Abnormal cortical sensorimotor activity during "Target" sound detection in subjects with acute acoustic trauma sequelae: an fMRI study

Agnès Job, Yoann Pons, Laurent Lamalle, Assia Jaillard, Karl Buck, Christoph Segebarth, Chantal Delon-Martin, Agnès Job, Yoann Pons, Laurent Lamalle, Assia Jaillard, Karl Buck, Christoph Segebarth, Chantal Delon-Martin

Abstract

The most common consequences of acute acoustic trauma (AAT) are hearing loss at frequencies above 3 kHz and tinnitus. In this study, we have used functional Magnetic Resonance Imaging (fMRI) to visualize neuronal activation patterns in military adults with AAT and various tinnitus sequelae during an auditory "oddball" attention task. AAT subjects displayed overactivities principally during reflex of target sound detection, in sensorimotor areas and in emotion-related areas such as the insula, anterior cingulate and prefrontal cortex, in premotor area, in cross-modal sensory associative areas, and, interestingly, in a region of the Rolandic operculum that has recently been shown to be involved in tympanic movements due to air pressure. We propose further investigations of this brain area and fine middle ear investigations, because our results might suggest a model in which AAT tinnitus may arise as a proprioceptive illusion caused by abnormal excitability of middle-ear muscle spindles possibly link with the acoustic reflex and associated with emotional and sensorimotor disturbances.

Keywords: Acoustic trauma; Middle ear; Proprioception; Tinnitus; fMRI.

Figures

Figure 1
Figure 1
Hearing levels of participants: right and left audiograms (Békésy method) in the AAT group (occasional and frequent/permanent tinnitus) and control group. Hearing loss is observed at high frequency in the AAT group.
Figure 2
Figure 2
Behavioral auditory task results in the AAT group and in control group. Task was performed in the audiolab and in the MR scanner. Intrasubject reaction-time variability and error rate were significantly higher in the AAT group.
Figure 3
Figure 3
Overall view of the differences of contrast between the AAT group (N = 19) and the control group (N = 19); AAT > controls, in the “target sounds vs. baseline” contrast using an auditory oddball task. Significance assessed at P < 0.001, uncorrected and extent > 20 voxels. Activations are superimposed on the mean anatomical image from the control group. Left hemisphere is left on the image.
Figure 4
Figure 4
fMRI image and graph of mean voxel intensities at MNI coordinates 42, −18, 18 (BA 43/40) of the significant difference between AAT subjects and Control subjects for the contrast “Target vs. Baseline.” Mean voxel intensities were presented according to tinnitus periodicity and handicap. Occasional tinnitus = T+; Frequent/Permanent tinnitus = T++; Low TRQ scores = H−; High TRQ scores = H+. There is a significant correlation between voxel intensities and the combination of tinnitus periodicity and the subjective distress/handicap (TRQ) (Spearman's rho: r = 0.66, P < 0.001).
Figure 5
Figure 5
Hyperactivation in the Rolandic operculum (BA 43/40) in the AAT group during auditory oddball task (red voxels) for the contrast “Target sound vs. baseline” with superimposition of cortical activations in BA 43 found in Job et al. (2011) study for the contrast “tympanic movement due to air pressure variations vs. no pressure variations” in normal hearing subjects (green voxels).

