, except where prohibited by US copyright law.

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References
  • 1

    Azevedo AAFigueiredo RR: Tinnitus treatment with acamprosate: double–blind study. Braz J Otorhinolaryngol 71:6186232005

  • 2

    Boccard SGFitzgerald JJPereira EAMoir LVan Hartevelt TJKringelbach ML: Targeting the affective component of chronic pain: a case series of deep brain stimulation of the anterior cingulate cortex. Neurosurgery 74:6286372014

    • Search Google Scholar
    • Export Citation
  • 3

    Congedo MJohn REDe Ridder DPrichep LIsenhart R: On the “dependence” of “independent” group EEG sources; an EEG study on two large databases. Brain Topogr 23:1341382010

    • Search Google Scholar
    • Export Citation
  • 4

    De Ridder DDe Mulder GWalsh VMuggleton NSunaert SMøller A: Magnetic and electrical stimulation of the auditory cortex for intractable tinnitus. Case report. J Neurosurg 100:5605642004

    • Search Google Scholar
    • Export Citation
  • 5

    De Ridder DElgoyhen ABRomo RLangguth B: Phantom percepts: tinnitus and pain as persisting aversive memory networks. Proc Natl Acad Sci USA 108:807580802011

    • Search Google Scholar
    • Export Citation
  • 6

    De Ridder DFransen HFrancois OSunaert SKovacs SVan De Heyning P: Amygdalohippocampal involvement in tinnitus and auditory memory. Acta Otolaryngol Suppl 126:50532006

    • Search Google Scholar
    • Export Citation
  • 7

    De Ridder Dvan der Loo EVan der Kelen KMenovsky Tvan de Heyning PMoller A: Do tonic and burst TMS modulate the lemniscal and extralemniscal system differentially?. Int J Med Sci 4:2422462007

    • Search Google Scholar
    • Export Citation
  • 8

    De Ridder Dvan der Loo EVan der Kelen KMenovsky Tvan de Heyning PMoller A: Theta, alpha and beta burst transcranial magnetic stimulation: brain modulation in tinnitus. Int J Med Sci 4:2372412007

    • Search Google Scholar
    • Export Citation
  • 9

    De Ridder DVanneste S: Targeting the parahippocampal area by auditory cortex stimulation in tinnitus. Brain Stimul 7:7097172014

  • 10

    De Ridder DVanneste SCongedo M: The distressed brain: a group blind source separation analysis on tinnitus. PLoS One 6:e242732011

  • 11

    De Ridder DVanneste SFreeman W: The Bayesian brain: Phantom percepts resolve sensory uncertainty. Neurosci Biobehav Rev 44:4152014

    • Search Google Scholar
    • Export Citation
  • 12

    De Ridder DVanneste SKovacs SSunaert SMenovsky Tvan de Heyning P: Transcranial magnetic stimulation and extradural electrodes implanted on secondary auditory cortex for tinnitus suppression. J Neurosurg 114:9039112011

    • Search Google Scholar
    • Export Citation
  • 13

    De Ridder DVanneste SMenovsky TLangguth B: Surgical brain modulation for tinnitus: the past, present and future. J Neurosurg Sci 56:3233402012

    • Search Google Scholar
    • Export Citation
  • 14

    De Ridder DVanneste SPlazier MMenovsky Tvan de Heyning PKovacs S: Dorsolateral prefrontal cortex transcranial magnetic stimulation and electrode implant for intractable tinnitus. World Neurosurg 77:7787842012

    • Search Google Scholar
    • Export Citation
  • 15

    De Ridder DVanneste SPlazier Mvan der Loo EMenovsky T: Burst spinal cord stimulation: toward paresthe– sia-free pain suppression. Neurosurgery 66:9869902010

    • Search Google Scholar
    • Export Citation
  • 16

    De Ridder DVanneste Svan der Loo EPlazier MMenovsky Tvan de Heyning P: Burst stimulation of the auditory cortex: a new form of neurostimulation for noise-like tinnitus suppression. J Neurosurg 112:128912942010

    • Search Google Scholar
    • Export Citation
  • 17

    De Ridder DVanneste SWeisz NLondero ASchlee WElgoyhen AB: An integrative model of auditory phantom perception: tinnitus as a unified percept of interacting separable subnetworks. Neurosci Biobehav Rev 44:16322014

    • Search Google Scholar
    • Export Citation
  • 18

    De Ridder DVerstraeten EVan der Kelen KDe Mulder GSunaert SVerlooy J: Transcranial magnetic stimulation for tinnitus: influence of tinnitus duration on stimulation parameter choice and maximal tinnitus suppression. Otol Neurotol 26:6166192005

    • Search Google Scholar
    • Export Citation
  • 19

    Goebel GHiller W: The tinnitus questionnaire. A standard instrument for grading the degree of tinnitus. Results of a multicenter study with the tinnitus questionnaire. HNO 42:1661721994. (Ger)

