Supra-Threshold Hearing and Fluctuation Profiles: Implications for Sensorineural and Hidden Hearing Loss

  • Laurel H. CarneyEmail author
Review Article


An important topic in contemporary auditory science is supra-threshold hearing. Difficulty hearing at conversational speech levels in background noise has long been recognized as a problem of sensorineural hearing loss, including that associated with aging (presbyacusis). Such difficulty in listeners with normal thresholds has received more attention recently, especially associated with descriptions of synaptopathy, the loss of auditory nerve (AN) fibers as a result of noise exposure or aging. Synaptopathy has been reported to cause a disproportionate loss of low- and medium-spontaneous rate (L/MSR) AN fibers. Several studies of synaptopathy have assumed that the wide dynamic ranges of L/MSR AN fiber rates are critical for coding supra-threshold sounds. First, this review will present data from the literature that argues against a direct role for average discharge rates of L/MSR AN fibers in coding sounds at moderate to high sound levels. Second, the encoding of sounds at supra-threshold levels is examined. A key assumption in many studies is that saturation of AN fiber discharge rates limits neural encoding, even though the majority of AN fibers, high-spontaneous rate (HSR) fibers, have saturated average rates at conversational sound levels. It is argued here that the cross-frequency profile of low-frequency neural fluctuation amplitudes, not average rates, encodes complex sounds. As described below, this fluctuation-profile coding mechanism benefits from both saturation of inner hair cell (IHC) transduction and average rate saturation associated with the IHC-AN synapse. Third, the role of the auditory efferent system, which receives inputs from L/MSR fibers, is revisited in the context of fluctuation-profile coding. The auditory efferent system is hypothesized to maintain and enhance neural fluctuation profiles. Lastly, central mechanisms sensitive to neural fluctuations are reviewed. Low-frequency fluctuations in AN responses are accentuated by cochlear nucleus neurons which, either directly or via other brainstem nuclei, relay fluctuation profiles to the inferior colliculus (IC). IC neurons are sensitive to the frequency and amplitude of low-frequency fluctuations and convert fluctuation profiles from the periphery into a phase-locked rate profile that is robust across a wide range of sound levels and in background noise. The descending projection from the midbrain (IC) to the efferent system completes a functional loop that, combined with inputs from the L/MSR pathway, is hypothesized to maintain “sharp” supra-threshold hearing, reminiscent of visual mechanisms that regulate optical accommodation. Examples from speech coding and detection in noise are reviewed. Implications for the effects of synaptopathy on control mechanisms hypothesized to influence supra-threshold hearing are discussed. This framework for understanding neural coding and control mechanisms for supra-threshold hearing suggests strategies for the design of novel hearing aid signal-processing and electrical stimulation patterns for cochlear implants.


auditory neural coding speech computational models 



The writing of this review was supported by NIH-DC-R01-001641, NIH-DC-R01-010813, by a sabbatical fellowship at Hanse Wissenschaftskolleg, Delmenhorst, Germany, and further inspired by conversations with colleagues in the Hearing Systems Group during a sabbatical visit to Technical University of Denmark. The manuscript was improved by helpful comments from Drs. David Cameron, Kenneth Henry, Joseph C. Holt, Brian Madden, Virginia Richards, Elizabeth Strickland, and the reviewers and by the editorial guidance of Dr. George Spirou.


  1. Almishaal A, Jennings SG (2016) Effects of a precursor on amplitude modulation detection are consistent with efferent feedback. J Acoust Soc Am 139:2155–2155Google Scholar
  2. Arnott RH, Wallace MN, Shackleton TM, Palmer AR (2004) Onset neurones in the anteroventral cochlear nucleus project to the dorsal cochlear nucleus. J Assoc Res Otolaryngol 5:153–170Google Scholar
  3. Babalian AL, Ryugo DK, Vischer MW, Rouiller EM (1999) Inhibitory synaptic interactions between cochlear nuclei: evidence from an in vitro whole brain study. Neuroreport 10:1913–1917Google Scholar
  4. Beattie RC, Raffin MJ (1985) Reliability of threshold, slope, and PB max for monosyllabic words. J Speech Hear Disord 50:166–178Google Scholar
  5. Beattie RC, Edgerton BJ, Svihovec DV (1977) A comparison of the Auditec of St. Louis cassette recordings of NU-6 and CID W-22 on a normal-hearing population. J Speech Hear Disord 42:60–64Google Scholar