References

    1. Al-Ani Z, Gray R. TMD current concepts: 1. An update. Dent. Update. 2007;34:278–280. 282–274, 287–278.
    1. Allin EF. Evolution of the mammalian middle ear. J. Morphol. 1975;147:403–437.
    1. Andersson JL, Hutton C, Ashburner J, Turner R, Friston K. Modeling geometric deformations in EPI time series. Neuroimage. 2001;13:903–919.
    1. Andersson G, Kaldo-Sandstrom V, Strom L, Stromgren T. Internet administration of the hospital anxiety and depression scale in a sample of tinnitus patients. J. Psychosom. Res. 2003;55:259–262.
    1. Axelsson A, Ringdahl A. Tinnitus–a study of its prevalence and characteristics. Br. J. Audiol. 1989;23:53–62.
    1. Baykushev S, Struppler A, Gozmanov G, Mavrov R. Motor threshold as indicator of premotor and motor cortex excitability. Electromyogr. Clin. Neurophysiol. 2008;48:259–264.
    1. Boecker H, Jankowski J, Ditter P, Scheef L. A role of the basal ganglia and midbrain nuclei for initiation of motor sequences. Neuroimage. 2008;39:1356–1369.
    1. Calhoun VD, Stevens MC, Pearlson GD, Kiehl KA. fMRI analysis with the general linear model: removal of latency-induced amplitude bias by incorporation of hemodynamic derivative terms. Neuroimage. 2004;22:252–257.
    1. Calvin-Figuiere S, Romaiguere P, Gilhodes JC, Roll JP. Antagonist motor responses correlate with kinesthetic illusions induced by tendon vibration. Exp. Brain Res. 1999;124:342–350.
    1. Critchley HD, Wiens S, Rotshtein P, Ohman A, Dolan RJ. Neural systems supporting interoceptive awareness. Nat. Neurosci. 2004;7:189–195.
    1. Cuny C, Norena A, El Massioui F, Chery-Croze S. Reduced attention shift in response to auditory changes in subjects with tinnitus. Audiol. Neurootol. 2004;9:294–302.
    1. Cusack R, Papadakis N. New robust 3-D phase unwrapping algorithms: application to magnetic field mapping and undistorting echoplanar images. Neuroimage. 2002;16:754–764.
    1. De Ridder D, De Mulder G, Menovsky T, Sunaert S, Kovacs S. Electrical stimulation of auditory and somatosensory cortices for treatment of tinnitus and pain. Prog. Brain Res. 2007;166:377–388.
    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;108:8075–8080.
    1. Dietrich V, Nieschalk M, Stoll W, Rajan R, Pantev C. Cortical reorganization in patients with high frequency cochlear hearing loss. Hear. Res. 2001;158:95–101.
    1. Eggermont JJ. Central tinnitus. Auris Nasus Larynx. 2003;30(Suppl):S7–S12.
    1. Eggermont JJ. Cortical tonotopic map reorganization and its implications for treatment of tinnitus. Acta Otolaryngol. 2006;556(Suppl):9–12.
    1. Engineer ND, Riley JR, Seale JD, Vrana WA, Shetake JA, Sudanagunta SP, Borland MS, Kilgard MP. Reversing pathological neural activity using targeted plasticity. Nature. 2011;470:101–104.
    1. Folmer RL, Griest SE, Martin WH. Chronic tinnitus as phantom auditory pain. Otolaryngol. Head Neck Surg. 2001;124:394–400.
    1. Goodwin GM, McCloskey DI, Matthews PB. Proprioceptive illusions induced by muscle vibration: contribution by muscle spindles to perception? Science. 1972;175:1382–1384.
    1. Hallam RS, McKenna L, Shurlock L. Tinnitus impairs cognitive efficiency. Int J Audiol. 2004;43:218–226.
    1. Haslinger B, Altenmüller E, Castrop F, Zimmer C, Dresel C. Sensorimotor overactivity as a pathophysiologic trait of embouchure dystonia. Neurology. 2010;74:1790–1797.
    1. Heller AJ. Classification and epidemiology of tinnitus. Otolaryngol. Clin. North Am. 2003;36:239–248.
    1. Hoehn-Saric R, McLeod DR. The peripheral sympathetic nervous system. Its role in normal and pathologic anxiety. Psychiatr. Clin. North Am. 1988;11:375–386.
    1. Hutton C, Bork A, Josephs O, Deichmann R, Ashburner J, Turner R. Image distortion correction in fMRI: a quantitative evaluation. Neuroimage. 2002;16:217–240.
    1. Jacobson GP, Calder JA, Newman CW, Peterson EL, Wharton JA, Ahmad BK. Electrophysiological indices of selective auditory attention in subjects with and without tinnitus. Hear. Res. 1996;97:66–74.
