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

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Abstract

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.

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References

  • Anderson LA, Malmierca MS (2013) The effect of auditory cortex deactivation on stimulus-specific adaptation in the inferior colliculus of the rat. Eur J Neurosci 37:52–62

    Article  CAS  PubMed  Google Scholar 

  • Antunes FM, Malmierca MS (2011) Effect of auditory cortex deactivation on stimulus-specific adaptation in the medial geniculate body. J Neurosci 31:17306–16

    Article  CAS  PubMed  Google Scholar 

  • Azeredo WJ, Kliment ML, Morley BJ, Relkin E, Slepecky NB, Sterns A, Warr WB, Weekly JM, Woods CI (1999) Olivocochlear neurons in the chinchilla: a retrograde fluorescent labelling study. Hear Res 134:57–70

    Article  CAS  PubMed  Google Scholar 

  • Backus BC, Guinan JJ Jr (2007) Measurement of the distribution of medial olivocochlear acoustic reflex strengths across normal-hearing individuals via otoacoustic emissions. J Assoc Res Otolaryngol 8:484–96

    Article  PubMed Central  PubMed  Google Scholar 

  • Bajo VM, Moore DR (2005) Descending projections from the auditory cortex to the inferior colliculus in the gerbil, Meriones unguiculatus. J Comp Neurol 486:101–16

    Article  PubMed  Google Scholar 

  • Bajo VM, King AJ (2013) Cortical modulation of auditory processing in the midbrain. Front Neural Circuits 6:114

    Article  PubMed Central  PubMed  Google Scholar 

  • Brown DJ, Patuzzi RB (2010) Evidence that the compound action potential (CAP) from the auditory nerve is a stationary potential generated across dura mater. Hear Res 267:12–26

    Article  PubMed  Google Scholar 

  • Buño W Jr (1978) Auditory nerve fiber activity influenced by contralateral ear sound stimulation. Exp Neurol 59:62–74

    Article  PubMed  Google Scholar 

  • Chambers AR, Hancock KE, Maison SF, Liberman MC, Polley DB (2012) Sound-evoked olivocochlear activation in unanesthetized mice. J Assoc Res Otolaryngol 13:209–17

    Article  PubMed Central  PubMed  Google Scholar 

  • Clarac, F (2005) The history of reflexes. Part 1: from Descartes to Pavlov. IBRO History of Neuroscience. [http://ibro.info/wp-content/uploads/2012/12/The-History-of-Reflexes-Part-1.pdf]

  • Clarac F (2008) Some historical reflections on the neural control of locomotion. Brain Res Rev 57:13–21

    Article  PubMed  Google Scholar 

  • Darrow KN, Maison SF, Liberman MC (2006) Cochlear efferent feedback balances interaural sensitivity. Nat Neurosci 9:1474–6

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Delano PH, Elgueda D, Hamame CM, Robles L (2007) Selective attention to visual stimuli reduces cochlear sensitivity in chinchillas. J Neurosci 27:4146–53

    Article  CAS  PubMed  Google Scholar 

  • Delano PH, Pavez E, Robles L, Maldonado PE (2008) Stimulus-dependent oscillations and evoked potentials in chinchilla auditory cortex. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 194:693–700

    Article  PubMed  Google Scholar 

  • De Ridder D, Verstraeten E, Van der Kelen K, De Mulder G, Sunaert S, Verlooy J, Van de Heyning P, Moller A (2005) Transcranial magnetic stimulation for tinnitus: influence of tinnitus duration on stimulation parameter choice and maximal tinnitus suppression. Otol Neurotol 26:616–9

    Article  PubMed  Google Scholar 

  • de Venecia RK, Liberman MC, Guinan JJ Jr, Brown MC (2005) Medial olivocochlear reflex interneurons are located in the posteroventral cochlear nucleus: a kainic acid lesion study in guinea pigs. J Comp Neurol 487:345–60

    Article  PubMed Central  PubMed  Google Scholar 

  • Doucet JR, Rose L, Ryugo DK (2002) The cellular origin of corticofugal projections to the superior olivary complex in the rat. Brain Res 925:28–41

    Article  CAS  PubMed  Google Scholar 

  • Eldredge DH, Miller JD, Bohne BA (1981) A frequency-position map for the chinchilla cochlea. J Acoust Soc Am 69:1091–1095

    Article  CAS  PubMed  Google Scholar 

  • Elgueda D, Delano PH, Robles L (2011) Effects of electrical stimulation of olivocochlear fibers in cochlear potentials in the chinchilla. J Assoc Res Otolaryngol 12:317–27

    Article  PubMed Central  PubMed  Google Scholar 

  • Feldman AG, Orlovsky GN (1972) The influence of different descending systems on the tonic stretch reflex in the cat. Exp Neurol 37:481–94

    Article  CAS  PubMed  Google Scholar 

  • Fenoy AJ, Severson MA, Volkov IO, Brugge JF, Howard MA 3rd (2006) Hearing suppression induced by electrical stimulation of human auditory cortex. Brain Res 1118:75–83

