The Olivocochlear Reflex Strength and Cochlear Sensitivity are Independently Modulated by Auditory Cortex Microstimulation

In mammals, efferent projections to the cochlear receptor are constituted by olivocochlear (OC) fibers that originate in the superior olivary complex. Medial and lateral OC neurons make synapses with outer hair cells and with auditory nerve fibers, respectively. In addition to the OC system, there are also descending projections from the auditory cortex that are directed towards the thalamus, inferior colliculus, cochlear nucleus, and superior olivary complex. Olivocochlear function can be assessed by measuring a brainstem reflex mediated by auditory nerve fibers, cochlear nucleus neurons, and OC fibers. Although it is known that the OC reflex is activated by contralateral acoustic stimulation and produces a suppression of cochlear responses, the influence of cortical descending pathways in the OC reflex is largely unknown. Here, we used auditory cortex electrical microstimulation in chinchillas to study a possible cortical modulation of cochlear and auditory nerve responses to tones in the absence and presence of contralateral noise. We found that cortical microstimulation produces two different peripheral modulations: (i) changes in cochlear sensitivity evidenced by amplitude modulation of cochlear microphonics and auditory nerve compound action potentials and (ii) enhancement or suppression of the OC reflex strength as measured by auditory nerve responses, which depended on the intersubject variability of the OC reflex. Moreover, both corticofugal effects were not correlated, suggesting the presence of two functionally different efferent pathways. These results demonstrate that auditory cortex electrical microstimulation independently modulates the OC reflex strength and cochlear sensitivity.

[1]  Robert V. Harrison,et al.  Three Distinct Auditory Areas of Cortex (AI, AII, and AAF) Defined by Optical Imaging of Intrinsic Signals , 2000, NeuroImage.

[2]  Jun Yan,et al.  Frequency-specific corticofugal modulation of the dorsal cochlear nucleus in mice , 2014, Front. Syst. Neurosci..

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

[4]  Jun Yan,et al.  Corticofugal Modulation of Initial Neural Processing of Sound Information from the Ipsilateral Ear in the Mouse , 2010, PloS one.

[5]  B. Schofield,et al.  Auditory cortical projections to the cochlear nucleus in guinea pigs , 2005, Hearing Research.

[6]  J. Guinan,et al.  Medial olivocochlear reflex interneurons are located in the posteroventral cochlear nucleus: A kainic acid lesion study in guinea pigs , 2005, The Journal of comparative neurology.

[7]  D Robertson,et al.  Evidence for direct cortical innervation of medial olivocochlear neurones in rats , 2000, Hearing Research.

[8]  A. Basbaum,et al.  The senses : a comprehensive reference , 2008 .

[9]  Anna R. Chambers,et al.  Sound-Evoked Olivocochlear Activation in Unanesthetized Mice , 2012, Journal of the Association for Research in Otolaryngology.

[10]  Carlos M. Hamamé,et al.  Auditory Cortex Basal Activity Modulates Cochlear Responses in Chinchillas , 2012, PloS one.

[11]  Donald Robertson,et al.  Primary afferent and cochlear nucleus contributions to extracellular potentials during tone-bursts , 2003, Hearing Research.

[12]  Carlos M. Hamamé,et al.  Selective Attention to Visual Stimuli Reduces Cochlear Sensitivity in Chinchillas , 2007, The Journal of Neuroscience.

[13]  Leslie D. Liberman,et al.  Efferent Feedback Slows Cochlear Aging , 2014, The Journal of Neuroscience.

[14]  E. Mugnaini,et al.  Distribution of descending projections from primary auditory neocortex to inferior colliculus mimics the topography of intracollicular projections , 1996, The Journal of comparative neurology.

[15]  T Kawase,et al.  Antimasking effects of the olivocochlear reflex. I. Enhancement of compound action potentials to masked tones. , 1993, Journal of neurophysiology.

[16]  W. Buño,et al.  Auditory nerve fiber activity influenced by contralateral ear sound stimulation , 1978, Experimental Neurology.

[17]  M. Liberman,et al.  Predicting Vulnerability to Acoustic Injury with a Noninvasive Assay of Olivocochlear Reflex Strength , 2000, The Journal of Neuroscience.

[18]  D. De Ridder,et al.  Tinnitus: therapeutic use of superficial brain stimulation. , 2013, Handbook of clinical neurology.

[19]  P. Avan,et al.  Medial olivocochlear efferent activity in awake guinea pigs , 2004, Neuroreport.

[20]  G. C. Thompson,et al.  Relationship of descending inferior colliculus projections to olivocochlear neurons , 1993, The Journal of comparative neurology.

[21]  Jinsheng Zhang Auditory cortex stimulation to suppress tinnitus: Mechanisms and strategies , 2013, Hearing Research.

[22]  J. Alvarado,et al.  Long-Term Evolution of Brainstem Electrical Evoked Responses to Sound after Restricted Ablation of the Auditory Cortex , 2013, PloS one.

[23]  M. Liberman,et al.  Modulation of cochlear afferent response by the lateral olivocochlear system: activation via electrical stimulation of the inferior colliculus. , 2003, Journal of neurophysiology.

[24]  The History of Reflexes Part 1 : From Descartes to Pavlov , .

[25]  François Mauguière,et al.  Evidence for corticofugal modulation of peripheral auditory activity in humans. , 2006, Cerebral cortex.

[26]  A. G. Feldman,et al.  The influence of different descending systems on the tonic stretch reflex in the cat. , 1972, Experimental neurology.