    • Search Google Scholar
    • Export Citation
  • 20

    Jastreboff PJ: Phantom auditory perception (tinnitus): mechanisms of generation and perception. Neurosci Res 8:2212541990

  • 21

    Joos KVanneste SDe Ridder D: Disentangling depression and distress networks in the tinnitus brain. PLoS One 7:e405442012

  • 22

    Landgrebe MLangguth BRosengarth KBraun SKoch AKleinjung T: Structural brain changes in tinnitus: grey matter decrease in auditory and non-auditory brain areas. Neuroimage 46:2132182009

    • Search Google Scholar
    • Export Citation
  • 23

    Langguth BKreuzer PMKleinjung TDe Ridder D: Tinnitus: causes and clinical management. Lancet Neurol 12:9209302013

  • 24

    Langguth BSchecklmann MLehner ALandgrebe MPo– eppl TBKreuzer PM: Neuroimaging and neuromodulation: complementary approaches for identifying the neuronal correlates of tinnitus. Front Syst Neurosci 6:152012

    • Search Google Scholar
    • Export Citation
  • 25

    Lipsman NWoodside DBGiacobbe PHamani CCarter JCNorwood SJ: Subcallosal cingulate deep brain stimulation for treatment-refractory anorexia nervosa: a phase 1 pilot trial. Lancet 381:136113702013

    • Search Google Scholar
    • Export Citation
  • 26

    Maudoux ALefebvre PCabay JEDemertzi AVanhaudenhuyse ALaureys S: Auditory resting-state network connectivity in tinnitus: a functional MRI study. PLoS One 7:e362222012

    • Search Google Scholar
    • Export Citation
  • 27

    Maudoux ALefebvre PCabay JEDemertzi AVanhaudenhuyse ALaureys S: Connectivity graph analysis of the auditory resting state network in tinnitus. Brain Res 1485:10212012

    • Search Google Scholar
    • Export Citation
  • 28

    Mayberg HSLozano AMVoon VMcNeely HESeminowicz DHamani C: Deep brain stimulation for treatment-resistant depression. Neuron 45:6516602005

    • Search Google Scholar
    • Export Citation
  • 29

    Meeus ODe Ridder DVan de Heyning P: Administration of the combination clonazepam-Deanxit as treatment for tinnitus. Otol Neurotol 32:7017092011

    • Search Google Scholar
    • Export Citation
  • 30

    Norena AMicheyl CChéry-Croze SCollet L: Psychoacoustic characterization of the tinnitus spectrum: implications for the underlying mechanisms of tinnitus. Audiol Neurootol 7:3583692002

    • Search Google Scholar
    • Export Citation
  • 31

    Noreña AJEggermont JJ: Enriched acoustic environment after noise trauma abolishes neural signs of tinnitus. Neuroreport 17:5595632006

    • Search Google Scholar
    • Export Citation
  • 32

    Nowé VVan de Heyning PParizel PM: MRI in patients with otovestibular complaints of unknown origin. B-ENT 3:Suppl 727352007

  • 33

    Pascual-Marqui R: Discrete, 3D distributed, linear imaging methods of electric neuronal activity. Part 1: exact, zero error localization. (http://arxiv.org/abs/0710.3341)Accessed June 25 2015

    • Export Citation
  • 34

    Pascual-Marqui R: Instantaneous and lagged measurements of linear and nonlinear dependence between groups of multivariate time series: frequency decomposition. http://arxiv.org/abs/0711.1455Accessed June 25 2015

    • Export Citation
  • 35

    Pascual-Marqui RD: Standardized low-resolution brain electromagnetic tomography (sLORETA): technical details. Methods Find Exp Clin Pharmacol 24:Suppl D5122002

    • Search Google Scholar
    • Export Citation
  • 36

    Sadaghiani SHesselmann GKleinschmidt A: Distributed and antagonistic contributions of ongoing activity fluctuations to auditory stimulus detection. J Neurosci 29:13410134172009

    • Search Google Scholar
    • Export Citation
  • 37

    Schecklmann MLandgrebe MPoeppl TBKreuzer PManner PMarienhagen J: Neural correlates of tinnitus duration and distress: A positron emission tomography study. Hum Brain Mapp 34:2332402013

    • Search Google Scholar
    • Export Citation
  • 38

    Schlee WHartmann TLangguth BWeisz N: Abnormal resting–state cortical coupling in chronic tinnitus. BMC Neurosci 10:112009

  • 39

    Schlee WWeisz NBertrand OHartmann TElbert T: Using auditory steady state responses to outline the functional connectivity in the tinnitus brain. PLoS One 3:e37202008

    • Search Google Scholar
    • Export Citation
  • 40

    Seeley WWMenon VSchatzberg AFKeller JGlover GHKenna H: Dissociable intrinsic connectivity networks for salience processing and executive control. J Neurosci 27:234923562007

