Realignment of Interaural Cortical Maps in Asymmetric Hearing Loss

Misalignment of interaural cortical response maps in asymmetric hearing loss evolves from initial gross divergence to near convergence over a 6 month recovery period. The evolution of left primary auditory cortex (AI) interaural frequency map changes is chronicled in squirrel monkeys with asymmetric hearing loss induced by overstimulating the right ear with a 1 kHz tone at 136 dB for 3 h. AI frequency response areas (FRAs), derived from tone bursts presented to the poorer or better hearing ears, are compared at 6, 12, and 24 weeks after acoustic overstimulation. Characteristic frequency (CF) and minimum threshold parameters are extracted from FRAs, and they are used to quantify interaural response map differences. A large interaural CF map misalignment of ΔCF ∼1.27 octaves at 6 weeks after overstimulation decreases substantially to ΔCF ∼0.62 octave at 24 weeks. Interaural cortical threshold map misalignment faithfully reflects peripheral asymmetric hearing loss at 6 and 12 weeks. However, AI threshold map misalignment essentially disappears at 24 weeks, primarily because ipsilateral cortical thresholds have become unexpectedly elevated relative to peripheral thresholds. The findings document that plastic change in central processing of sound stimuli arriving from the nominally better hearing ear may account for progressive realignment of both interaural frequency and threshold maps.

[1]  T. Imig,et al.  Consequences of unilateral hearing loss: Cortical adjustment to unilateral deprivation , 2008, Hearing Research.

[2]  Donal G. Sinex,et al.  Acute spiral ganglion lesions change the tuning and tonotopic organization of cat inferior colliculus neurons , 2000, Hearing Research.

[3]  D. Irvine,et al.  PLASTICITY IN THE ADULT CENTRAL AUDITORY SYSTEM. , 2006, Acoustics Australia.

[4]  E I Knudsen,et al.  Dynamics of visually guided auditory plasticity in the optic tectum of the barn owl. , 1995, Journal of neurophysiology.

[5]  Jos J Eggermont,et al.  Neural changes in cat auditory cortex after a transient pure-tone trauma. , 2003, Journal of neurophysiology.

[6]  G. Plourde Auditory evoked potentials. , 2006, Best practice & research. Clinical anaesthesiology.

[7]  D. C. Teas,et al.  Single unit study of binaural interaction in the auditory cortex of the chinchilla , 1976, Brain Research.

[8]  S. Cheung Frequency Map Variations in Squirrel Monkey Primary Auditory Cortex , 2005, The Laryngoscope.

[9]  S. Green Auditory sensitivity and equal loudness in the squirrel monkey (Saimiri sciureus). , 1975, Journal of the experimental analysis of behavior.

[10]  J. Kaas,et al.  Neuroplasticity of the adult primate auditory cortex following cochlear hearing loss. , 1993, The American journal of otology.

[11]  Christoph E Schreiner,et al.  Plasticity in Primary Auditory Cortex of Monkeys with Altered Vocal Production , 2005, The Journal of Neuroscience.

[12]  W. Burke,et al.  Plasticity in adult cat visual cortex (area 17) following circumscribed monocular lesions of all retinal layers , 2000, The Journal of physiology.

[13]  Jos J Eggermont,et al.  Moderate noise trauma in juvenile cats results in profound cortical topographic map changes in adulthood , 2000, Hearing Research.

[14]  R. Felix,et al.  Excitatory, inhibitory and facilitatory frequency response areas in the inferior colliculus of hearing impaired mice , 2007, Hearing Research.

[15]  T. Imig,et al.  Binaural columns in the primary field (A1) of cat auditory cortex , 1977, Brain Research.

[16]  D. Irvine,et al.  Effect of unilateral partial cochlear lesions in adult cats on the representation of lesioned and unlesioned cochleas in primary auditory cortex , 1993, The Journal of comparative neurology.

[17]  Jos J. Eggermont,et al.  Changes in cat primary auditory cortex after minor-to-moderate pure-tone induced hearing loss , 2002, Hearing Research.

[18]  Donald Robertson,et al.  Plasticity of frequency organization in auditory cortex of guinea pigs with partial unilateral deafness , 1989, The Journal of comparative neurology.