[27]  W. Warr,et al.  Olivocochlear neurons in the chinchilla: a retrograde fluorescent labelling study , 1999, Hearing Research.

[28]  Boris Gourévitch,et al.  How different are the local field potentials and spiking activities? Insights from multi-electrodes arrays , 2012, Journal of Physiology-Paris.

[29]  L. C. Oatman Role of visual attention on auditory evoked potentials in unanesthetized cats. , 1971, Experimental neurology.

[30]  L. Robles,et al.  3.24 – Efferent System , 2008 .

[31]  J. D. Miller,et al.  A frequency-position map for the chinchilla cochlea. , 1977, The Journal of the Acoustical Society of America.

[32]  Slow build-up of cochlear suppression during sustained contralateral noise: Central modulation of olivocochlear efferents? , 2009, Hearing Research.

[33]  Jochen Kaiser,et al.  Attentional Modulation of the Inner Ear: A Combined Otoacoustic Emission and EEG Study , 2014, The Journal of Neuroscience.

[34]  N. Suga,et al.  Reorganization of the cochleotopic map in the bat's auditory system by inhibition , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[35]  Sergio P. Rigonatti,et al.  Transient tinnitus suppression induced by repetitive transcranial magnetic stimulation and transcranial direct current stimulation , 2006, European journal of neurology.

[36]  N. Harel,et al.  Tonotopic mapping in auditory cortex of the chinchilla , 1996, Hearing Research.

[37]  R. Fay,et al.  Auditory and Vestibular Efferents , 2011 .

[38]  Jinsheng Zhang,et al.  Auditory Cortex Electrical Stimulation Suppresses Tinnitus in Rats , 2011, Journal of the Association for Research in Otolaryngology.

[39]  A. H. Tang,et al.  Spinal-cord Depressant Effects of Ketamine and Etoxadrol* in the Cat and the Rat , 1973, Anesthesiology.

[40]  John J. Guinan,et al.  Measurement of the Distribution of Medial Olivocochlear Acoustic Reflex Strengths Across Normal-Hearing Individuals via Otoacoustic Emissions , 2007, Journal of the Association for Research in Otolaryngology.

[41]  D. Moore,et al.  Descending projections from the auditory cortex to the inferior colliculus in the gerbil, Meriones unguiculatus , 2005, The Journal of comparative neurology.

[42]  TS Sridhar,et al.  A novel cholinergic "slow effect" of efferent stimulation on cochlear potentials in the guinea pig , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[43]  M. Malmierca,et al.  The effect of auditory cortex deactivation on stimulus‐specific adaptation in the inferior colliculus of the rat , 2013, The European journal of neuroscience.

[44]  M. Charles Liberman,et al.  Rapid assessment of sound-evoked olivocochlear feedback: Suppression of compound action potentials by contralateral sound , 1989, Hearing Research.

[45]  J. Brugge,et al.  Hearing suppression induced by electrical stimulation of human auditory cortex , 2006, Brain Research.

[46]  Effects of Electrical Stimulation of Olivocochlear Fibers in Cochlear Potentials in the Chinchilla , 2011, Journal of the Association for Research in Otolaryngology.

[47]  C. Ring,et al.  Effects of arousal and natural baroreceptor activation on the human muscle stretch reflex. , 2004, Psychophysiology.

[48]  Pedro E. Maldonado,et al.  Stimulus-dependent oscillations and evoked potentials in chinchilla auditory cortex , 2008, Journal of Comparative Physiology A.

[49]  M. Malmierca,et al.  Descending Connections of Auditory Cortex to the Midbrain and Brain Stem , 2011 .

[50]  D. W. Smith,et al.  Effects of cross-modal selective attention on the sensory periphery: Cochlear sensitivity is altered by selective attention , 2012, Neuroscience.

[51]  Victoria M. Bajo,et al.  Cortical modulation of auditory processing in the midbrain , 2013, Front. Neural Circuits.

[52]  B. Schofield Central Descending Auditory Pathways , 2011 .

[53]  Stefan Sunaert,et al.  Transcranial Magnetic Stimulation for Tinnitus: Influence of Tinnitus Duration on Stimulation Parameter Choice and Maximal Tinnitus Suppression , 2005, Otology & neurotology : official publication of the American Otological Society, American Neurotology Society [and] European Academy of Otology and Neurotology.

[54]  Jun Yan,et al.  Corticofugal Modulation of Initial Sound Processing in the Brain , 2008, The Journal of Neuroscience.

[55]  R. Patuzzi,et al.  Evidence that the compound action potential (CAP) from the auditory nerve is a stationary potential generated across dura mater , 2010, Hearing Research.

[56]  H. Straka Ontogenetic rules and constraints of vestibulo-ocular reflex development , 2010, Current Opinion in Neurobiology.

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

[58]  M. Malmierca,et al.  Effect of Auditory Cortex Deactivation on Stimulus-Specific Adaptation in the Medial Geniculate Body , 2011, The Journal of Neuroscience.

[59]  E. Garcı́a-Austt,et al.  Correlative changes of auditory nerve and microphonic potentials throughout sleep , 1989, Hearing Research.

[60]  D. Ryugo,et al.  The cellular origin of corticofugal projections to the superior olivary complex in the rat , 2002, Brain Research.

[61]  M. Liberman,et al.  Cochlear efferent feedback balances interaural sensitivity , 2006, Nature Neuroscience.

[62]  François Clarac,et al.  Some historical reflections on the neural control of locomotion , 2008, Brain Research Reviews.