[en] The underlying functional neuroanatomy of tinnitus remains poorly understood. Few studies have focused on functional cerebral connectivity changes in tinnitus patients. The aim of this study was to test if functional MRI "resting-state" connectivity patterns in auditory network differ between tinnitus patients and normal controls. Thirteen chronic tinnitus subjects and fifteen age-matched healthy controls were studied on a 3 tesla MRI. Connectivity was investigated using independent component analysis and an automated component selection approach taking into account the spatial and temporal properties of each component. Connectivity in extra-auditory regions such as brainstem, basal ganglia/NAc, cerebellum, parahippocampal, right prefrontal, parietal, and sensorimotor areas was found to be increased in tinnitus subjects. The right primary auditory cortex, left prefrontal, left fusiform gyrus, and bilateral occipital regions showed a decreased connectivity in tinnitus. These results show that there is a modification of cortical and subcortical functional connectivity in tinnitus encompassing attentional, mnemonic, and emotional networks. Our data corroborate the hypothesized implication of non-auditory regions in tinnitus physiopathology and suggest that various regions of the brain seem involved in the persistent awareness of the phenomenon as well as in the development of the associated distress leading to disabling chronic tinnitus.
Lefèbvre, Philippe ; Université de Liège - ULiège > Département des sciences cliniques > Oto-rhino-laryngologie et audiophonologie
CABAY, Jean-Evrard ; Centre Hospitalier Universitaire de Liège - CHU > Département de Physique Médicale > Service médical de médecine nucléaire et imagerie onco
Demertzi, Athina ; Université de Liège > Centre de recherches du cyclotron
Moller, (2011) Textbook of Tinnitus New York Springer.
Eggermont JJ, Roberts LE, (2004) The neuroscience of tinnitus. Trends Neurosci 27: 676-682.
Adjamian P, Sereda M, Hall DA, (2009) The mechanisms of tinnitus: perspectives from human functional neuroimaging. Hear Res 253: 15-31.
Barrs D, Brackmann D, (1984) Translabyrinthine nerve section: effect on tinnitus. The Journal of Laryngology & Otology (Supplement) pp. 287-293.
House JW, Brackmann DE, (1981) Tinnitus: surgical treatment. Ciba Found Symp 85: 204-216.
Schlee W, Mueller N, Hartmann T, Keil J, Lorenz I, et al. (2009) Mapping cortical hubs in tinnitus. BMC Biol 7: 80.
Schlee W, Weisz N, Bertrand O, Hartmann T, Elbert T, (2008) Using auditory steady state responses to outline the functional connectivity in the tinnitus brain. PLoS One 3: e3720.
Vanneste S, van de Heyning P, De Ridder D, (2011) The neural network of phantom sound changes over time: a comparison between recent-onset and chronic tinnitus patients. Eur J Neurosci 34: 718-731.
Vanneste S, Focquaert F, Van de Heyning P, De Ridder D, (2011) Different resting state brain activity and functional connectivity in patients who respond and not respond to bifrontal tDCS for tinnitus suppression. Exp Brain Res 210: 217-227.
Biswal B, Yetkin FZ, Haughton VM, Hyde JS, (1995) Functional connectivity in the motor cortex of resting human brain using echo-planar MRI. Magn Reson Med 34: 537-541.
Damoiseaux JS, Rombouts SA, Barkhof F, Scheltens P, Stam CJ, et al. (2006) Consistent resting-state networks across healthy subjects. Proc Natl Acad Sci U S A 103: 13848-13853.
De Luca M, Beckmann CF, De Stefano N, Matthews PM, Smith SM, (2006) fMRI resting state networks define distinct modes of long-distance interactions in the human brain. Neuroimage 29: 1359-1367.
Beckmann CF, DeLuca M, Devlin JT, Smith SM, (2005) Investigations into resting-state connectivity using independent component analysis. Philos Trans R Soc Lond B Biol Sci 360: 1001-1013.
van den Heuvel M, Mandl R, Hulshoff Pol H, (2008) Normalized cut group clustering of resting-state FMRI data. PLoS One 3: e2001.
Laird AR, Fox PM, Eickhoff SB, Turner JA, Ray KL, et al. (2011) Behavioral interpretations of intrinsic connectivity networks. J Cogn Neurosci 23: 4022-4037.
