Long-term, passive exposure to non-traumatic acoustic noise induces neural adaptation in the adult rat medial geniculate body and auditory cortex

Exposure to loud sounds can lead to permanent hearing loss, i.e., the elevation of hearing thresholds. Exposure at more moderate sound pressure levels (SPLs) (non-traumatic and within occupational limits) may not elevate thresholds, but could in the long-term be detrimental to speech intelligibility by altering its spectrotemporal representation in the central auditory system. In support of this, electrophysiological and behavioral changes following long-term, passive (no conditioned learning) exposure at moderate SPLs have recently been observed in adult animals. To assess the potential effects of moderately loud noise on the entire auditory brain, we employed functional magnetic resonance imaging (fMRI) to study noise-exposed adult rats. We find that passive, pulsed broadband noise exposure for two months at 65 dB SPL leads to a decrease of the sound-evoked blood oxygenation level-dependent fMRI signal in the thalamic medial geniculate body (MGB) and in the auditory cortex (AC). This points to the thalamo-cortex as the site of the neural adaptation to the moderately noisy environment. The signal reduction is statistically significant during 10 Hz pulsed acoustic stimulation (MGB: p<0.05, AC: p<10(-4)), but not during 5 Hz stimulation. This indicates that noise exposure has a greater effect on the processing of higher pulse rate sounds. This study has enhanced our understanding of functional changes following exposure by mapping changes across the entire auditory brain. These findings have important implications for speech processing, which depends on accurate processing of sounds with a wide spectrum of pulse rates.

[1]  Dose-response hearing loss for white noise in the Sprague-Dawley rat. , 1988, Fundamental and applied toxicology : official journal of the Society of Toxicology.

[2]  Joe S. Cheng,et al.  Noninvasive fMRI Investigation of Interaural Level Difference Processing in the Rat Auditory Subcortex , 2013, PloS one.

[3]  Deborah A. Hall,et al.  How challenges in auditory fMRI led to general advancements for the field , 2012, NeuroImage.

[4]  D. Hall,et al.  The mechanisms of tinnitus: Perspectives from human functional neuroimaging , 2009, Hearing Research.

[5]  S. Nelson,et al.  Homeostatic plasticity in the developing nervous system , 2004, Nature Reviews Neuroscience.

[6]  J. Eggermont,et al.  Cortical tonotopic map plasticity and behavior , 2011, Neuroscience & Biobehavioral Reviews.

[7]  K Scheffler,et al.  Cortical reorganization after acute unilateral hearing loss traced by fMRI , 2000, Neurology.

[8]  J. Middleton,et al.  Imaging the neural correlates of tinnitus: a comparison between animal models and human studies , 2012, Front. Syst. Neurosci..

[9]  J. Eggermont,et al.  Reversible Long-Term Changes in Auditory Processing in Mature Auditory Cortex in the Absence of Hearing Loss Induced by Passive, Moderate-Level Sound Exposure , 2012, Ear and hearing.

[10]  J. Hirsch,et al.  fMRI Evidence for Cortical Modification during Learning of Mandarin Lexical Tone , 2003, Journal of Cognitive Neuroscience.

[11]  Klaus Scheffler,et al.  Musical Training Induces Functional Plasticity in Human Hippocampus , 2010, The Journal of Neuroscience.

[12]  François Lazeyras,et al.  FMRI evidence for activation of multiple cortical regions in the primary auditory cortex of deaf subjects users of multichannel cochlear implants. , 2004, Cerebral cortex.

[13]  Kevin C. Chan,et al.  BOLD fMRI investigation of the rat auditory pathway and tonotopic organization , 2012, NeuroImage.

[14]  J. Edeline,et al.  Is the din really harmless? Long-term effects of non-traumatic noise on the adult auditory system , 2014, Nature Reviews Neuroscience.

[15]  C Pantev,et al.  Dynamics of auditory plasticity after cochlear implantation: a longitudinal study. , 2006, Cerebral cortex.

[16]  U. Mitzdorf Current source-density method and application in cat cerebral cortex: investigation of evoked potentials and EEG phenomena. , 1985, Physiological reviews.

[17]  D. Irvine,et al.  Absence of plasticity of the frequency map in dorsal cochlear nucleus of adult cats after unilateral partial cochlear lesions , 1998, The Journal of comparative neurology.