    1. Jastreboff PJ. Phantom auditory perception (tinnitus): mechanisms of generation and perception. Neurosci. Res. 1990;8:221–254.
    1. Jastreboff PJ. Tinnitus retraining therapy. Prog. Brain Res. 2007;166:415–423.
    1. Jastreboff PJ, Hazell JWP. Tinnitus retraining therapy. Cambridge: Cambridge Univ. Press; 2004. p. 276.
    1. Jastreboff PJ, Gray WC, Gold SL. Neurophysiological approach to tinnitus patients. Am. J. Otol. 1996;17:236–240.
    1. Job A, Cian C, Esquivie D, Leifflen D, Trousselard M, Charles C, Nottet J-B. Moderate variations of mood/emotional states related to alterations in cochlear otoacoustic emissions and tinnitus onset in young normal hearing subjects exposed to gun impulse noise. Hear. Res. 2004;193:31–38.
    1. Job A, Raynal M, Kossowski M. Susceptibility to tinnitus revealed at 2 kHz range by bilateral lower DPOAEs in normal hearing subjects with noise exposure. Audiol. Neurootol. 2007;12:137–144.
    1. Job A, Paucod J-C, O’Beirne GA, Delon-Martin C. Cortical repesentation of tympanic membrane movements due to pressure variation: a fMRI study. Hum. Brain Mapp. 2011;32:744–749.
    1. Kaltenbach JA. Neurophysiologic mechanisms of tinnitus. J. Am. Acad. Audiol. 2000;11:125–137.
    1. Kierner AC, Zelenka I, Lukas JR, Aigner M, Mayr R. Observations on the number, distribution and morphological peculiarities of muscle spindles in the tensor tympani and stapedius muscle of man. Hear. Res. 1999;135:71–77.
    1. Knobel KA, Sanchez TG. Influence of silence and attention on tinnitus perception. Otolaryngol. Head Neck Surg. 2008;138:18–22.
    1. Knobel KA, Sanchez TG. Selective auditory attention and silence elicit auditory hallucination in a nonclinical sample. Cogn. Neuropsychiatry. 2009;14:1–10.
    1. Kovacs S, Peeters R, Smits M, De Ridder D, Van Hecke P, Sunaert S. Activation of cortical and subcortical auditory structures at 3 T by means of a functional magnetic resonance imaging paradigm suitable for clinical use. Invest. Radiol. 2006;41:87–96.
    1. Krubitzer L, Huffman KJ, Disbrow E, Recanzone G. Organization of area 3a in macaque monkeys: contributions to the cortical phenotype. J. Comp. Neurol. 2004;471:97–111.
    1. Laplane D, Talairach J, Meininger V, Bancaud J, Bouchareine A. Motor consequences of motor area ablations in man. J. Neurol. Sci. 1977;31:29–49.
    1. Leaver AM, Renier L, Chevillet MA, Morgan S, Kim HJ, Rauschecker JP. Dysregulation of limbic and auditory networks in tinnitus. Neuron. 2011;69:33–43.
    1. Levine RA. Somatic (craniocervical) tinnitus and the dorsal cochlear nucleus hypothesis. Am. J. Otolaryngol. 1999;20:351–362.
    1. Levine RA, Abel M, Cheng H. CNS somatosensory-auditory interactions elicit or modulate tinnitus. Exp. Brain Res. 2003;153:643–648.
    1. Levine RA, Nam EC, Oron Y, Melcher JR. Evidence for a tinnitus subgroup responsive to somatosensory based treatment modalities. Prog. Brain Res. 2007;166:195–207.
    1. Liberman MC, Dodds LW. Acute ultrastructural changes in acoustic trauma: serial-section reconstruction of stereocilia and cuticular plates. Hear. Res. 1987;26:45–64.
    1. Lockwood AH, Salvi RJ, Burkard RF. Tinnitus. N. Engl. J. Med. 2002;347:904–910.
    1. Meric C, Pham E, Chery-Croze S. Validation assessment of a French version of the tinnitus reaction questionnaire: a comparison between data from English and French versions. J. Speech Lang. Hear. Res. 2000;43:184–190.
    1. Moller AR. Similarities between chronic pain and tinnitus. Am. J. Otol. 1997;18:577–585.
    1. Moller AR. Pathophysiology of tinnitus. Otolaryngol. Clin. North Am. 2003;36:249–266. v-vi.
    1. Muhlnickel W, Elbert T, Taub E, Flor H. Reorganization of auditory cortex in tinnitus. Proc. Natl. Acad. Sci. U. S. A. 1998;95:10340–10343.
    1. Norena AJ, Eggermont JJ. Changes in spontaneous neural activity immediately after an acoustic trauma: implications for neural correlates of tinnitus. Hear. Res. 2003;183:137–153.
    1. Nottet JB, Moulin A, Brossard N, Suc B, Job A. Otoacoustic emissions and persistent tinnitus after acute acoustic trauma. Laryngoscope. 2006;116:970–975.