[19]  Ramesh Rajan,et al.  Effects of restricted cochlear lesions in adult cats on the frequency organization of the inferior colliculus , 2003, The Journal of comparative neurology.

[20]  C E Schreiner,et al.  Functional organization of squirrel monkey primary auditory cortex: responses to pure tones. , 2001, Journal of neurophysiology.

[21]  Christoph E. Schreiner,et al.  Auditory Cortex Mapmaking: Principles, Projections, and Plasticity , 2007, Neuron.

[22]  Donal G Sinex,et al.  Immediate changes in tuning of inferior colliculus neurons following acute lesions of cat spiral ganglion. , 2002, Journal of neurophysiology.

[23]  R. Rajan,et al.  Plasticity of excitation and inhibition in the receptive field of primary auditory cortical neurons after limited receptor organ damage. , 2001, Cerebral cortex.

[24]  Peter L. Brooks,et al.  Visualizing data , 1997 .

[25]  A. King,et al.  Auditory Plasticity: Vocal Output Shapes Auditory Cortex , 2005, Current Biology.

[26]  R. Rajan,et al.  Receptor organ damage causes loss of cortical surround inhibition without topographic map plasticity , 1998, Nature Neuroscience.

[27]  Josef Syka,et al.  Plastic changes in the central auditory system after hearing loss, restoration of function, and during learning. , 2002, Physiological reviews.

[28]  J I Gold,et al.  Abnormal Auditory Experience Induces Frequency-Specific Adjustments in Unit Tuning for Binaural Localization Cues in the Optic Tectum of Juvenile Owls , 2000, The Journal of Neuroscience.

[29]  T. Kamada,et al.  Auditory evoked potentials in the Japanese monkey. , 1991, Journal of medical primatology.

[30]  Eric I. Knudsen,et al.  Adaptive auditory plasticity in developing and adult animals , 2007, Progress in Neurobiology.

[31]  M. Semple,et al.  Binaural processing of sound pressure level in cat primary auditory cortex: evidence for a representation based on absolute levels rather than interaural level differences. , 1993, Journal of neurophysiology.

[32]  K. Barsz,et al.  Reorganization of receptive fields following hearing loss in inferior colliculus neurons , 2007, Neuroscience.

[33]  J I Gold,et al.  Hearing impairment induces frequency-specific adjustments in auditory spatial tuning in the optic tectum of young owls. , 1999, Journal of neurophysiology.

[34]  R. Lasky,et al.  Otoacoustic emission, evoked potential, and behavioral auditory thresholds in the rhesus monkey (Macaca mulatta) , 1999, Hearing Research.

[35]  J. Kaas,et al.  The reorganization of somatosensory cortex following peripheral nerve damage in adult and developing mammals. , 1983, Annual review of neuroscience.

[36]  D. Hubel,et al.  RECEPTIVE FIELDS OF CELLS IN STRIATE CORTEX OF VERY YOUNG, VISUALLY INEXPERIENCED KITTENS. , 1963, Journal of neurophysiology.

[37]  T W Picton,et al.  Thresholds for short-latency auditory-evoked potentials to tones in notched noise in normal-hearing and hearing-impaired subjects. , 1990, Audiology : official organ of the International Society of Audiology.

[38]  D. Hubel,et al.  SINGLE-CELL RESPONSES IN STRIATE CORTEX OF KITTENS DEPRIVED OF VISION IN ONE EYE. , 1963, Journal of neurophysiology.

[39]  Jean-Pascal Pfister,et al.  Optimal Spike-Timing-Dependent Plasticity for Precise Action Potential Firing in Supervised Learning , 2005, Neural Computation.

[40]  J. Rauschecker Cortical map plasticity in animals and humans. , 2002, Progress in brain research.

[41]  Tobias Bonhoeffer,et al.  Lifelong learning: ocular dominance plasticity in mouse visual cortex , 2006, Current Opinion in Neurobiology.

[42]  E. Knudsen,et al.  Experience-dependent plasticity in the inferior colliculus: a site for visual calibration of the neural representation of auditory space in the barn owl , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.