    • Search Google Scholar
    • Export Citation
  • 41

    Smits MKovacs Sde Ridder DPeeters RRvan Hecke PSunaert S: Lateralization of functional magnetic resonance imaging (fMRI) activation in the auditory pathway of patients with lateralized tinnitus. Neuroradiology 49:6696792007

    • Search Google Scholar
    • Export Citation
  • 42

    Song JJDe Ridder DVan de Heyning PVanneste S: Mapping tinnitus–related brain activation: an activation–likelihood estimation metaanalysis of PET studies. J Nucl Med 53:155015572012

    • Search Google Scholar
    • Export Citation
  • 43

    van der Loo ECongedo MVanneste SVan De Heyning PDe Ridder D: Insular lateralization in tinnitus distress. Auton Neurosci 165:1911942011

    • Search Google Scholar
    • Export Citation
  • 44

    van der Loo EGais SCongedo MVanneste SPlazier MMenovsky T: Tinnitus intensity dependent gamma oscillations of the contralateral auditory cortex. PLoS One 4:e73962009

    • Search Google Scholar
    • Export Citation
  • 45

    Vanneste SAzevedo ADe Ridder D: The effect of naltrexone on the perception and distress in tinnitus: an open-label pilot study. Int J Clin Pharmacol Ther 51:5112013

    • Search Google Scholar
    • Export Citation
  • 46

    Vanneste SCongedo MDe Ridder D: Pinpointing a highly specific pathological functional connection that turns phantom sound into distress. Cereb Cortex 24:226822822013

    • Search Google Scholar
    • Export Citation
  • 47

    Vanneste SHeyning PVRidder DD: Contralateral parahippocampal gamma-band activity determines noise-like tinnitus laterality: a region of interest analysis. Neuroscience 199:4814902011

    • Search Google Scholar
    • Export Citation
  • 48

    Vanneste SDe Ridder D: The auditory and non-auditory brain areas involved in tinnitus. An emergent property of multiple parallel overlapping subnetworks. Front Syst Neurosci 6:312012

    • Search Google Scholar
    • Export Citation
  • 49

    Vanneste SDe Ridder D: Bifrontal transcranial direct current stimulation modulates tinnitus intensity and tinnitus-distress-related brain activity. Eur J Neurosci 34:6056142011

    • Search Google Scholar
    • Export Citation
  • 50

    Vanneste SDe Ridder D: Brain areas controlling heart rate variability in tinnitus and tinnitus–related distress. PLoS One 8:e597282013

    • Search Google Scholar
    • Export Citation
  • 51

    Vanneste SDe Ridder D: Differences between a single session and repeated sessions of 1 Hz TMS by double–cone coil prefrontal stimulation for the improvement of tinnitus. Brain Stimul 6:1551592013

    • Search Google Scholar
    • Export Citation
  • 52

    Vanneste SFigueiredo RDe Ridder D: Treatment of tinnitus with cyclobenzaprine: an open–label study. Int J Clin Pharmacol Ther 50:3383442012

    • Search Google Scholar
    • Export Citation
  • 53

    Vanneste SOst JLangguth BDe Ridder D: TMS by double-cone coil prefrontal stimulation for medication resistant chronic depression: a case report. Neurocase 20:61682014

    • Search Google Scholar
    • Export Citation
  • 54

    Vanneste SPlazier MVan de Heyning PDe Ridder D: Repetitive transcranial magnetic stimulation frequency dependent tinnitus improvement by double cone coil prefrontal stimulation. J Neurol Neurosurg Psychiatry 82:116011642011

    • Search Google Scholar
    • Export Citation
  • 55

    Vanneste SPlazier MVan de Heyning PDe Ridder D: Transcutaneous electrical nerve stimulation (TENS) of upper cervical nerve (C2) for the treatment of somatic tinnitus. Exp Brain Res 204:2832872010

    • Search Google Scholar
    • Export Citation
  • 56

    Vanneste SPlazier Mder Loo Evde Heyning PVCongedo MDe Ridder D: The neural correlates of tinnitus-related distress. Neuroimage 52:4704802010

    • Search Google Scholar
    • Export Citation
  • 57

    Vanneste Svan de Heyning PDe Ridder D: The neural network of phantom sound changes over time: a comparison between recent-onset and chronic tinnitus patients. Eur J Neurosci 34:7187312011

    • Search Google Scholar
    • Export Citation
  • 58

    Vanneste Svan Dongen MDe Vree BHiseni Svan der Velden EStrydis C: Does enriched acoustic environment in humans abolish chronic tinnitus clinically and electrophysiologically? A double blind placebo controlled study. Hear Res 296:1411482013

    • Search Google Scholar
    • Export Citation
  • 59

    Weisz NHartmann TDohrmann KSchlee WNorena A: High–frequency tinnitus without hearing loss does not mean absence of deafferentation. Hear Res 222:1081142006

    • Search Google Scholar
    • Export Citation
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