Table of Contents Author Guidelines Submit a Manuscript
BioMed Research International
Volume 2015, Article ID 489619, 15 pages
http://dx.doi.org/10.1155/2015/489619
Research Article

Source-Space Cross-Frequency Amplitude-Amplitude Coupling in Tinnitus

MRC Institute of Hearing Research, University Park, Nottingham NG7 2RD, UK

Received 29 July 2015; Revised 19 October 2015; Accepted 26 October 2015

Academic Editor: Stefan Rampp

Copyright © 2015 Oliver Zobay and Peyman Adjamian. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. D. Baguley, D. McFerran, and D. Hall, “Tinnitus,” The Lancet, vol. 382, no. 9904, pp. 1600–1607, 2013. View at Publisher · View at Google Scholar · View at Scopus
  2. S. I. Erlandsson and L. R.-M. Hallberg, “Prediction of quality of life in patients with tinnitus,” British Journal of Audiology, vol. 34, no. 1, pp. 11–19, 2000. View at Publisher · View at Google Scholar · View at Scopus
  3. J. A. Kaltenbach, “Tinnitus: models and mechanisms,” Hearing Research, vol. 276, no. 1-2, pp. 52–60, 2011. View at Publisher · View at Google Scholar · View at Scopus
  4. S. Yang, B. D. Weiner, L. S. Zhang, S.-J. Cho, and S. Bao, “Homeostatic plasticity drives tinnitus perception in an animal model,” Proceedings of the National Academy of Sciences of the United States of America, vol. 108, no. 36, pp. 14974–14979, 2011. View at Publisher · View at Google Scholar · View at Scopus
  5. A. H. Lockwood, R. J. Salvi, M. L. Coad, M. L. Towsley, D. S. Wack, and B. W. Murphy, “The functional neuroanatomy of tinnitus—evidence for limbic system links and neural plasticity,” Neurology, vol. 50, no. 1, pp. 114–120, 1998. View at Publisher · View at Google Scholar · View at Scopus
  6. A. H. Lockwood, D. S. Wack, R. F. Burkard et al., “The functional anatomy of gaze-evoked tinnitus and sustained lateral gaze,” Neurology, vol. 56, no. 4, pp. 472–480, 2001. View at Publisher · View at Google Scholar · View at Scopus
  7. F. Mirz, C. B. Pedersen, K. Ishizu et al., “Positron emission tomography of cortical centers of tinnitus,” Hearing Research, vol. 134, no. 1-2, pp. 133–144, 1999. View at Publisher · View at Google Scholar · View at Scopus
  8. J. R. Melcher, I. S. Sigalovsky, J. J. Guinan Jr., and R. A. Levine, “Lateralized tinnitus studied with functional magnetic resonance imaging: abnormal inferior colliculus activation,” Journal of Neurophysiology, vol. 83, no. 2, pp. 1058–1072, 2000. View at Google Scholar · View at Scopus
  9. P. Adjamian, M. Sereda, and D. A. Hall, “The mechanisms of tinnitus: perspectives from human functional neuroimaging,” Hearing Research, vol. 253, no. 1-2, pp. 15–31, 2009. View at Publisher · View at Google Scholar · View at Scopus
  10. C. P. Lanting, E. de Kleine, and P. van Dijk, “Neural activity underlying tinnitus generation: results from PET and fMRI,” Hearing Research, vol. 255, no. 1-2, pp. 1–13, 2009. View at Publisher · View at Google Scholar · View at Scopus
  11. R. R. Llinás, U. Ribary, D. Jeanmonod, E. Kronberg, and P. P. Mitra, “Thalamocortical dysrhythmia: a neurological and neuropsychiatric syndrome characterized by magnetoencephalography,” Proceedings of the National Academy of Sciences of the United States of America, vol. 96, no. 26, pp. 15222–15227, 1999. View at Publisher · View at Google Scholar · View at Scopus
  12. R. Llinás, F. J. Urbano, E. Leznik, R. R. Ramírez, and H. J. F. van Marle, “Rhythmic and dysrhythmic thalamocortical dynamics: GABA systems and the edge effect,” Trends in Neurosciences, vol. 28, no. 6, pp. 325–333, 2005. View at Publisher · View at Google Scholar · View at Scopus
  13. N. Weisz, S. Moratti, M. Meinzer, K. Dohrmann, and T. Elbert, “Tinnitus perception and distress is related to abnormal spontaneous brain activity as measured by magnetoencephalography,” PLoS Medicine, vol. 2, no. 6, pp. 546–553, 2005. View at Publisher · View at Google Scholar · View at Scopus
  14. N. Weisz, S. Müller, W. Schlee, K. Dohrmann, T. Hartmann, and T. Elbert, “The neural code of auditory phantom perception,” The Journal of Neuroscience, vol. 27, no. 6, pp. 1479–1484, 2007. View at Publisher · View at Google Scholar · View at Scopus