Demertzi A, Soddu A, Faymonville ME, Bahri MA, Gosseries O, et al. (2011) Hypnotic modulation of resting state fMRI default mode and extrinsic network connectivity. Prog Brain Res 193: 309-322.
Boveroux P, Vanhaudenhuyse A, Bruno MA, Noirhomme Q, Lauwick S, et al. (2010) Breakdown of within- and between-network resting state functional magnetic resonance imaging connectivity during propofol-induced loss of consciousness. Anesthesiology 113: 1038-1053.
Zhou J, Greicius MD, Gennatas ED, Growdon ME, Jang JY, et al. (2010) Divergent network connectivity changes in behavioural variant frontotemporal dementia and Alzheimer's disease. Brain 133: 1352-1367.
Greicius MD, Srivastava G, Reiss AL, Menon V, (2004) Default-mode network activity distinguishes Alzheimer's disease from healthy aging: evidence from functional MRI. Proc Natl Acad Sci U S A 101: 4637-4642.
Greicius MD, Flores BH, Menon V, Glover GH, Solvason HB, et al. (2007) Resting-state functional connectivity in major depression: abnormally increased contributions from subgenual cingulate cortex and thalamus. Biol Psychiatry 62: 429-437.
Vanhaudenhuyse A, Noirhomme Q, Tshibanda LJ, Bruno MA, Boveroux P, et al. (2010) Default network connectivity reflects the level of consciousness in non-communicative brain-damaged patients. Brain 133: 161-171.
Boly M, Tshibanda L, Vanhaudenhuyse A, Noirhomme Q, Schnakers C, et al. (2009) Functional connectivity in the default network during resting state is preserved in a vegetative but not in a brain dead patient. Hum Brain Mapp 30: 2393-2400.
Hunter MD, Eickhoff SB, Miller TW, Farrow TF, Wilkinson ID, et al. (2006) Neural activity in speech-sensitive auditory cortex during silence. Proc Natl Acad Sci U S A 103: 189-194.
Newman CW, Jacobson GP, Spitzer JB, (1996) Development of the Tinnitus Handicap Inventory. Arch Otolaryngol Head Neck Surg 122: 143-148.
Hallam RS, (1996) Manual of the Tinnitus Questionnaire (TQ) London Psychological Corporation.
Soddu A, Vanhaudenhuyse A, Bahri MA, Bruno MA, Boly M, et al. (2011) Identifying the default-mode component in spatial IC analyses of patients with disorders of consciousness. Hum Brain Mapp 33 (4): 778-796.
Esposito F, Scarabino T, Hyvarinen A, Himberg J, Formisano E, et al. (2005) Independent component analysis of fMRI group studies by self-organizing clustering. Neuroimage 25: 193-205.
De Martino F, Gentile F, Esposito F, Balsi M, Di Salle F, et al. (2007) Classification of fMRI independent components using IC-fingerprints and support vector machine classifiers. Neuroimage 34: 177-194.
Goebel R, Esposito F, Formisano E, (2006) Analysis of functional image analysis contest (FIAC) data with brainvoyager QX: From single-subject to cortically aligned group general linear model analysis and self-organizing group independent component analysis. Hum Brain Mapp 27: 392-401.
Forman SD, Cohen JD, Fitzgerald M, Eddy WF, Mintun MA, et al. (1995) Improved assessment of significant activation in functional magnetic resonance imaging (fMRI): use of a cluster-size threshold. Magn Reson Med 33: 636-647.
WHO (1991) Grades of hearing impairment. Hearing Network News 1.
Jastreboff PJ, (1990) Phantom auditory perception (tinnitus): mechanisms of generation and perception. Neurosci Res 8: 221-254.
Jastreboff PJ, Hazell JW, (1993) A neurophysiological approach to tinnitus: clinical implications. Br J Audiol 27: 7-17.
Rauschecker JP, Leaver AM, Muhlau M, (2010) Tuning out the noise: limbic-auditory interactions in tinnitus. Neuron 66: 819-826.