  6. Bharadwaj HM, Verhulst S, Shaheen L, Liberman MC, Shinn-Cunningham BG (2014) Cochlear neuropathy and the coding of supra-threshold sound. Front Syst Neurosci 8:26Google Scholar
  7. Blackburn CC, Sachs MB (1990) The representations of the steady-state vowel sound /Ɛ/ in the discharge patterns of cat anteroventral cochlear nucleus neurons. J Neurophysiol 63:1191–1212Google Scholar
  8. Cant NB (1993) The synaptic organization of the ventral cochlear nucleus of the cat: the peripheral cap of small cells. In: Merchán MA, Juiz JM, Godfrey DA, Mugnaini E (eds) The mammalian cochlear nuclei: organization and function. Springer, New York, pp 91–105Google Scholar
  9. Cant NB (2005) Projections from the cochlear nuclear complex to the inferior colliculus. In: Winer JA, Schreiner CE (eds) The inferior colliculus. Springer, New York, pp 115–131Google Scholar
  10. Cant NB, Benson CG (2003) Parallel auditory pathways: projection patterns of the different neuronal populations in the dorsal and ventral cochlear nuclei. Brain Res Bull 60:457–474Google Scholar
  11. Cant NB, Oliver DL (2018) Overview of the organization of the mammalian auditory pathways: projection pathways and intrinsic microcircuits. In: Oliver DL, Cant NB, Fay RR, Popper AN (eds) The mammalian auditory pathways: synaptic organization and microcircuits. Springer handbook of auditory research. Springer, New YorkGoogle Scholar
  12. Carlyon RP (1987) A release from masking by continuous, random, notched noise. J Acoust Soc Am 81:418–426Google Scholar
  13. Carlyon R (1989) Changes in the masked thresholds of brief tones produced by prior bursts of noise. Hear Res 41:223–235Google Scholar
  14. Carlyon RP, Moore BC (1984) Intensity discrimination: a severe departure from Weber’s law. J Acoust Soc Am 76:1369–1376Google Scholar
  15. Carney LH (2018) Fluctuation contrast and speech-on-speech masking: model midbrain responses to simultaneous speech. In: Santurette S, Dau T, Dalsgaard JC, Tranebjærg L, Andersen T, Poulsen T (eds) Adaptive Processes in Hearing, Proceedings of the International Symposium on Auditory and Audiological Research (ISAAR), vol 6. The Danavox Jubilee Foundation, Ballerup, pp 75–82Google Scholar
  16. Carney LH, Schwarz DM (2014) A Speech Enhancement Strategy based on Midbrain Response Properties, Abstract IHCON meeting.Google Scholar
  17. Carney LH, Richards VM (2016) Predicting masked thresholds based on physiological models of auditory nerve and inferior colliculus population responses. J Acoust Soc Am 140:3272. Google Scholar
  18. Carney LH, Li T, McDonough JM (2015) Speech coding in the brain: representation of vowel formants by midbrain neurons tuned to sound fluctuations. eNeuro 2Google Scholar
  19. Carney LH, Kim DO, Kuwada S (2016) Speech coding in the midbrain: effects of sensorineural hearing loss. In Physiology, psychoacoustics and cognition in normal and impaired hearing, Springer. Advances in experimental medicine and biology. 894:427–435Google Scholar
  20. Carney LH, Oetjen H, Klump G (2017) Discrimination of Schroeder-phase complex stimuli: physiological, behavioral, and modeling studies in the Mongolian gerbil. J Acoust Soc Am 141:3827. Google Scholar
  21. Caspary DM, Ling L, Turner JG, Hughes LF (2008) Inhibitory neurotransmission, plasticity and aging in the mammalian central auditory system. J Exp Biol 211:1781–1791Google Scholar
  22. Cheatham MA, Dallos P (2000) The dynamic range of inner hair cell and organ of Corti responses. J Acoust Soc Am 107:1508–1520Google Scholar
  23. Colburn HS, Carney LH, Heinz MG (2003) Quantifying the information in auditory-nerve responses for level discrimination. J Assoc Res Otolaryngol 4:294–311Google Scholar
  24. Cooper NP, Yates GK (1994) Nonlinear input-output functions derived from the responses of guinea-pig cochlear nerve fibres: variations with characteristic frequency. Hear Res 78:221–234Google Scholar
  25. Dallos P (1985) Response characteristics of mammalian cochlear hair cells. J Neurosci 5:1591–1608Google Scholar
  26. Dallos P (1986) Neurobiology of cochlear inner and outer hair cells: intracellular recordings. Hear Res 22:185–198Google Scholar
  27. Dau T, Kollmeier B, Kohlrausch A (1997a) Modeling auditory processing of amplitude modulation. I. Detection and masking with narrow-band carriers. J Acoust Soc Am 102:2892–2905Google Scholar
  28. Dau T, Kollmeier B, Kohlrausch A (1997b) Modeling auditory processing of amplitude modulation. II. Spectral and temporal integration. J Acoust Soc Am 102:2906–2919Google Scholar
  29. Davis KA, Hancock KE, Delgutte B (2010) Computational models of inferior colliculus neurons. In: Meddis R, Lopez-Poveda E, Fay RR, Popper AN (eds) Computational models of the auditory system. Springer, New York, pp 129–176Google Scholar