  15. H. Ashton, K. Reid, R. Marsh, I. Johnson, K. Alter, and T. Griffiths, “High frequency localised ‘hot spots’ in temporal lobes of patients with intractable tinnitus: a quantitative electroencephalographic (QEEG) study,” Neuroscience Letters, vol. 426, no. 1, pp. 23–28, 2007. View at Publisher · View at Google Scholar · View at Scopus
  16. M. Moazami-Goudarzi, L. Michels, N. Weisz, and D. Jeanmonod, “Temporo-insular enhancement of EEG low and high frequencies in patients with chronic tinnitus. QEEG study of chronic tinnitus patients,” BMC Neuroscience, vol. 11, article 40, 2010. View at Publisher · View at Google Scholar · View at Scopus
  17. P. Adjamian, M. Sereda, O. Zobay, D. A. Hall, and A. R. Palmer, “Neuromagnetic indicators of tinnitus and tinnitus masking in patients with and without hearing loss,” Journal of the Association for Research in Otolaryngology, vol. 13, no. 5, pp. 715–731, 2012. View at Publisher · View at Google Scholar · View at Scopus
  18. I. Adamchic, T. Toth, C. Hauptmann, and P. A. Tass, “Reversing pathologically increased EEG power by acoustic coordinated reset neuromodulation,” Human Brain Mapping, vol. 35, no. 5, pp. 2099–2118, 2014. View at Publisher · View at Google Scholar · View at Scopus
  19. E. W. J. Weiler and K. Brill, “Quantitative electroencephalography patterns in patients suffering from tinnitus,” International Tinnitus Journal, vol. 10, no. 2, pp. 127–131, 2004. View at Google Scholar · View at Scopus
  20. P. Adjamian, “The application of electro- and magneto-encephalography in tinnitus research—methods and interpretations,” Frontiers in Neurology, vol. 5, article 228, 2014. View at Publisher · View at Google Scholar · View at Scopus
  21. O. Zobay, A. R. Palmer, D. A. Hall, M. Sereda, P. Adjamian, and B. Langguth, “Source space estimation of oscillatory power and brain connectivity in tinnitus,” PLoS ONE, vol. 10, no. 3, Article ID e0120123, 2015. View at Publisher · View at Google Scholar
  22. R. Llinás, U. Ribary, D. Jeanmonod et al., “Thalamocortical dysrhythmia I. Functional and imaging aspects,” Thalamus & Related Systems, vol. 1, no. 3, pp. 237–244, 2001. View at Publisher · View at Google Scholar · View at Scopus
  23. G. Fuggetta, M. A. Bennett, P. A. Duke, and A. M. J. Young, “Quantitative electroencephalography as a biomarker for proneness toward developing psychosis,” Schizophrenia Research, vol. 153, no. 1–3, pp. 68–77, 2014. View at Publisher · View at Google Scholar · View at Scopus
  24. D. Jeanmonod, J. Schulman, R. Ramirez et al., “Neuropsychiatric thalamocortical dysrhythmia: surgical implications,” Thalamus & Related Systems, vol. 2, no. 2, pp. 103–113, 2003. View at Publisher · View at Google Scholar · View at Scopus
  25. N. J. Ray, N. Jenkinson, M. L. Kringelbach et al., “Abnormal thalamocortical dynamics may be altered by deep brain stimulation: using magnetoencephalography to study phantom limb pain,” Journal of Clinical Neuroscience, vol. 16, no. 1, pp. 32–36, 2009. View at Publisher · View at Google Scholar · View at Scopus
  26. S. Velikova, M. Locatelli, C. Insacco, E. Smeraldi, G. Comi, and L. Leocani, “Dysfunctional brain circuitry in obsessive-compulsive disorder: source and coherence analysis of EEG rhythms,” NeuroImage, vol. 49, no. 1, pp. 977–983, 2010. View at Publisher · View at Google Scholar · View at Scopus
  27. S. Vanneste and D. De Ridder, “Bifrontal transcranial direct current stimulation modulates tinnitus intensity and tinnitus-distress-related brain activity,” European Journal of Neuroscience, vol. 34, no. 4, pp. 605–614, 2011. View at Publisher · View at Google Scholar · View at Scopus
  28. S. Vanneste, J.-J. Song, and D. De Ridder, “Tinnitus and musical hallucinosis: the same but more,” NeuroImage, vol. 82, pp. 373–383, 2013. View at Publisher · View at Google Scholar · View at Scopus
  29. P. Adjamian, D. A. Hall, A. R. Palmer, T. W. Allan, and D. R. M. Langers, “Neuroanatomical abnormalities in chronic tinnitus in the human brain,” Neuroscience and Biobehavioral Reviews, vol. 45, pp. 119–133, 2014. View at Publisher · View at Google Scholar · View at Scopus
