Skip to main content
SpringerLink
Log in

Comparing Distortion Product Otoacoustic Emissions to Intracochlear Distortion Products Inferred from a Noninvasive Assay

  • Research Article
  • Published:
Journal of the Association for Research in Otolaryngology Aims and scope Submit manuscript

Abstract

The behavior of intracochlear distortion products (iDPs) was inferred by interacting a probe tone (f3) with the iDP of interest to produce a “secondary” distortion product otoacoustic emission termed DPOAE2ry. Measures of the DPOAE2ry were then used to deduce the properties of the iDP. This approach was used in alert rabbits and anesthetized gerbils to compare ear-canal 2f1-f2 and 2f2-f1 DPOAE f2/f1 ratio functions, level/phase (L/P) maps, and interference-response areas (IRAs) to their simultaneously collected DPOAE2ry counterparts. These same measures were also collected in a human volunteer to demonstrate similarities with their laboratory animal counterparts and their potential applicability to humans. Results showed that DPOAEs and inferred iDPs evidenced distinct behaviors and properties. That is, DPOAE ratio functions elicited by low-level primaries peaked around an f2/f1 = 1.21 or 1.25, depending on species, while the corresponding inferred iDP ratio functions peaked at f2/f1 ratios of ~1. Additionally, L/P maps showed rapid phase variation with DPOAE frequency (fdp) for the narrow-ratio 2f1-f2 and all 2f2-f1 DPOAEs, while the corresponding DPOAE2ry measures evidenced relatively constant phases. Common features of narrow-ratio DPOAE IRAs, such as large enhancements for interference tones (ITs) presented above f2, were not present in DPOAE2ry IRAs. Finally, based on prior experiments in gerbils, the behavior of the iDP directly measured in intracochlear pressure was compared to the iDP inferred from the DPOAE2ry and found to be similar. Together, these findings are consistent with the notion that under certain conditions, ear-canal DPOAEs provide poor representations of iDPs and thus support a “beamforming” hypothesis. According to this concept, distributed emission components directed toward the ear canal from the f2 and basal to f2 regions can be of differing phases and thus cancel, while these same components directed toward fdp add in phase.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

FIG. 1
FIG. 2
FIG. 3
FIG. 4
FIG. 5

Similar content being viewed by others

Abbreviations

A/D:

Analog-to-digital

BM:

Basilar membrane

CF:

Characteristic frequency

CP:

Compression pressure

CT:

Combination tone

DP:

Distortion product

DP-gram:

DPOAE level as a function of f2 primary-tone frequencies

DPOAE:

Ear-canal distortion product otoacoustic emission

DPOAE2ry :

A secondary DPOAE produced by interacting a DPOAE at 2f1-f2 or 2f2-f1 with a third tone (f3)

DSP:

Digital signal processor

EQPiDP :

Equivalent ear-canal pressure that produces a DPOAE2ry

f1 and f2 :

Lower and upper frequency primary tones, respectively

f2/f1 :

Ratio describing the frequency separation of f1 and f2

fdp :

Distortion product frequency

iDP:

Intracochlear distortion product

iDP2ry :

A secondary intracochlear DP produced by interacting f3 with a DP

IACUC:

Institutional Animal Care and Use Committee

IRA:

Interference-response area

IRB:

Institutional Review Board

IT:

Interference tone

L/P map:

level/phase map

L1 and L2 :

Levels of f1 and f2, respectively

μm:

Micrometer or micron

NF:

Noise floor

oct:

Octave

OHC:

Outer hair cell

PST :

Intracochlear pressure in scala tympani

PC:

Personal computer

SPL:

Sound pressure level

TW:

Traveling wave

VA:

Veterans Affairs

Referrences

  • Allen JB, Fahey PF (1993) A second cochlear-frequency map that correlates distortion product and neural tuning measurements. J Acoust Soc Am 94:809–816