  30. Dean I, Harper NS, McAlpine D (2005) Neural population coding of sound level adapts to stimulus statistics. Nat Neurosci 8:1684–1689Google Scholar
  31. Delano PH, Elgueda D, Hamame CM, Robles L (2007) Selective attention to visual stimuli reduces cochlear sensitivity in chinchillas. J Neurosci 27:4146–4153Google Scholar
  32. Delgutte B (1987) Peripheral auditory processing of speech information: implications from a physiological study of intensity discrimination. In: Schouten ME (ed) The psychophysics of speech perception. Springer, Netherlands, pp 333–353Google Scholar
  33. Delgutte B (1996) Physiological models for basic auditory percepts. In: Hawkins HL, McMullen TA, Fay RR (eds) Auditory computation. Springer, New York, pp 157–220Google Scholar
  34. Delgutte B, Kiang NY (1984a) Speech coding in the auditory nerve: I. Vowel-like sounds. J Acoust Soc Am 75:866–878Google Scholar
  35. Delgutte B, Kiang NY (1984b) Speech coding in the auditory nerve: V. Vowels in background noise. J Acoust Soc Am 75:908–918Google Scholar
  36. Deng L, Geisler CD (1987) Responses of auditory-nerve fibers to nasal consonant–vowel syllables. J Acoust Soc Am 82:1977–1988Google Scholar
  37. Deng L, Geisler CD, Greenberg S (1987) Responses of auditory-nerve fibers to multiple-tone complexes. J Acoust Soc Am 82:1989–2000Google Scholar
  38. Doucet JR, Ryugo DK (2006) Structural and functional classes of multipolar cells in the ventral cochlear nucleus. Anat Rec 288:331–344Google Scholar
  39. Dragicevic CD, Aedo C, León A, Bowen M, Jara N, Terreros G, Robles L, Delano PH (2015) The olivocochlear reflex strength and cochlear sensitivity are independently modulated by auditory cortex microstimulation. J Assoc Res Otolaryngol 16:223–240Google Scholar
  40. Encina-Llamas G, Aravindakshan P, Harte JM, Dau T, Kujawa SG, Shinn-Cunningham B, Epp B (2017) Hidden hearing loss with envelope following responses (EFRs): the off-frequency problem. ARO Abstracts 40:4Google Scholar
  41. Fan L, Carney LH (2017) Neural responses in the inferior colliculus to diotic tone-in-noise stimuli support detection based on envelope and neural fluctuation, Abstract, Association for Research in Otolaryngology 40:250Google Scholar
  42. Fant G (1960) Acoustic theory of speech perception. Mouton, The HagueGoogle Scholar
  43. Fettiplace R, Ricci AJ (2006) Mechanoelectrical transduction in auditory hair cells. In: Eatock RA, Fay RR (eds) Vertebrate hair cells. Springer, New York, pp 154–203Google Scholar
  44. Florentine M, Buus SR (1981) An excitation-pattern model for intensity discrimination. J Acoust Soc Am 70:1646–1654Google Scholar
  45. Florentine M, Buus SR, Mason CR (1987) Level discrimination as a function of level for tones from 0.25 to 16 kHz. J Acoust Soc Am 81:1528–1541Google Scholar
  46. Forrest TG, Green DM (1987) Detection of partially filled gaps in noise and the temporal modulation transfer function. J Acoust Soc Am 82:1933–1943Google Scholar
  47. Freyman RL, Griffin AM, Oxenham AJ (2012) Intelligibility of whispered speech in stationary and modulated noise maskers. J Acoust Soc Am 132:2514–2523Google Scholar
  48. Fuente A (2015) The olivocochlear system and protection from acoustic trauma: a mini literature review. Front Syst Neurosci 9(94):1–6Google Scholar
  49. Furman AC, Kujawa SG, Liberman MC (2013) Noise-induced cochlear neuropathy is selective for fibers with low spontaneous rates. J Neurophysiol 110:577–586Google Scholar
  50. Gai Y, Carney LH (2006) Temporal measures and neural strategies for detection of tones in noise based on responses in anteroventral cochlear nucleus. J Neurophysiol 96:2451–2464Google Scholar
  51. Gai Y, Carney LH (2008) Influence of inhibitory inputs on rate and timing of responses in the anteroventral cochlear nucleus. J Neurophysiol 99:1077–1095Google Scholar
  52. Ghoshal S, Kim DO (1996) Marginal shell of the anteroventral cochlear nucleus: intensity coding in single units of the unanesthetized, decerebrate cat. Neurosci Lett 205:71–74Google Scholar
  53. Green DM (1988) Profile analysis: auditory intensity discrimination (no. 13). Oxford University Press, OxfordGoogle Scholar
  54. Guinan JJ (2011) Physiology of the medial and lateral olivocochlear systems. In: Ryugo DK, Fay RR, Popper AN (eds) Auditory and vestibular efferents. Springer, New York, pp 39–81Google Scholar
  55. Guinan Jr JJ (1996) Physiology of olivocochlear efferents. In: Dallos P, Fay RR (eds) The cochlea. Springer, New York, pp 435–502Google Scholar
  56. Gummer M, Yates GK, Johnstone BM (1988) Modulation transfer function of efferent neurones in the guinea pig cochlea. Hear Res 36:41–51Google Scholar
  57. Harrison JM, Howe ME (1974) Anatomy of the afferent auditory nervous system of mammals. In: Keidel WD, Neff WD (eds) Auditory system. Springer, Berlin Heidelberg, pp 283–336Google Scholar