  30. E. Maris and R. Oostenveld, “Nonparametric statistical testing of EEG- and MEG-data,” Journal of Neuroscience Methods, vol. 164, no. 1, pp. 177–190, 2007. View at Publisher · View at Google Scholar · View at Scopus
  31. C. W. Newman, G. P. Jacobson, and J. B. Spitzer, “Development of the tinnitus handicap inventory,” Archives of Otolaryngology—Head & Neck Surgery, vol. 122, no. 2, pp. 143–148, 1996. View at Publisher · View at Google Scholar · View at Scopus
  32. A. McCombe, D. Baguley, R. Coles, L. McKenna, C. McKinney, and P. Windle-Taylor, “Guidelines for the grading of tinnitus severity: the results of a working group commissioned by the British Association of Otolaryngologists, Head and Neck Surgeons, 1999,” Clinical Otolaryngology and Allied Sciences, vol. 26, no. 5, pp. 388–393, 2001. View at Publisher · View at Google Scholar · View at Scopus
  33. S. Khalfa, S. Dubal, E. Veuillet, F. Perez-Diaz, R. Jouvent, and L. Collet, “Psychometric normalization of a hyperacusis questionnaire,” ORL, vol. 64, no. 6, pp. 436–442, 2002. View at Publisher · View at Google Scholar · View at Scopus
  34. L. E. Roberts, G. Moffat, M. Baumann, L. M. Ward, and D. J. Bosnyak, “Residual inhibition functions overlap tinnitus spectra and the region of auditory threshold shift,” Journal of the Association for Research in Otolaryngology, vol. 9, no. 4, pp. 417–435, 2008. View at Publisher · View at Google Scholar · View at Scopus
  35. M. Sereda, D. A. Hall, D. J. Bosnyak et al., “Re-examining the relationship between audiometric profile and tinnitus pitch,” International Journal of Audiology, vol. 50, no. 5, pp. 303–312, 2011. View at Publisher · View at Google Scholar · View at Scopus
  36. P. Adjamian, G. R. Barnes, A. Hillebrand et al., “Co-registration of magnetoencephalography with magnetic resonance imaging using bite-bar-based fiducials and surface-matching,” Clinical Neurophysiology, vol. 115, no. 3, pp. 691–698, 2004. View at Publisher · View at Google Scholar · View at Scopus
  37. R. Oostenveld, P. Fries, E. Maris, and J.-M. Schoffelen, “FieldTrip: open source software for advanced analysis of MEG, EEG, and invasive electrophysiological data,” Computational Intelligence and Neuroscience, vol. 2011, Article ID 156869, 9 pages, 2011. View at Publisher · View at Google Scholar · View at Scopus
  38. D. W. Shattuck and R. M. Leahy, “BrainSuite: an automated cortical surface identification tool,” Medical Image Analysis, vol. 6, no. 2, pp. 129–142, 2002. View at Publisher · View at Google Scholar · View at Scopus
  39. B. D. van Veen, W. van Drongelen, M. Yuchtman, and A. Suzuki, “Localization of brain electrical activity via linearly constrained minimum variance spatial filtering,” IEEE Transactions on Biomedical Engineering, vol. 44, no. 9, pp. 867–880, 1997. View at Publisher · View at Google Scholar · View at Scopus
  40. J. Vrba and S. E. Robinson, “Signal processing in magnetoencephalography,” Methods, vol. 25, no. 2, pp. 249–271, 2001. View at Publisher · View at Google Scholar · View at Scopus
  41. K. Sekihara and S. S. Nagarajan, Adaptive Spatial Filters for Electromagnetic Brain Imaging, Springer, Berlin, Germany, 2008. View at Publisher · View at Google Scholar
  42. M. J. Brookes, J. Vrba, S. E. Robinson et al., “Optimising experimental design for MEG beamformer imaging,” NeuroImage, vol. 39, no. 4, pp. 1788–1802, 2008. View at Publisher · View at Google Scholar · View at Scopus
  43. B. Masimore, J. Kakalios, and A. D. Redish, “Measuring fundamental frequencies in local field potentials,” Journal of Neuroscience Methods, vol. 138, no. 1-2, pp. 97–105, 2004. View at Publisher · View at Google Scholar · View at Scopus
  44. A. Bruns, R. Eckhorn, H. Jokeit, and A. Ebner, “Amplitude envelope correlation detects coupling among incoherent brain signals,” NeuroReport, vol. 11, no. 7, pp. 1509–1514, 2000. View at Publisher · View at Google Scholar · View at Scopus
  45. W. D. Penny, E. Duzel, K. J. Miller, and J. G. Ojemann, “Testing for nested oscillation,” Journal of Neuroscience Methods, vol. 174, no. 1, pp. 50–61, 2008. View at Publisher · View at Google Scholar · View at Scopus