    Article  CAS  PubMed  Google Scholar 

  • Avan P, Buki B, Petit C (2013) Auditory distortions: origins and functions. Physiol Rev 93:1563–1619. doi:10.1152/physrev.00029.2012

    Article  CAS  PubMed  Google Scholar 

  • Cooper NP, Rhode WS (1997) Mechanical responses to two-tone distortion products in the apical and basal turns of the mammalian cochlea. J Neurophysiol 78:261–270

    CAS  PubMed  Google Scholar 

  • de Boer E, Nuttall AL, Hu N, Zou Y, Zheng J (2005) The Allen-Fahey experiment extended. J Acoust Soc Am 117:1260–1266

    Article  PubMed  Google Scholar 

  • Dong W, Olson ES (2005) Two-tone distortion in intracochlear pressure. J Acoust Soc Am 117:2999–3015

    Article  PubMed  PubMed Central  Google Scholar 

  • Dong W, Olson ES (2006) Middle ear forward and reverse transmission in gerbil. J Neurophysiol 95:2951–2961

    Article  PubMed  Google Scholar 

  • Dong W, Olson ES (2008) Supporting evidence for reverse cochlear traveling waves. J Acoust Soc Am 123:222–240. doi:10.1121/1.2816566

    Article  CAS  PubMed  Google Scholar 

  • Dong W, Olson ES (2013) Detection of cochlear amplification and its activation. Biophys J 105:1067–1078. doi:10.1016/j.bpj.2013.06.049

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fahey PF, Stagner BB, Lonsbury-Martin BL, Martin GK (2000) Nonlinear interactions that could explain distortion product interference response areas. J Acoust Soc Am 108:1786–1802

    Article  CAS  PubMed  Google Scholar 

  • Fahey PF, Stagner BB, Martin GK (2006) Mechanism for bandpass frequency characteristic in distortion product otoacoustic emission generation. J Acoust Soc Am 119:991–996

    Article  CAS  PubMed  Google Scholar 

  • Goldstein JL, Buchsbaum G, Furst M (1978) Compatibility between psychophysical and physiological measurements of aural combination tones. J Acoust Soc Am 63:474–485

    Article  CAS  PubMed  Google Scholar 

  • Harris FP, Lonsbury-Martin BL, Stagner BB, Coats AC, Martin GK (1989) Acoustic distortion products in humans: systematic changes in amplitude as a function of f2/f1 ratio. J Acoust Soc Am 85:220–229

    Article  CAS  PubMed  Google Scholar 

  • He W, Ren T (2013) Basilar membrane vibration is not involved in the reverse propagation of otoacoustic emissions. Sci Rep 3:1874–1880

    CAS  PubMed  PubMed Central  Google Scholar 

  • Huang S, Olson ES (2011) Auditory nerve excitation via a non-traveling wave mode of basilar membrane motion. J Assoc Res Otolaryngol 12:559–575

    Article  PubMed  PubMed Central  Google Scholar 

  • Johnson TA, Neely ST, Garner CA, Gorga MP (2006) Influence of primary-level and primary-frequency ratios on human distortion product otoacoustic emissions. J Acoust Soc Am 119:418–428

    Article  PubMed  PubMed Central  Google Scholar 

  • Knight RD, Kemp DT (2000) Indications of different distortion product otoacoustic emission mechanisms from a detailed f1, f2 area study. J Acoust Soc Am 107:457–473

    Article  CAS  PubMed  Google Scholar 

  • Knight RD, Kemp DT (2001) Wave and place fixed DPOAE maps of the human ear. J Acoust Soc Am 109:1513–1525

    Article  CAS  PubMed  Google Scholar 

  • Martin GK, Jassir D, Stagner BB, Whitehead ML, Lonsbury-Martin BL (1998) Locus of generation for the 2f1-f2 vs 2f2-f1 distortion-product otoacoustic emissions in normal-hearing humans revealed by suppression tuning, onset latencies, and amplitude correlations. J Acoust Soc Am 103:1957–1971