  58. Heinz MG, Colburn HS, Carney LH (2001a) Evaluating auditory performance limits: I. One-parameter discrimination using a computational model for the auditory nerve. Neural Comput 13:2273–2316Google Scholar
  59. Heinz MG, Colburn HS, Carney LH (2001b) Rate and timing cues associated with the cochlear amplifier: level discrimination based on monaural cross-frequency coincidence detection. J Acoust Soc Am 110:2065–2084Google Scholar
  60. Helmholtz HV (1909) In: JPC S (ed) Physiological optics, vol 3. Optical Society of America, Washington, DCGoogle Scholar
  61. Henry KS, Kale S, Heinz MG (2014) Noise-induced hearing loss increases the temporal precision of complex envelope coding by auditory-nerve fibers. Front Syst Neurosci 8:1–10Google Scholar
  62. Henry KS, Abrams KS, Forst J, Mender MJ, Neilans EG, Idrobo F, Carney LH (2017) Midbrain synchrony to envelope structure supports behavioral sensitivity to single-formant vowel-like sounds in noise. J Assoc Res Otolaryngol 18:165–181Google Scholar
  63. Hienz RD, Stiles P, May BJ (1998) Effects of bilateral olivocochlear lesions on vowel formant discrimination in cats. Hear Res 116:10–20Google Scholar
  64. Hillenbrand J, Getty LA, Clark MJ, Wheeler K (1995) Acoustic characteristics of American English vowels. J Acoust Soc Am 97:3099–3111Google Scholar
  65. Hirsh IJ, Davis H, Silverman SR, Reynolds EG, Eldert E, Benson RW (1952) Development of materials for speech audiometry. Journal of Speech and Hearing Disorders 17:321–337Google Scholar
  66. Huet A, Batrel C, Tang Y, Desmadryl G, Wang J, Puel JL, Bourien J (2016) Sound coding in the auditory nerve of gerbils. Hear Res 338:32–39Google Scholar
  67. Huffman RF, Henson OW (1990) The descending auditory pathway and acousticomotor systems: connections with the inferior colliculus. Brain Res Rev 15:295–323Google Scholar
  68. Jacewicz E, Fox RA, Salmons J (2007) Vowel duration in three American English dialects. American Speech 82:367–385Google Scholar
  69. Jackson BS, Carney LH (2005) The spontaneous-rate histogram of the auditory nerve can be explained by only two or three spontaneous rates and long-range dependence. J Assoc Res Otolaryngol 6:148–159Google Scholar
  70. Jenkins WM, Masterton RB (1982) Sound localization: effects of unilateral lesions in central auditory system. J Neurophysiol 47:987–1016Google Scholar
  71. Jennings SG, Strickland EA, Heinz MG (2009) Precursor effects on behavioral estimates of frequency selectivity and gain in forward masking. J Acoust Soc Am 125:2172–2181Google Scholar
  72. Jesteadt W, Schairer KS, Neff DL (2005) Effect of variability in level on forward masking and on increment detection. J Acoust Soc Am 118:325–337Google Scholar
  73. Johnson DH (1980) The relationship between spike rate and synchrony in responses of auditory-nerve fibers to single tones. J Acoust Soc Am 68:1115–1122Google Scholar
  74. Joris PX (2003) Interaural time sensitivity dominated by cochlea-induced envelope patterns. J Neurosci 23:6345–6350Google Scholar
  75. Joris PX, Yin TC (1992) Responses to amplitude-modulated tones in the auditory nerve of the cat. J Acoust Soc Am 91:215–232Google Scholar
  76. Joris PX, Schreiner CE, Rees A (2004) Neural processing of amplitude-modulated sounds. Physiol Rev 84:541–577Google Scholar
  77. Kale S, Heinz MG (2010) Envelope coding in auditory nerve fibers following noise-induced hearing loss. J Assoc Res Otolaryngol 11:657–673Google Scholar
  78. Kidd Jr G, Mason CR, Brantley MA, Owen GA (1989) Roving-level tone-in-noise detection. J Acoust Soc Am 86:1310–1317Google Scholar
  79. Kim DO, Zahorik P, Carney LH, Bishop BB, Kuwada S (2015) Auditory distance coding in rabbit midbrain neurons and human perception: monaural amplitude modulation depth as a cue. J Neurosci 35:5360–5372Google Scholar
  80. Kohlrausch A, Püschel D, Alphei H (1992) Temporal resolution and modulation analysis in models of the auditory system. The Auditory Processing of Speech: From Sounds to Words 10:85–98Google Scholar
  81. Kohlrausch A, Fassel R, van der Heijden M, Kortekaas R, van de Par S, Oxenham AJ, Püschel D (1997) Detection of tones in low-noise noise: further evidence for the role of envelope fluctuations. Acta Acustica United with Acustica 83:659–669Google Scholar
  82. Krishna BS, Semple MN (2000) Auditory temporal processing: responses to sinusoidally amplitude-modulated tones in the inferior colliculus. J Neurophysiol 84:255–273Google Scholar
  83. Kujawa SG, Liberman MC (2009) Adding insult to injury: cochlear nerve degeneration after “temporary” noise-induced hearing loss. J Neurosci 29:14077–14085Google Scholar
  84. Kujawa SG, Liberman MC (2015) Synaptopathy in the noise-exposed and aging cochlea: primary neural degeneration in acquired sensorineural hearing loss. Hear Res 330:191–199Google Scholar
