Healthy‐side dominance of middle‐ and long‐latency neuromagnetic fields in idiopathic sudden sensorineural hearing loss

Any lesion along the neural axis may induce a subsequent functional reorganization at the level above. The present study used magnetoencephalography to investigate auditory‐evoked magnetic fields [a component of the middle‐latency auditory evoked fields peaking at ~50 ms (P50m) and a component of the long‐latency auditory evoked fields peaking at ~100 ms (N100m)] on stimulation of both healthy and affected ears in patients with acute unilateral idiopathic sudden sensorineural hearing loss (ISSNHL) of moderate degree in order to elucidate the functional plasticity of the auditory system. Sixteen right‐handed, previously untreated adult patients with acute unilateral left (n = 8) or right (n = 8) ISSNHL of moderate degree were studied. Sixteen right‐handed healthy volunteers with normal hearing served as control. Auditory neuromagnetic responses, measured by a whole‐head 306‐channel neuromagnetometer, were detected by monaural tone stimulation applied to affected and healthy ears, respectively, in different sessions. Intragroup and intergroup interhemispheric differences of peak dipole strengths and latencies of P50m and N100m, respectively, to monaural tones were evaluated. Healthy‐side amplitude dominance of both P50m and N100m was found in ISSNHL, i.e. contralateral dominance was preserved on affected‐ear stimulation but ipsilateral dominance was seen on healthy‐ear stimulation. The phenomena could be attributed to the combined contralateral attenuation and ipsilateral enhancement of P50m and N100m activity in response to healthy‐ear stimulation. Our findings confirmed that functional modulation can occur within the first few tens of milliseconds of evoked response at the auditory cortex in ISSNHL. The mechanisms of healthy‐side dominance might be ascribed to a functional retune of auditory pathways, i.e. conjoined contralateral inhibition and ipsilateral excitation of the auditory pathway in response to healthy‐ear stimulation. The effect could be registered in cortical responses.

[1]  J. Mäkelä,et al.  Whole-head mapping of middle-latency auditory evoked magnetic fields. , 1994, Electroencephalography and clinical neurophysiology.

[2]  Jen-Chuen Hsieh,et al.  Loss of interhemispheric inhibition on the ipsilateral primary sensorimotor cortex in patients with brachial plexus injury: fMRI study , 2002, Annals of neurology.

[3]  J. Hsieh,et al.  Healthy‐side dominance of cortical neuromagnetic responses in sudden hearing loss , 2003, Annals of neurology.

[4]  N. Fujiki,et al.  Enhanced activation of the auditory cortex in patients with inner-ear hearing impairment: a magnetoencephalographic study , 2003, Clinical Neurophysiology.

[5]  Diane Kurtzberg,et al.  Effects of Sensorineural Hearing Loss on Cortical Event-Related Potential and Behavioral Measures of Speech-Sound Processing , 2002, Ear and hearing.

[6]  T. Yoshimoto,et al.  Middle and long latency peak sources in auditory evoked magnetic fields for tone bursts in humans , 2000, Neuroscience Letters.

[7]  Paul K Foster,et al.  A model for perilymphatic fistula induced hearing loss in the guinea pig cochlea , 2002, Hearing Research.

[8]  Dan H Sanes,et al.  The effect of bilateral deafness on excitatory and inhibitory synaptic strength in the inferior colliculus , 2002, The European journal of neuroscience.

[9]  K Mathiak,et al.  Contralaterality of cortical auditory processing at the level of the M50/M100 complex and the mismatch field: A whole-head magnetoencephalography study , 2001, Neuroreport.

[10]  Cortical representation of hearing restoration in patients with sudden deafness , 2002, Neuroreport.

[11]  N. Fujiki,et al.  Influence of unilateral deafness on auditory evoked magnetic field , 1998, Neuroreport.

[12]  Auditory middle-latency responses in patients with localized and non-localized lesions of the central nervous system , 1991, Journal of Neurology.

[13]  J. Fell,et al.  Lateralized auditory spatial perception and the contralaterality of cortical processing as studied with functional magnetic resonance imaging and magnetoencephalography , 1999, Human brain mapping.

[14]  N. Suga,et al.  Modulation of cochlear hair cells by the auditory cortex in the mustached bat , 2002, Nature Neuroscience.

[15]  D. Moore,et al.  Down-regulation of inhibition following unilateral deafening , 2000, Hearing Research.

[16]  G. Jacobson,et al.  Magnetoencephalographic Studies of Auditory System Function , 1994, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[17]  C. G. Benson,et al.  Altered glycinergic synaptic activities in guinea pig brain stem auditory nuclei after unilateral cochlear ablation , 2000, Hearing Research.