    1. Nozzoli C, Masi G, Ferrannini E, Simone F. Sympathetic activation and muscle spindle. Funct. Neurol. 1987;2:553–557.
    1. Paltoglou AE, Sumner CJ, Hall DA. Examining the role of frequency specificity in the enhancement and suppression of human cortical activity by auditory selective attention. Hear. Res. 2009;257:106–118.
    1. Rajan R, Irvine DR. Neuronal responses across cortical field A1 in plasticity induced by peripheral auditory organ damage. Audiol. Neurootol. 1998;3:123–144.
    1. Roberts LE, Eggermont JJ, Caspary DM, Shore SE, Melcher JR, Kaltenback JA. Ringing ears: the neuroscience of tinnitus. J. Neurosci. 2010;30:14972–14979.
    1. Roll JP, Vedel JP, Ribot E. Alteration of proprioceptive messages induced by tendon vibration in man: a microneurographic study. Exp. Brain Res. 1989;76:213–222.
    1. Romaiguere P, Anton JL, Roth M, Casini L, Roll JP. Motor and parietal cortical areas both underlie kinaesthesia. Brain Res. Cogn. Brain Res. 2003;16:74–82.
    1. Sanchez TG, Guerra GC, Lorenzi MC, Brandao AL, Bento RF. The influence of voluntary muscle contractions upon the onset and modulation of tinnitus. Audiol. Neurootol. 2002;7:370–375.
    1. Schlee W, Weisz N, Bertrand O, Hartmann T, Elbert T. Using auditory steady state responses to outline the functional connectivity in the tinnitus brain. PLoS One. 2008;3:e3720.
    1. Schwarz M, Sontag KH, Wand P. Non-dopaminergic neurones of the reticular part of substantia nigra can gate static fusimotor action onto flexors in cat. J. Physiol. 1984a;354:333–344.
    1. Schwarz M, Sontag KH, Wand P. Sensory-motor processing in substantia nigra pars reticulata in conscious cats. J. Physiol. 1984b;347:129–147.
    1. Seeley WW, Menon V, Schatzberg AF, Keller J, Glover GH. Dissociable intrinsic connectivity networks for salience processing and executive control. J. Neurosci. 2007;27:2349–2356.
    1. Shiomi Y, Tsuji J, Naito Y, Fujiki N, Yamamoto N. Characteristics of DPOAE audiogram in tinnitus patients. Hear. Res. 1997;108:83–88.
    1. Shore SE, Koehler S, Oldakowski M, Hughes LF, Syed S. Dorsal cochlear nucleus responses to somatosensory stimulation are enhanced after noise-induced hearing loss. Eur. J. Neurosci. 2008;27:155–168.
    1. Smits M, Kovacs S, de Ridder D, Peeters RR, van Hecke P. Lateralization of functional magnetic resonance imaging (fMRI) activation in the auditory pathway of patients with lateralized tinnitus. Neuroradiology. 2007;49:669–679.
    1. Tonndorf J. The analogy between tinnitus and pain: a suggestion for a physiological basis of chronic tinnitus. Hear. Res. 1987;28:271–275.
    1. Valsecchi M, Turatto M. Microsaccadic responses in a bimodal oddball task. Psychol. Res. 2009;73:23–33.
    1. Vanneste S, Plazier M, der Loo E, de Heyning PV, Congedo M, De Ridder D. The neural correlates of tinnitus-related distress. Neuroimage. 2010;52:470–480.
    1. Verret C, Matras-Maslin V, Haus-Cheymol R, Berger F, Texier G, Decam C, Poncet J, Spiegel A. 2005. p. 42. Traumatismes sonores aigus dans les armées. Résultats de la surveillance épidémiologique de 2002 à 2004. Département d’épidémiologie et de santé publique nord. Ecole du Val de Grâce.
    1. Verschueren SM, Swinnen SP, Cordo PJ, Dounskaia NV. Proprioceptive control of multijoint movement: unimanual circle drawing. Exp. Brain Res. 1999;127:171–181.
    1. Weisz N, Wienbruch C, Dohrmann K, Elbert T. Neuromagnetic indicators of auditory cortical reorganization of tinnitus. Brain. 2005;128:2722–2731.
    1. Wilson PH, Henry J, Bowen M, Haralambous G. Tinnitus reaction questionnaire: psychometric properties of a measure of distress associated with tinnitus. J. Speech Hear. Res. 1991;34:197–201.
    1. WMA. Seoul-Corea: WMA; 2008. Ethical principles for medical research involving human subjects: WMA 18th general assembly (1964), Helsinki, Finland (Declaration of Helsinki) In: editor. 6th revision.

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