  85. Langner G, Schreiner CE (1988) Periodicity coding in the inferior colliculus of the cat. I. Neuronal mechanisms. J Neurophysiol 60:1799–1822Google Scholar
  86. Leake PA, Snyder RL (1989) Topographic organization of the central projections of the spiral ganglion in cats. J Comp Neurol 281:612–629Google Scholar
  87. Lentz JJ, Richards VM, Matiasek MR (1999) Different auditory filter bandwidth estimates based on profile analysis, notched noise, and hybrid tasks. J Acoust Soc Am 106:2779–2792Google Scholar
  88. Liberman MC (1978) Auditory-nerve response from cats raised in a low-noise chamber. J Acoust Soc Am 63:442–455Google Scholar
  89. Liberman MC (1991) Central projections of auditory-nerve fibers of differing spontaneous rate. I. Anteroventral cochlear nucleus. J Comp Neurol 313:240–258Google Scholar
  90. Liberman MC, Kujawa SG (2017) Cochlear synaptopathy in acquired sensorineural hearing loss: manifestations and mechanisms. Hear Res 349:138–147. Google Scholar
  91. Lobarinas E, Salvi R, Ding D (2013) Insensitivity of the audiogram to carboplatin induced inner hair cell loss in chinchillas. Hear Res 302:113–120Google Scholar
  92. Lopez-Poveda EA (2014) Why do I hear but not understand? Stochastic undersampling as a model of degraded neural encoding of speech. Front Neurosci 8:1–7Google Scholar
  93. Lopez-Poveda EA, Eustaquio-Martín A (2006) A biophysical model of the inner hair cell: the contribution of potassium currents to peripheral auditory compression. J Assoc Res Otolaryngol 7:218–235Google Scholar
  94. Lowen SB, Teich MC (1996) The periodogram and Allan variance reveal fractal exponents greater than unity in auditory-nerve spike trains. J Acoust Soc Am 99:3585–3591Google Scholar
  95. Lyzenga J, Horst JW (1997) Frequency discrimination of stylized synthetic vowels with a single formant. J Acoust Soc Am 102:1755–1767Google Scholar
  96. Maison S, Micheyl C, Collet L (1999) Sinusoidal amplitude modulation alters contralateral noise suppression of evoked otoacoustic emissions in humans. Neuroscience 91:133–138Google Scholar
  97. Manis PB, Xie R, Wang Y, Marrs GS, Spirou GA (2012) The endbulbs of held. In: Trussell L, Popper A, Fay R (eds) Synaptic mechanisms in the auditory system. Springer handbook of auditory research, vol 41. Springer, New York, pp 61–93Google Scholar
  98. Mao J, Carney LH (2015) Tone-in-noise detection using envelope cues: comparison of signal-processing-based and physiological models. J Assoc Res Otolaryngol 16:121–133Google Scholar
  99. Mao J, Vosoughi A, Carney LH (2013) Predictions of diotic tone-in-noise detection based on a nonlinear optimal combination of energy, envelope, and fine-structure cues. J Acoust Soc Am 134:396–406Google Scholar
  100. May BJ, McQuone SJ (1995) Effects of bilateral olivocochlear lesions on pure-tone intensity discrimination in cats. Audit Neurosci 1:385–400Google Scholar
  101. May BJ, Sachs MB (1992) Dynamic range of neural rate responses in the ventral cochlear nucleus of awake cats. J Neurophysiol 68:1589–1602Google Scholar
  102. May BJ, Budelis J, Niparko JK (2004) Behavioral studies of the olivocochlear efferent system: learning to listen in noise. Arch Otolaryngol Head Neck Surg 130:660–664.Google Scholar
  103. McGill WJ, Goldberg JP (1968) A study of the near-miss involving Weber’s law and pure-tone intensity discrimination. Atten Percept Psychophys 4:105–109Google Scholar
  104. Mellott JG, Bickford ME, Schofield BR (2014) Descending projections from auditory cortex to excitatory and inhibitory cells in the nucleus of the brachium of the inferior colliculus. Front Syst Neurosci 8(188):1–15Google Scholar
  105. Micheyl C, Maison S, Carlyon RP, Andéol G, Collet L (1999) Contralateral suppression of transiently evoked otoacoustic emissions by harmonic complex tones in humans. J Acoust Soc Am 105:293–305Google Scholar
  106. Miller RL, Schilling JR, Franck KR, Young ED (1997) Effects of acoustic trauma on the representation of the vowel /ε/ in cat auditory nerve fibers. J Acoust Soc Am 101:3602–3616Google Scholar
  107. Millman RE, Mattys SL, Gouws AD, Prendergast G (2017) Magnified neural envelope coding predicts deficits in speech perception in noise. J Neurosci 37(32):7727–7736. Google Scholar
  108. Moore BC (2012) An introduction to the psychology of hearing. Brill, LeidenGoogle Scholar
  109. Moore BC, Glasberg BR (1993) Simulation of the effects of loudness recruitment and threshold elevation on the intelligibility of speech in quiet and in a background of speech. J Acoust Soc Am 94:2050–2062Google Scholar
  110. Nayagam DA, Clarey JC, Paolini AG (2005) Powerful, onset inhibition in the ventral nucleus of the lateral lemniscus. J Neurophysiol 94:1651–1654Google Scholar