[18]  W. Trojaborg,et al.  Long-term neurotoxicity in patients treated with cisplatin, vinblastine, and bleomycin for metastatic germ cell cancer. , 1989, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[19]  R. Altschuler,et al.  Diversity and plasticity in amino acid receptor subunits in the rat auditory brain stem , 2000, Hearing Research.

[20]  E. Pekkonen,et al.  Magnetoencephalographic evidence of abnormal auditory processing in amyotrophic lateral sclerosis with bulbar signs , 2004, Clinical Neurophysiology.

[21]  R. Levine,et al.  Auditory dysfunction in stroke. , 2000, Acta oto-laryngologica.

[22]  J. Loeb,et al.  Asymmetric flaccid paralysis: A neuromuscular presentation of West Nile virus infection , 2003, Annals of neurology.

[23]  D R Moore,et al.  Anatomy and physiology of binaural hearing. , 1991, Audiology : official organ of the International Society of Audiology.

[24]  C. Fischer,et al.  Asymmetrical localization of benzodiazepine receptors in the human auditory cortex. , 2001, Acta oto-laryngologica.

[25]  N. Kraus,et al.  Auditory brain stem and middle latency responses in a patient with cortical deafness. , 1982, Electroencephalography and clinical neurophysiology.

[26]  R. Illing,et al.  Acoustic trauma induces reemergence of the growth‐ and plasticity‐associated protein GAP‐43 in the rat auditory brainstem , 2002, The Journal of comparative neurology.

[27]  M. Torrens.  Co-Planar Stereotaxic Atlas of the Human Brain—3-Dimensional Proportional System: An Approach to Cerebral Imaging, J. Talairach, P. Tournoux. Georg Thieme Verlag, New York (1988), 122 pp., 130 figs. DM 268 , 1990 .

[28]  R J Salvi,et al.  Plasticity of response properties of inferior colliculus neurons following acute cochlear damage. , 1996, Journal of neurophysiology.

[29]  D. Born,et al.  Afferent influences on brain stem auditory nuclei of the chicken: Neuron number and size following cochlea removal , 1985, The Journal of comparative neurology.

[30]  F. Byl,et al.  The efficacy of steroids in the treatment of idiopathic sudden hearing loss. A double-blind clinical study. , 1980, Archives of otolaryngology.

[31]  D. Durham,et al.  Central nervous system plasticity during hair cell loss and regeneration , 2000, Hearing Research.

[32]  H. Ramsay,et al.  Modification of auditory pathway functions in patients with hearing improvement after middle ear surgery , 1998, Otolaryngology--head and neck surgery : official journal of American Academy of Otolaryngology-Head and Neck Surgery.

[33]  S. Khalfa,et al.  Evidence of peripheral auditory activity modulation by the auditory cortex in humans , 2001, Neuroscience.

[34]  A. Quaranta,et al.  ABR in multiple sclerosis. Ipsi- versus contralateral derivation. , 1986, Scandinavian audiology.

[35]  P. Teale,et al.  Auditory evoked magnetic fields in adults with fragile X syndrome , 2001, Neuroreport.

[36]  J. Mäkelä,et al.  Auditory pathway plasticity in adult humans after unilateral idiopathic sudden sensorineural hearing loss , 1995, Hearing Research.

[37]  N. Suga,et al.  Corticofugal amplification of facilitative auditory responses of subcortical combination-sensitive neurons in the mustached bat. , 1999, Journal of neurophysiology.

[38]  Jian Wang,et al.  Auditory plasticity and hyperactivity following cochlear damage , 2000, Hearing Research.

[39]  J. Gross,et al.  Fibroblast growth factors (FGFs) in the cochlear nucleus of the adult mouse following acoustic overstimulation , 2002, Hearing Research.

[40]  Nobuo Suga,et al.  Plasticity and Corticofugal Modulation for Hearing in Adult Animals , 2002, Neuron.

[41]  W. Gstoettner,et al.  Specificity of auditory brainstem response audiometry criteria in acoustic neuroma screening as a function of deviations of reference values in patients with cochlear hearing loss , 2004, European Archives of Oto-Rhino-Laryngology.

[42]  Risto Näätänen,et al.  Age‐related functional differences between auditory cortices: a whole- head MEG study , 1995, Neuroreport.

[43]  F. Byl.  Sudden hearing loss: Eight years' experience and suggested prognostic table , 1984, The Laryngoscope.

[44]  T. Onitsuka,et al.  The effect of interstimulus intervals and between-block rests on the auditory evoked potential and magnetic field: is the auditory P50 in humans an overlapping potential? , 2000, Clinical Neurophysiology.

[45]  J. Mäkelä,et al.  Modification of neuromagnetic responses of the human auditory cortex by masking sounds , 2004, Experimental Brain Research.

[46]  C. Pantev,et al.  Cortical reorganization in patients with high frequency cochlear hearing loss , 2001, Hearing Research.