    Article  CAS  PubMed  Google Scholar 

  • Martin GK, Stagner BB, Jassir D, Telischi FF, Lonsbury-Martin BL (1999) Suppression and enhancement of distortion-product otoacoustic emissions by interference tones above f2: I. basic findings in rabbits. Hear Res 136:105–123

    Article  CAS  PubMed  Google Scholar 

  • Martin GK, Villasuso EI, Stagner BB, Lonsbury-Martin BL (2003) Suppression and enhancement of distortion-product otoacoustic emissions by an interference tone above f2: II. findings in humans. Hear Res 177:111–122

    Article  PubMed  Google Scholar 

  • Martin GK, Stagner BB, Fahey PF, Lonsbury-Martin BL (2009) Steep and shallow phase gradient DPOAEs arising basal to the primary tones. J Acoust Soc Am 125:EL85–EL92

    PubMed  Google Scholar 

  • Martin GK, Stagner BB, Lonsbury-Martin BL (2010) Evidence for basal distortion-product otoacoustic emission components. J Acoust Soc Am 127:2955–2972

    Article  PubMed  PubMed Central  Google Scholar 

  • Martin GK, Stagner BB, Chung Y-S, Lonsbury-Martin BL (2011) Characterizing distortion-product otoacoustic emission components across four species. J Acoust Soc Am 129:3090–3103

    Article  PubMed  PubMed Central  Google Scholar 

  • Martin GK, Stagner BB, Lonsbury-Martin BL (2013) Time-domain demonstration of distributed distortion product otoacoustic emission components. J Acoust Soc Am 134:342–355

    Article  PubMed  PubMed Central  Google Scholar 

  • Olson ES (1998) Observing middle and inner ear mechanics with novel intracochlear pressure sensors. J Acoust Soc Am 103:3445–3463

    Article  CAS  PubMed  Google Scholar 

  • Olson ES (1999) Direct measurement of intra-cochlear pressure waves. Nature 402:526–529

    Article  CAS  PubMed  Google Scholar 

  • Probst R, Lonsbury-Martin BL, Martin GK (1991) A review of otoacoustic emissions. J Acoust Soc Am 89:2027–2067

    Article  CAS  PubMed  Google Scholar 

  • Ren T (2004) Reverse propagation of sound in the gerbil cochlea. Nat Neurosci 7:333–334

    Article  CAS  PubMed  Google Scholar 

  • Rhode WS (2007) Distortion product otoacoustic emissions and basilar membrane vibration in the 6–9 kHz region of sensitive chinchilla cochleae. J Acoust Soc Am 122:2725–2737

    Article  PubMed  Google Scholar 

  • Rhode WS, Cooper NP (1997) Two-tone suppression and distortion production on the basilar membrane in the hook region of cat and guinea pig cochleae. Hear Res 66:31–45

    Article  Google Scholar 

  • Robles L, Ruggero MA (2001) Mechanics of the mammalian cochlea. Physiol Rev 81:1305–1352

    CAS  PubMed  PubMed Central  Google Scholar 

  • Robles L, Ruggero MA, Rich NC (1997) Two-tone distortion on the basilar membrane of the chinchilla cochlea. J Neurophysiol 77:2385–2399

    CAS  PubMed  PubMed Central  Google Scholar 

  • Shera CA (2003) Wave interference in the generation of reflection- and distortion-source emissions. In: Gummer AW (ed) Biophysics of the cochlea: molecules to models. World Sci Pr, Singapore, pp 439–453

    Chapter  Google Scholar 

  • Shera CA, Guinan JJ (1999) Evoked otoacoustic emissions arise by two fundamentally different mechanisms: a taxonomy for mammalian otoacoustic emissions. J Acoust Soc Am 105:782–798