  111. Nelson PC, Carney LH (2004) A phenomenological model of peripheral and central neural responses to amplitude-modulated tones. J Acoust Soc Am 116(4):2173–2186Google Scholar
  112. Nelson PC, Carney LH (2007) Neural rate and timing cues for detection and discrimination of amplitude-modulated tones in the awake rabbit inferior colliculus. J Neurophysiol 97:522–539Google Scholar
  113. Nilsson M, Soli SD, Sullivan JA (1994) Development of the hearing in noise test for the measurement of speech reception thresholds in quiet and in noise. J Acoust Soc Am 95:1085–1099Google Scholar
  114. Oertel D, Wu SH, Garb MW, Dizack C (1990) Morphology and physiology of cells in slice preparations of the posteroventral cochlear nucleus of mice. J Comp Neurol 295:136–154Google Scholar
  115. Olsen WO (1998) Average speech levels and spectra in various speaking/listening conditions: a summary of the Pearson, Bennett, & Fidell (1977) report. Am J Audiol 7:21–25Google Scholar
  116. Oxenham AJ (2016) Predicting the perceptual consequences of hidden hearing loss. Trends in Hearing 20:1–6Google Scholar
  117. Oxenham AJ, Wojtczak M (2016) Predicting effects of hidden hearing loss using signal detection theory. J Acoust Soc Am 140:3150–3150Google Scholar
  118. Palmer AR, Wallace MN, Arnott RH, Shackleton TM (2003) Morphology of physiologically characterised ventral cochlear nucleus stellate cells. Exp Brain Res 153:418–426Google Scholar
  119. Patterson RD, Moore BCJ (1986) Auditory filters and excitation patterns as representations of frequency resolution. In: Moore BCJ (ed) Frequency selectivity in hearing. Academic, London, pp 123–177Google Scholar
  120. Pickett JM (1956) Effects of vocal force on the intelligibility of speech sounds. J Acoust Soc Am 28:902–905Google Scholar
  121. Pierscionek BK (1993) What we know and understand about presbyopia. Clin Exp Optom 76:83–90Google Scholar
  122. Plack CJ, Barker D, Prendergast G (2014) Perceptual consequences of “hidden” hearing loss. Trends Hear 18:1–11Google Scholar
  123. Plack CJ, Léger A, Prendergast G, Kluk K, Guest H, Munro KJ (2016) Toward a diagnostic test for hidden hearing loss. Trends Hear 20:1–9Google Scholar
  124. Rao A, Carney LH (2014) Speech enhancement for listeners with hearing loss based on a model for vowel coding in the auditory midbrain. IEEE Trans Biomed Eng 61:2081–2091Google Scholar
  125. Rees A, Langner G (2005) Temporal coding in the auditory midbrain. In: Winer JA, Schreiner CE (eds) The inferior colliculus. Springer, New York, pp 346–376Google Scholar
  126. Remez RE, Rubin PE, Pisoni DB, Carrell TD (1981) Speech perception without traditional speech cues. Science 212:947–949Google Scholar
  127. Rhode WS, Greenberg S (1992) Physiology of the cochlear nuclei. In: Popper AN, Fay RR (eds) The mammalian auditory pathway: neurophysiology. Springer, New York, pp 94–152Google Scholar
  128. Rhode WS, Greenberg S (1994) Encoding of amplitude modulation in the cochlear nucleus of the cat. J Neurophysiol 71:1797–1825Google Scholar
  129. Rhode WS, Oertel D, Smith PH (1983) Physiological response properties of cells labeled intracellularly with horseradish peroxidase in cat ventral cochlear nucleus. J Comp Neurol 213:448–463Google Scholar
  130. Richards VM (1992) The detectability of a tone added to narrow bands of equal-energy noise. J Acoust Soc Am 91:3424–3435Google Scholar
  131. Roberts WM, Rutherford MA (2008) Linear and nonlinear processing in hair cells. J Exp Biol 211:1775–1780Google Scholar
  132. Ruggles DR, Freyman RL, Oxenham AJ (2014) Influence of musical training on understanding voiced and whispered speech in noise. PLoS One 9:e86980Google Scholar
  133. Russell IJ, Sellick PM (1983) Low-frequency characteristics of intracellularly recorded receptor potentials in guinea-pig cochlear hair cells. J Physiol 338:179–206Google Scholar
  134. Russell IJ, Richardson GP, Cody AR (1986) Mechanosensitivity of mammalian auditory hair cells in vitro. Nature 321:517–519Google Scholar
  135. Ryugo DK (2008) Projections of low spontaneous rate, high threshold auditory nerve fibers to the small cell cap of the cochlear nucleus in cats. Neuroscience 154:114–126Google Scholar
  136. Ryugo DK, Sento S (1991) Synaptic connections of the auditory nerve in cats: relationship between endbulbs of held and spherical bushy cells. J Comp Neurol 305:35–48Google Scholar
  137. Sachs MB, Young ED (1979) Encoding of steady-state vowels in the auditory nerve: representation in terms of discharge rate. J Acoust Soc Am 66:470–479Google Scholar
  138. Sachs MB, Voigt HF, Young ED (1983) Auditory nerve representation of vowels in background noise. J Neurophysiol 50:27–45Google Scholar
  139. Sachs MB, Bruce IC, Miller RL, Young ED (2002) Biological basis of hearing-aid design. Ann Biomed Eng 30:157–168Google Scholar