[18]  M. Verhoye,et al.  Light stimulus frequency dependence of activity in the rat visual system as studied with high-resolution BOLD fMRI. , 2006, Journal of neurophysiology.

[19]  Alan P. Koretsky,et al.  High Resolution BOLD-fMRI of the Auditory System in Rats , 2008 .

[20]  R. Linke,et al.  Convergent and complementary projections of the caudal paralaminar thalamic nuclei to rat temporal and insular cortex. , 2000, Cerebral cortex.

[21]  Kate E Watkins,et al.  Changes in neural activity associated with learning to articulate novel auditory pseudowords by covert repetition , 2008, Human brain mapping.

[22]  Weimin Zheng,et al.  Auditory map reorganization and pitch discrimination in adult rats chronically exposed to low-level ambient noise , 2012, Front. Syst. Neurosci..

[23]  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.

[24]  Niraj S. Desai,et al.  Activity-dependent scaling of quantal amplitude in neocortical neurons , 1998, Nature.

[25]  V. Murthy,et al.  Synaptic gain control and homeostasis , 2003, Current Opinion in Neurobiology.

[26]  J. Eggermont,et al.  Spectrally enhanced acoustic environment disrupts frequency representation in cat auditory cortex , 2006, Nature Neuroscience.

[27]  Timothy D. Griffiths,et al.  Orthogonal representation of sound dimensions in the primate midbrain , 2011, Nature Neuroscience.

[28]  T. Duong,et al.  Regional Cerebral Blood Flow and BOLD Responses in Conscious and Anesthetized Rats under Basal and Hypercapnic Conditions: Implications for Functional MRI Studies , 2003, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[29]  J. Eggermont,et al.  Passive exposure of adult cats to moderate-level tone pip ensembles differentially decreases AI and AII responsiveness in the exposure frequency range , 2010, Hearing Research.

[30]  Tao Jin,et al.  Cortical layer-dependent dynamic blood oxygenation, cerebral blood flow and cerebral blood volume responses during visual stimulation , 2008, NeuroImage.

[31]  Mark C. W. van Rossum,et al.  Activity Deprivation Reduces Miniature IPSC Amplitude by Decreasing the Number of Postsynaptic GABAA Receptors Clustered at Neocortical Synapses , 2002, The Journal of Neuroscience.

[32]  Kevin C. Chan,et al.  BOLD Temporal Dynamics of Rat Superior Colliculus and Lateral Geniculate Nucleus following Short Duration Visual Stimulation , 2011, PloS one.

[33]  Kevin C. Chan,et al.  Balanced steady‐state free precession fMRI with intravascular susceptibility contrast agent , 2012, Magnetic resonance in medicine.

[34]  Kevin C. Chan,et al.  BOLD responses in the superior colliculus and lateral geniculate nucleus of the rat viewing an apparent motion stimulus , 2011, NeuroImage.

[35]  M. Liberman,et al.  Adding Insult to Injury: Cochlear Nerve Degeneration after “Temporary” Noise-Induced Hearing Loss , 2009, The Journal of Neuroscience.

[36]  Michael M Merzenich,et al.  Environmental noise exposure degrades normal listening processes , 2012, Nature Communications.

[37]  Chongyu Ren,et al.  Effects of Repeated “Benign” Noise Exposures in Young CBA Mice: Shedding Light on Age-related Hearing Loss , 2012, Journal of the Association for Research in Otolaryngology.

[38]  Christopher P. Pawela,et al.  Modeling of region-specific fMRI BOLD neurovascular response functions in rat brain reveals residual differences that correlate with the differences in regional evoked potentials , 2008, NeuroImage.

[39]  Alfredo Fontanini,et al.  Network homeostasis: a matter of coordination , 2009, Current Opinion in Neurobiology.

[40]  J. Eggermont,et al.  Effects of passive, moderate-level sound exposure on the mature auditory cortex: Spectral edges, spectrotemporal density, and real-world noise , 2013, Hearing Research.

[41]  V. Bajo,et al.  Insult-induced adaptive plasticity of the auditory system , 2014, Front. Neurosci..

[42]  Ed X. Wu,et al.  The inferior colliculus is involved in deviant sound detection as revealed by BOLD fMRI , 2014, NeuroImage.

[43]  Ravi S. Menon,et al.  Functional imaging of auditory cortex in adult cats using high-field fMRI. , 2014, Journal of visualized experiments : JoVE.

[44]  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.