    Article  CAS  PubMed  Google Scholar 

  • Shera CA, Guinan JJ (2007) Cochlear traveling-wave amplification, suppression, and beamforming probed using noninvasive calibration of intracochlear distortion sources. J Acoust Soc Am 121:1003–1016

    Article  PubMed  Google Scholar 

  • Shera CA, Guinan JJ (2008) Mechanisms of mammalian otoacoustic emission. In: Manley GA, Fay RR, Popper AN (eds) Active processes and otoacoustic emissions. Springer, New York, pp 305–342

    Google Scholar 

  • Shera CA, Tubis A, Talmadge CL (2006) Four counter-arguments for slow-wave OAEs. In: Nuttall AL, Ren T, Gillespie P, Grosh K, de Boer E (eds) Auditory mechanisms: processes and models. World Sci Pr, Singapore, pp 449–457

    Chapter  Google Scholar 

  • Shera CA, Tubis A, Talmadge CL, de Boer E, Fahey PF, Guinan JJ (2007) Allen-Fahey and related experiments support the predominance of cochlear slow-wave otoacoustic emissions. J Acoust Soc Am 121:1564–1575

    Article  PubMed  Google Scholar 

  • Stagner BB, Meinke D, Lonsbury-Martin BL, Martin GK (2007) Group delay contour plots derived from DPOAE level/phase maps in normal hearing and noise-damaged humans. Assn Res Otolaryngol Abstr 30:177

    Google Scholar 

  • Stagner BB, Martin GK, Lonsbury-Martin BL (2014) The intracochlear DP-gram: a noninvasive assay of basilar membrane distortion products in noise-exposed rabbits. Assn Res Otolaryngol Abstr 37:63

    Google Scholar 

  • Whitehead ML, Lonsbury-Martin BL, Martin GK (1993) Measurement of 2f1-f2 excitation at the distortion-frequency place in the cochlea using ear-canal distortion products. Assn Res Otolaryngol Abstr 16:99

    Google Scholar 

  • Whitehead ML, McCoy MJ, Lonsbury-Martin BL, Martin GK (1995) Dependence of distortion-product otoacoustic emissions on primary levels in normal and impaired ears: I. Effects of decreasing L2 below L1. J Acoust Soc Am 97:2346–2358

    Article  CAS  PubMed  Google Scholar 

  • Whitehead ML, Stagner BB, Martin GK, Lonsbury-Martin BL (1996) Visualization of the onset of distortion-product otoacoustic emissions, and measurement of their latency. J Acoust Soc Am 100:1663–1679

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported in part by the US National Institutes of Health (National Institute on Deafness and Other Communication Disorders DC000613) and the US Department of Veterans Affairs (VA) (VA/Rehabilitative Research and Development C449R, C6212L). The authors thank Alisa Hetrick for the technical assistance. We also want to thank three anonymous reviewers for their thoughtful comments that undoubtedly improved the manuscript.

Author information

Authors and Affiliations

  1. Research Service, VA Loma Linda Healthcare System, 11201 Benton Street, Loma Linda, CA, 92357-1000, USA

    Glen K. Martin, Barden B. Stagner, Wei Dong & Brenda L. Lonsbury-Martin

  2. Department of Otolaryngology–Head and Neck Surgery, Loma Linda University Health, Loma Linda, CA, USA

    Glen K. Martin, Wei Dong & Brenda L. Lonsbury-Martin

Authors
  1. Glen K. Martin
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Barden B. Stagner
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Wei Dong
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Brenda L. Lonsbury-Martin
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Glen K. Martin.

Ethics declarations

Conflict of Interest

The authors declare that they have no conflicts of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Martin, G.K., Stagner, B.B., Dong, W. et al. Comparing Distortion Product Otoacoustic Emissions to Intracochlear Distortion Products Inferred from a Noninvasive Assay. JARO 17, 271–287 (2016). https://doi.org/10.1007/s10162-016-0552-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10162-016-0552-1

Keywords

Search

Navigation