  140. Sachs MB, May BJ, Le Prell GS, Hienz RD (2006) Adequacy of auditory-nerve rate representations of vowels: comparison with behavioral measures in cat. In: Greenberg S, Ainsworth W (eds) Listening to speech: an auditory perspective. Lawrence Erlbaum, Mahwah, pp 115–127Google Scholar
  141. Schaette R, McAlpine D (2011) Tinnitus with a normal audiogram: physiological evidence for hidden hearing loss and computational model. J Neurosci 31:13452–13457Google Scholar
  142. Schalk TB, Sachs MB (1980) Nonlinearities in auditory-nerve fiber responses to bandlimited noise. J Acoust Soc Am 67:903–913Google Scholar
  143. Schofield BR (2011) Central descending auditory pathways. In: Ryugo DK, Fay RR, Popper AN (eds) Auditory and vestibular Efferents. Springer, New York, pp 261–290Google Scholar
  144. Schofield BR, Cant NB (1997) Ventral nucleus of the lateral lemniscus in guinea pigs: cytoarchitecture and inputs from the cochlear nucleus. J Comp Neurol 379:363–385Google Scholar
  145. Schofield BR, Cant NB (1999) Descending auditory pathways: projections from the inferior colliculus contact superior olivary cells that project bilaterally to the cochlear nuclei. J Comp Neurol 409:210–223Google Scholar
  146. Sewell WF (1984) Furosemide selectively reduces one component in rate-level functions from auditory-nerve fibers. Hear Res 15:69–72Google Scholar
  147. Sherman SM, Spear PD (1982) Organization of visual pathways in normal and visually deprived cats. Physiol Rev 62:738–855Google Scholar
  148. Siebert WM (1965) Some implications of the stochastic behavior of primary auditory neurons. Kybernetika 2:206–215Google Scholar
  149. Sinex DG (2008) Responses of cochlear nucleus neurons to harmonic and mistuned complex tones. Hear Res 238:39–48Google Scholar
  150. Sinex DG, Sabes JH, Li H (2002) Responses of inferior colliculus neurons to harmonic and mistuned complex tones. Hear Res 168:150–162Google Scholar
  151. Sinex DG, Guzik H, Li H, Sabes JH (2003) Responses of auditory nerve fibers to harmonic and mistuned complex tones. Hear Res 182:130–139Google Scholar
  152. Smith RL, Brachman ML (1982) Adaptation in auditory-nerve fibers: a revised model. Biol Cybern 44:107–120Google Scholar
  153. Smith DW, Keil A (2015) The biological role of the medial olivocochlear efferents in hearing: separating evolved function from exaptation. Front Syst Neurosci 9(12):1–6Google Scholar
  154. Smith PH, Rhode WS (1989) Structural and functional properties distinguish two types of multipolar cells in the ventral cochlear nucleus. J Comp Neurol 282:595–616Google Scholar
  155. Smith RL, Zwislocki JJ (1975) Short-term adaptation and incremental responses of single auditory-nerve fibers. Biol Cybern 17:169–182Google Scholar
  156. Smith RL, Brachman ML, Frisina RD (1985) Sensitivity of auditory-nerve fibers to changes in intensity: a dichotomy between decrements and increments. J Acoust Soc Am 78:1310–1316Google Scholar
  157. Smith PH, Massie A, Joris PX (2005) Acoustic stria: anatomy of physiologically characterized cells and their axonal projection patterns. J Comp Neurol 482:349–371Google Scholar
  158. Spirou GA, Brownell WE, Zidanic M (1990) Recordings from cat trapezoid body and HRP labeling of globular bushy cell axons. J Neurophysiol 63:1169–1190Google Scholar
  159. Spirou GA, Rager J, Manis PB (2005) Convergence of auditory-nerve fiber projections onto globular bushy cells. Neuroscience 136:843–863Google Scholar
  160. Strickland EA (2008) The relationship between precursor level and the temporal effect. J Acoust Soc Am 123:946–954Google Scholar
  161. Strickland EA, Krishnan LA (2005) The temporal effect in listeners with mild to moderate cochlear hearing impairment. J Acoust Soc Am 118:3211–3217Google Scholar
  162. Studebaker GA, Sherbecoe RL, McDaniel DM, Gwaltney CA (1999) Monosyllabic word recognition at higher-than-normal speech and noise levels. J Acoust Soc Am 105:2431–2444Google Scholar
  163. Swaminathan J, Goldsworthy RL, Zurek PM, Léger AC, Braida LD (2014) Preliminary evaluation of a physiologically inspired signal processing strategy for cochlear implants. J Acoust Soc Am 135:2410–2410Google Scholar
  164. Teich MC, Lowen SB (1994) Fractal patterns in auditory nerve-spike trains. IEEE Engineering in Medicine and Biology Magazine 13:197–202Google Scholar
  165. Teich MC, Johnson DH, Kumar AR, Turcott RG (1990) Rate fluctuations and fractional power-law noise recorded from cells in the lower auditory pathway of the cat. Hear Res 46:41–52Google Scholar
  166. Terreros G, Delano PH (2015) Corticofugal modulation of peripheral auditory responses. Front Syst Neurosci 9(134):1–8Google Scholar