  46. G. S. Maddala and K. Lahiri, Introduction to Econometrics, Wiley, Chichester, UK, 2009.
  47. E. S. Edgington and P. Onghena, Randomization Tests, Chapman & Hall/CRC Press, Boca Raton, Fla, USA, 2007.
  48. S. E. Maxwell and H. D. Delaney, Designing Experiments and Analyzing Data: A Model Comparison Perspective, Lawrence Erlbaum Associates, Mahwah, NJ, USA, 2004.
  49. R Core Team, R: A Language and Environment for Statistical Computing, R Foundation for Statistical Computing, Vienna, Austria, 2015, http://www.R-project.org/.
  50. A. Canty and B. Ripley, boot: Bootstrap R (S-Plus) Functions, R package version 1.3-16, 2015.
  51. A. C. Davison and D. V. Hinkley, Bootstrap Methods and Their Applications, Cambridge University Press, Cambridge, UK, 1997.
  52. R. Schaette and D. McAlpine, “Tinnitus with a normal audiogram: physiological evidence for hidden hearing loss and computational model,” Journal of Neuroscience, vol. 31, no. 38, pp. 13452–13457, 2011. View at Publisher · View at Google Scholar · View at Scopus
  53. J.-M. Schoffelen and J. Gross, “Source connectivity analysis with MEG and EEG,” Human Brain Mapping, vol. 30, no. 6, pp. 1857–1865, 2009. View at Publisher · View at Google Scholar · View at Scopus
  54. W. Schlee, N. Weisz, O. Bertrand, T. Hartmann, and T. Elbert, “Using auditory steady state responses to outline the functional connectivity in the tinnitus brain,” PLoS ONE, vol. 3, no. 11, Article ID e3720, 2008. View at Publisher · View at Google Scholar · View at Scopus
  55. W. Schlee, N. Mueller, T. Hartmann, J. Keil, I. Lorenz, and N. Weisz, “Mapping cortical hubs in tinnitus,” BMC Biology, vol. 7, article 80, 2009. View at Publisher · View at Google Scholar · View at Scopus
  56. A. N. Silchenko, I. Adamchic, C. Hauptmann, and P. A. Tass, “Impact of acoustic coordinated reset neuromodulation on effective connectivity in a neural network of phantom sound,” NeuroImage, vol. 77, pp. 133–147, 2013. View at Publisher · View at Google Scholar · View at Scopus
  57. R. T. Canolty and R. T. Knight, “The functional role of cross-frequency coupling,” Trends in Cognitive Sciences, vol. 14, no. 11, pp. 506–515, 2010. View at Publisher · View at Google Scholar · View at Scopus
  58. M. A. Belluscio, K. Mizuseki, R. Schmidt, R. Kempter, and G. Buzsáki, “Cross-frequency phase-phase coupling between theta and gamma oscillations in the hippocampus,” The Journal of Neuroscience, vol. 32, no. 2, pp. 423–435, 2012. View at Publisher · View at Google Scholar · View at Scopus
  59. W. Schlee, I. Lorenz, T. Hartmann, N. Müller, H. Schulz, and N. Weisz, “A global brain model of tinnitus,” in Textbook of Tinnitus, A. R. Møller, B. Langguth, D. De Ridder, and T. Kleinjung, Eds., pp. 161–169, Springer, New York, NY, USA, 2011. View at Publisher · View at Google Scholar
  60. D. De Ridder, A. B. Elgoyhen, R. Romo, and B. Langguth, “Phantom percepts: tinnitus and pain as persisting aversive memory networks,” Proceedings of the National Academy of Sciences of the United States of America, vol. 108, no. 20, pp. 8075–8080, 2011. View at Publisher · View at Google Scholar · View at Scopus
  61. M. J. Anderson and J. Robinson, “Permutation tests for linear models,” Australian & New Zealand Journal of Statistics, vol. 43, no. 1, pp. 75–88, 2001. View at Publisher · View at Google Scholar · View at Scopus
  62. D. Freedman and D. Lane, “A nonstochastic interpretation of reported significance levels,” Journal of Business & Economic Statistics, vol. 1, no. 4, pp. 292–298, 1983. View at Publisher · View at Google Scholar