[45]  M. Verhoye,et al.  Functional magnetic resonance imaging (FMRI) with auditory stimulation in songbirds. , 2013, Journal of visualized experiments : JoVE.

[46]  J. Isaac,et al.  Thalamocortical Inputs Show Post-Critical-Period Plasticity , 2012, Neuron.

[47]  D. De Ridder,et al.  Neuroimaging and Neuromodulation: Complementary Approaches for Identifying the Neuronal Correlates of Tinnitus , 2012, Front. Syst. Neurosci..

[48]  Kevin C. Chan,et al.  High fidelity tonotopic mapping using swept source functional magnetic resonance imaging , 2012, NeuroImage.

[49]  N. Kiang,et al.  Acoustic trauma in cats. Cochlear pathology and auditory-nerve activity. , 1978, Acta oto-laryngologica. Supplementum.

[50]  G. Turrigiano Homeostatic plasticity in neuronal networks: the more things change, the more they stay the same , 1999, Trends in Neurosciences.

[51]  G. Turrigiano The Self-Tuning Neuron: Synaptic Scaling of Excitatory Synapses , 2008, Cell.

[52]  F. Hyder,et al.  Cerebral energetics and spiking frequency: The neurophysiological basis of fMRI , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[53]  Michael M. Merzenich,et al.  Natural Restoration of Critical Period Plasticity in the Juvenile and Adult Primary Auditory Cortex , 2011, The Journal of Neuroscience.

[54]  Marc R Kamke,et al.  Plasticity in the tonotopic organization of the medial geniculate body in adult cats following restricted unilateral cochlear lesions , 2003, The Journal of comparative neurology.

[55]  R A Levine,et al.  Lateralized tinnitus studied with functional magnetic resonance imaging: abnormal inferior colliculus activation. , 2000, Journal of neurophysiology.

[56]  Ed X. Wu,et al.  Functional magnetic resonance imaging of sound pressure level encoding in the rat central auditory system , 2013, NeuroImage.

[57]  J. Eggermont,et al.  Intermittent exposure with moderate-level sound impairs central auditory function of mature animals without concomitant hearing loss , 2010, Hearing Research.

[58]  Stefan Uppenkamp,et al.  Functional magnetic resonance imaging of the ascending stages of the auditory system in dogs , 2013, BMC Veterinary Research.

[59]  Arafat Angulo-Perkins,et al.  Music listening engages specific cortical regions within the temporal lobes: Differences between musicians and non-musicians , 2014, Cortex.

[60]  D. Tank,et al.  Brain magnetic resonance imaging with contrast dependent on blood oxygenation. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[61]  T. Hensch Critical period regulation. , 2004, Annual review of neuroscience.

[62]  G. Paxinos,et al.  The Rat Brain in Stereotaxic Coordinates , 1983 .

[63]  Essa Yacoub,et al.  Spatial organization of frequency preference and selectivity in the human inferior colliculus , 2012, Nature Communications.

[64]  I. Winkler,et al.  Long-term exposure to noise impairs cortical sound processing and attention control. , 2004, Psychophysiology.

[65]  Dave R. M. Langers,et al.  Tonotopic mapping of human auditory cortex , 2014, Hearing Research.

[66]  Kevin C. Chan,et al.  Functional MRI of postnatal visual development in normal and hypoxic–ischemic-injured superior colliculi , 2010, NeuroImage.

[67]  J. A. Frost,et al.  Function of the left planum temporale in auditory and linguistic processing , 1996, NeuroImage.

[68]  J. Eggermont,et al.  Passive exposure of adult cats to bandlimited tone pip ensembles or noise leads to long-term response suppression in auditory cortex , 2011, Hearing Research.

[69]  Niraj S. Desai,et al.  Plasticity in the intrinsic excitability of cortical pyramidal neurons , 1999, Nature Neuroscience.

[70]  J. Eggermont,et al.  Long-term, partially-reversible reorganization of frequency tuning in mature cat primary auditory cortex can be induced by passive exposure to moderate-level sounds , 2009, Hearing Research.

[71]  P. Alku,et al.  Long-term exposure to occupational noise alters the cortical organization of sound processing , 2005, Clinical Neurophysiology.

[72]  Shinobu Masaki,et al.  Learning-induced neural plasticity associated with improved identification performance after training of a difficult second-language phonetic contrast , 2003, NeuroImage.

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