  167. Thompson AM, Thompson GC (1993) Relationship of descending inferior colliculus projections to olivocochlear neurons. J Comp Neurol 335:402–412Google Scholar
  168. Tsuji J, Liberman MC (1997) Intracellular labeling of auditory nerve fibers in guinea pig: central and peripheral projections. J Comp Neurol 381:188–202Google Scholar
  169. Umeda N (1977) Consonant duration in American English. J Acoust Soc Am 61:846–858Google Scholar
  170. van der Heijden M, Kohlrausch A (1995) The role of envelope fluctuations in spectral masking. J Acoust Soc Am 97:1800–1807Google Scholar
  171. Victor JD, Nirenberg S (2013) Spike trains as event sequences: fundamental implications. In: DiLorenzo PM, Victor JD (eds) Spike timing: mechanisms and function. CRC Press, Boca Raton, pp 3–33Google Scholar
  172. Viemeister NF (1988) Intensity coding and the dynamic range problem. Hear Res 34:267–274Google Scholar
  173. Warr WB (1992) Organization of olivocochlear efferent systems in mammals. In: Webster DB, Fay R (eds) The mammalian auditory pathway: neuroanatomy. Springer, New York, pp 410–448Google Scholar
  174. Warren EH, Liberman MC (1989) Effects of contralateral sound on auditory-nerve responses. I. Contributions of cochlear efferents. Hear Res 37:89–104Google Scholar
  175. Weale RA (1962) Presbyopia. Br J Ophthalmol 46:660–668Google Scholar
  176. Wen B, Wang GI, Dean I, Delgutte B (2009) Dynamic range adaptation to sound level statistics in the auditory nerve. J Neurosci 29:13797–13808Google Scholar
  177. Wilson BS, Dorman MF (2008) Cochlear implants: a remarkable past and a brilliant future. Hear Res 242:3–21Google Scholar
  178. Winslow RL, Sachs MB (1988) Single-tone intensity discrimination based on auditory-nerve rate responses in backgrounds of quiet, noise, and with stimulation of the crossed olivocochlear bundle. Hear Res 35:165–189Google Scholar
  179. Winslow RL, Barta PE, Sachs MB (1987) Rate coding in the auditory nerve. In: Yost WA, Watson CS (eds) Auditory processing of complex sounds. Lawrence Erlbaum, Hillsdale, pp 212–224Google Scholar
  180. Winter IM, Palmer AR (1991) Intensity coding in low-frequency auditory-nerve fibers of the guinea pig. J Acoust Soc Am 90:1958–1967Google Scholar
  181. Winter IM, Robertson D, Yates GK (1990) Diversity of characteristic frequency rate-intensity functions in guinea pig auditory nerve fibres. Hear Res 45:191–202Google Scholar
  182. Wong S, Henry KS (2018) Effects of auditory-nerve damage on behavioral tone detection by budgerigars in quiet and in noise. ARO Abstracts 41:13Google Scholar
  183. Yates GK (1990) Basilar membrane nonlinearity and its influence on auditory nerve rate-intensity functions. Hear Res 50:145–162Google Scholar
  184. Yates G, Johnstone B, Patuzzi R, Robertson D (1992) Mechanical preprocessing in the mammalian cochlea. Trends Neurosci 15(2):57–61Google Scholar
  185. Ye Y, Machado DG, Kim DO (2000) Projection of the marginal shell of the anteroventral cochlear nucleus to olivocochlear neurons in the cat. J Comp Neurol 420:127–138Google Scholar
  186. Young ED, Davis KA (2002) Circuitry and function of the dorsal cochlear nucleus. In: Oertel D, Fay RR, Popper AN (eds) Integrative functions in the mammalian auditory pathway. Springer, New York, pp 160–206Google Scholar
  187. Zeddies DG, Siegel JH (2004) A biophysical model of an inner hair cell. J Acoust Soc Am 116:426–441Google Scholar
  188. Zhong Z, Henry KS, Heinz MG (2014) Sensorineural hearing loss amplifies neural coding of envelope information in the central auditory system of chinchillas. Hear Res 309:55–62Google Scholar
  189. Zilany MSA, Bruce IC (2007) Representation of the vowel /ε/ in normal and impaired auditory nerve fibers: model predictions of responses in cats. J Acoust Soc Am 122:402–417Google Scholar
  190. Zilany MSA, Carney LH (2010) Power-law dynamics in an auditory-nerve model can account for neural adaptation to sound-level statistics. J Neurosci 30:10380–10390Google Scholar
  191. Zilany MS, Bruce IC, Nelson PC, Carney LH (2009) A phenomenological model of the synapse between the inner hair cell and auditory nerve: long-term adaptation with power-law dynamics. J Acoust Soc Am 126:2390–2412Google Scholar
  192. Zilany MS, Bruce IC, Carney LH (2014) Updated parameters and expanded simulation options for a model of the auditory periphery. J Acoust Soc Am 135:283–286Google Scholar
  193. Zwicker E (1965) Temporal effects in simultaneous masking by white‐noise bursts. J Acoust Soc Am 37:653–663Google Scholar

Copyright information

© Association for Research in Otolaryngology 2018

Authors and Affiliations

  1. 1.Departments of Biomedical Engineering, Neuroscience, and Electrical & Computer Engineering, Del Monte Institute for NeuroscienceUniversity of RochesterRochesterUSA

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