De Ridder D, Elgoyhen AB, Romo R, Langguth B, (2011) Phantom percepts: tinnitus and pain as persisting aversive memory networks. Proc Natl Acad Sci U S A 108: 8075-8080.
Smith SM, Fox PT, Miller KL, Glahn DC, Fox PM, et al. (2009) Correspondence of the brain's functional architecture during activation and rest. Proc Natl Acad Sci U S A 106: 13040-13045.
Weisz N, Muller S, Schlee W, Dohrmann K, Hartmann T, et al. (2007) The neural code of auditory phantom perception. J Neurosci 27: 1479-1484.
van der Loo E, Gais S, Congedo M, Vanneste S, Plazier M, et al. (2009) Tinnitus intensity dependent gamma oscillations of the contralateral auditory cortex. PLoS One 4: e7396.
Mirz F, Pedersen B, Ishizu K, Johannsen P, Ovesen T, et al. (1999) Positron emission tomography of cortical centers of tinnitus. Hear Res 134: 133-144.
Lockwood AH, Salvi RJ, Coad ML, Towsley ML, Wack DS, et al. (1998) The functional neuroanatomy of tinnitus: evidence for limbic system links and neural plasticity. Neurology 50: 114-120.
Smits M, Kovacs S, de Ridder D, Peeters RR, van Hecke P, et al. (2007) Lateralization of functional magnetic resonance imaging (fMRI) activation in the auditory pathway of patients with lateralized tinnitus. Neuroradiology 49: 669-679.
Reyes SA, Salvi RJ, Burkard RF, Coad ML, Wack DS, et al. (2002) Brain imaging of the effects of lidocaine on tinnitus. Hear Res 171: 43-50.
Engelien A, Stern E, Isenberg N, Engelien W, Frith C, et al. (2000) The parahippocampal region and auditory-mnemonic processing. Ann N Y Acad Sci 911: 477-485.
De Ridder D, Fransen H, Francois O, Sunaert S, Kovacs S, et al. (2006) Amygdalohippocampal involvement in tinnitus and auditory memory. Acta Otolaryngol Suppl pp. 50-53.
Leaver AM, Renier L, Chevillet MA, Morgan S, Kim HJ, et al. (2011) Dysregulation of limbic and auditory networks in tinnitus. Neuron 69: 33-43.
Larson PS, Cheung SW, (2011) Deep brain stimulation in area LC controllably triggers auditory phantom percepts. Neurosurgery 70 (2): 398-405.
Weisz N, Moratti S, Meinzer M, Dohrmann K, Elbert T, (2005) Tinnitus perception and distress is related to abnormal spontaneous brain activity as measured by magnetoencephalography. PLoS Med 2: e153.
Kleinjung T, Eichhammer P, Landgrebe M, Sand P, Hajak G, et al. (2008) Combined temporal and prefrontal transcranial magnetic stimulation for tinnitus treatment: a pilot study. Otolaryngol Head Neck Surg 138: 497-501.
Knight RT, Grabowecky MF, Scabini D, (1995) Role of human prefrontal cortex in attention control. Adv Neurol 66: 21-34; discussion 34-26.
Beard AW, (1965) Results of leucotomy operations for tinnitus. J Psychosom Res 9: 29-32.
Murphy JP, (1951) Frontal lobe surgery in treatment of intractable pain; a critique. Yale J Biol Med 23: 493-500.
Watts JW, Freeman W, (1946) Psychosurgery for the relief of unbearable pain. J Int Coll Surg 9: 679-683.
Petacchi A, Laird AR, Fox PT, Bower JM, (2005) Cerebellum and auditory function: an ALE meta-analysis of functional neuroimaging studies. Hum Brain Mapp 25: 118-128.
Osaki Y, Nishimura H, Takasawa M, Imaizumi M, Kawashima T, et al. (2005) Neural mechanism of residual inhibition of tinnitus in cochlear implant users. Neuroreport 16: 1625-1628.
Lockwood AH, Wack DS, Burkard RF, Coad ML, Reyes SA, et al. (2001) The functional anatomy of gaze-evoked tinnitus and sustained lateral gaze. Neurology 56: 472-480.
Cacace AT, (2003) Expanding the biological basis of tinnitus: crossmodal origins and the role of neuroplasticity. Hear Res 175: 112-132.