    Article  CAS  PubMed  Google Scholar 

  • Fregni F, Marcondes R, Boggio PS, Marcolin MA, Rigonatti SP, Sanchez G, Nitsche MA, Pascual-Leone A (2006) Transient tinnitus suppression induced by repetitive transcranial magnetic stimulation and transcranial direct current stimulation. Eur J Neurol 13:996–1001

    Article  CAS  PubMed  Google Scholar 

  • Gaucher Q, Edeline JM, Gourévitch B (2012) How different are the local field potentials and spiking activities? Insights from multi-electrodes arrays. J Physiol Paris 106:93–103

    Article  PubMed  Google Scholar 

  • Groff JA, Liberman MC (2003) Modulation of cochlear afferent response by the lateral olivocochlear system: activation via electrical stimulation of the inferior colliculus. J Neurophysiol 90:3178–200

    Article  PubMed  Google Scholar 

  • Guitton MJ, Avan P, Puel JL, Bonfils P (2004) Medial olivocochlear efferent activity in awake guinea pigs. Neuroreport 15:1379–82

    Article  CAS  PubMed  Google Scholar 

  • Harel N, Mori N, Sawada S, Mount RJ, Harrison RV (2000) Three distinct auditory areas of cortex (AI, AII, and AAF) defined by optical imaging of intrinsic signals. Neuroimage 11:302–12

    Article  CAS  PubMed  Google Scholar 

  • Harrison RV, Kakigi A, Hirakawa H, Harel N, Mount RJ (1996) Tonotopic mapping in auditory cortex of the chinchilla. Hear Res 100:157–63

    Article  CAS  PubMed  Google Scholar 

  • Kawase T, Liberman MC (1993) Antimasking effects of the olivocochlear reflex. I. Enhancement of compound action potentials to masked tones. J Neurophysiol 70:2519–32

    CAS  PubMed  Google Scholar 

  • Khalfa S, Bougeard R, Morand N, Veuillet E, Isnard J, Guenot M, Ryvlin P, Fischer C, Collet L (2001) Evidence of peripheral auditory activity modulation by the auditory cortex in humans. Neuroscience 104:347–58

    Article  CAS  PubMed  Google Scholar 

  • Kong L, Xiong C, Li L, Yan J (2014) Frequency-specific corticofugal modulation of the dorsal cochlear nucleus in mice. Front Syst Neurosci 1;8:125.

  • Lamas V, Alvarado JC, Carro J, Merchán MA (2013) Long-term evolution of brainstem electrical evoked responses to sound after restricted ablation of the auditory cortex. PLoS One 8(9):e73585

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Langguth B, De Ridder D (2013) Tinnitus: therapeutic use of superficial brain stimulation. Handb Clin Neurol 116:441–67

    Article  PubMed  Google Scholar 

  • Larsen E, Liberman MC (2009) Slow build-up of cochlear suppression during sustained contralateral noise: central modulation of olivocochlear efferents? Hear Res 256:1–10

    Article  PubMed Central  PubMed  Google Scholar 

  • Leon A, Elgueda D, Silva MA, Hamamé CM, Delano PH (2012) Auditory cortex basal activity modulates cochlear responses in chinchillas. PLoS One 7(4):e36203

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Liberman MC (1989) Rapid assessment of sound-evoked olivocochlear feedback: suppression of compound action potentials by contralateral sound. Hear Res 38:47–56

    Article  CAS  PubMed  Google Scholar 

  • Liberman MC, Liberman LD, Maison SF (2014) Efferent feedback slows cochlear aging. J Neurosci 34:4599–607

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Luo F, Wang Q, Kashani A, Yan J (2008) Corticofugal modulation of initial sound processing in the brain. J Neurosci 28:11615–21

    Article  CAS  PubMed  Google Scholar 

  • Liu X, Yan Y, Wang Y, Yan J (2010) Corticofugal modulation of initial neural processing of sound information from the ipsilateral ear in the mouse. PLoS One 5(11):e14038

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Maison SF, Liberman MC (2000) Predicting vulnerability to acoustic injury with a noninvasive assay of olivocochlear reflex strength. J Neurosci 20:4701–7

    CAS  PubMed  Google Scholar 

  • Malmierca and Ryugo (2011) Descending connections of the auditory cortex to the midbrain and the brainstem. Chapter 9, The auditory cortex, Eds. Winer JA and Schreiner CE, Springer.

  • McIntyre D, Ring C, Carroll D (2004) Effects of arousal and natural baroreceptor activation on the human muscle stretch reflex. Psychophysiology 41:954–60

    Article  PubMed  Google Scholar 

  • Mulders WH, Robertson D (2000) Evidence for direct cortical innervation of medial olivocochlear neurones in rats. Hear Res 144:65–72

    Article  CAS  PubMed  Google Scholar 

  • Oatman LC (1971) Role of visual attention on auditory evoked potentials in unanesthetized cats. Exp Neurol 32:341–356

    Article  CAS  PubMed  Google Scholar 

  • Perrot X, Ryvlin P, Isnard J, Guénot M, Catenoix H, Fischer C, Mauguière F, Collet L (2006) Evidence for corticofugal modulation of peripheral auditory activity in humans. Cereb Cortex 16:941–8

    Article  PubMed  Google Scholar 

  • Robles L, Delano PH (2008) Efferent system. The senses: a comprehensive reference. Academic Press, London, pp 413–445

    Book  Google Scholar 

  • Saldaña E, Feliciano M, Mugnaini E (1996) Distribution of descending projections from primary auditory neocortex to inferior colliculus mimics the topography of intracollicular projections. J Comp Neurol 371:15–40

    Article  PubMed  Google Scholar 

  • Schofield BR (2010) Central descending auditory pathways. Auditory and vestibular efferents. Springer, New York, pp 261–290

    Google Scholar 

  • Schofield BR, Coomes DL (2005) Auditory cortical projections to the cochlear nucleus in guinea pigs. Hear Res 199:89–102

    Article  PubMed  Google Scholar 

  • Sellick P, Patuzzi R, Robertson D (2003) Primary afferent and cochlear nucleus contributions to extracellular potentials during tone-bursts. Hear Res 176:42–58

    Article  PubMed  Google Scholar 

  • Sridhar TS, Liberman MC, Brown MC, Sewell WF (1995) A novel cholinergic “slow effect” of efferent stimulation on cochlear potentials in the guinea pig. J Neurosci 15:3667–78

    CAS  PubMed  Google Scholar 

  • Srinivasan S, Keil A, Stratis K, Woodruff Carr KL, Smith DW (2012) Effects of cross-modal selective attention on the sensory periphery: cochlear sensitivity is altered by selective attention. Neuroscience 223:325–32

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Straka H (2010) Ontogenetic rules and constraints of vestibulo-ocular reflex development. Curr Opin Neurobiol 20:689–95

    Article  CAS  PubMed  Google Scholar 

  • Tang AH, Schroeder LA (1973) Spinal-cord depressant effects of ketamine and etoxadrol in the cat and the rat. Anesthesiology 39:37–43

    Article  CAS  PubMed  Google Scholar 

  • Thompson AM, Thompson GC (1993) Relationship of descending inferior colliculus projections to olivocochlear neurons. J Comp Neurol 335:402–12

    Article  CAS  PubMed  Google Scholar 

  • Velluti R, Pedemonte M, Garcia-Austt E (1989) Correlative changes of auditory nerve and microphonic potentials throughout sleep. Hear Res 39:203–208

    Article  CAS  PubMed  Google Scholar 

  • Wittekindt A, Kaiser J, Abel C (2014) Attentional modulation of the inner ear: a combined otoacoustic emission and EEG study. J Neurosci 34:9995–10002

    Article  CAS  PubMed  Google Scholar 

  • Xiao Z, Suga N (2002a) Modulation of cochlear hair cells by the auditory cortex in the mustached bat. Nat Neurosci 5:57–63

    Article  CAS  PubMed  Google Scholar 

  • Xiao Z, Suga N (2002b) Reorganization of the cochleotopic map in the bat’s auditory system by inhibition. Proc Natl Acad Sci USA 99:15743–8

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zhang J, Zhang Y, Zhang X (2011) Auditory cortex electrical stimulation suppresses tinnitus in rats. J Assoc Res Otolaryngol 12:185–201

    Article  PubMed Central  PubMed  Google Scholar 

  • Zhang J (2013) Auditory cortex stimulation to suppress tinnitus: mechanisms and strategies. Hear Res 295:38–57

    Article  PubMed  Google Scholar 

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Acknowledgments

This study was funded by Fondecyt 1120256 to PHD, Apoyo de viaje de la Vicerrectoría de Investigación de la Universidad de Chile to PHD, and Beca CONICYT to CDD and Fundación Puelma. We thank Fernando Vergara for his technical assistance.

Conflict of Interest

The authors declare that they have no conflict of interest.

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Authors and Affiliations

  1. Laboratorio de Neurobiología de la Audición, Programa de Fisiología y Biofísica, Instituto de Ciencias Biomédicas, Facultad de Medicina, Universidad de Chile, 8380453, Santiago, Chile

    Constantino D. Dragicevic, Cristian Aedo, Alex León, Macarena Bowen, Natalia Jara, Gonzalo Terreros, Luis Robles & Paul H. Delano

  2. Escuela Fonoaudiología, Facultad de Medicina, Universidad de Chile, 8380453, Santiago, Chile

    Macarena Bowen

  3. Departamento de Otorrinolaringología, Hospital Clínico de la Universidad de Chile, 8380456, Santiago, Chile

    Paul H. Delano

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  1. Constantino D. Dragicevic
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  2. Cristian Aedo
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  3. Alex León
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  4. Macarena Bowen
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  7. Luis Robles
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  8. Paul H. Delano
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Correspondence to Paul H. Delano.

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Dragicevic, C.D., Aedo, C., León, A. et al. The Olivocochlear Reflex Strength and Cochlear Sensitivity are Independently Modulated by Auditory Cortex Microstimulation. JARO 16, 223–240 (2015). https://doi.org/10.1007/s10162-015-0509-9

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  • DOI: https://doi.org/10.1007/s10162-015-0509-9

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