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Journal of the Association for Research in Otolaryngology

Published in:

01-09-2007

Neural and Behavioral Sensitivity to Interaural Time Differences Using Amplitude Modulated Tones with Mismatched Carrier Frequencies

Authors: Deidra A. Blanks, Jason M. Roberts, Emily Buss, Joseph W. Hall, Douglas C. Fitzpatrick

Published in: Journal of the Association for Research in Otolaryngology | Issue 3/2007

Abstract

Bilateral cochlear implantation is intended to provide the advantages of binaural hearing, including sound localization and better speech recognition in noise. In most modern implants, temporal information is carried by the envelope of pulsatile stimulation, and thresholds to interaural time differences (ITDs) are generally high compared to those obtained in normal hearing observers. One factor thought to influence ITD sensitivity is the overlap of neural populations stimulated on each side. The present study investigated the effects of acoustically stimulating bilaterally mismatched neural populations in two related paradigms: rabbit neural recordings and human psychophysical testing. The neural coding of interaural envelope timing information was measured in recordings from neurons in the inferior colliculus of the unanesthetized rabbit. Binaural beat stimuli with a 1-Hz difference in modulation frequency were presented at the best modulation frequency and intensity as the carrier frequencies at each ear were varied. Some neurons encoded envelope ITDs with carrier frequency mismatches as great as several octaves. The synchronization strength was typically nonmonotonically related to intensity. Psychophysical data showed that human listeners could also make use of binaural envelope cues for carrier mismatches of up to 2–3 octaves. Thus, the physiological and psychophysical data were broadly consistent, and suggest that bilateral cochlear implants should provide information sufficient to detect envelope ITDs even in the face of bilateral mismatch in the neural populations responding to stimulation. However, the strongly nonmonotonic synchronization to envelope ITDs suggests that the limited dynamic range with electrical stimulation may be an important consideration for ITD encoding.

ANSI. American National Standards Specification for Audiometers. New York, American National Standards Institute, 1996.

Bala AD, Spitzer MW, et al. Prediction of auditory spatial acuity from neural images on the owl’s auditory space map. Nature. 424(6950):771–774, 2003.PubMedCrossRef

Batra R, Yin TC. Cross correlation by neurons of the medial superior olive: a reexamination. J. Assoc. Res. Otolaryngol. 5(3):238–252, 2004.PubMedCrossRef

Batra R, Kuwada S, et al. Sensitivity to interaural temporal disparities of low and high frequency neurons in the superior olivary complex. II. Coincidence detection. J. Neurophysiol. 78:1237–1247, 1997.PubMed

Bernstein LR, Trahiotis C. Lateralization of sinusoidally amplitude-modulated tones: Effects of spectral locus and temporal variation. J. Acoust. Soc. Am. 78:514–523, 1985.PubMedCrossRef

Colburn HS. Theory of binaural interaction based on auditory-nerve data. I. General strategy and preliminary results on interaural discrimination. J. Acoust. Soc. Am. 54:1458–1470, 1973.PubMedCrossRef

Dreyer A, Delgutte B. Phase locking of auditory-nerve fibers to the envelopes of high-frequency sounds: implications for sound localization. J Neurophysiol. 96(5):2327–2341, 2006.PubMedCrossRef

Fitzpatrick DC, Kuwada S. Tuning to interaural time differences across frequency. J. Neurosci. 21(13):4844–4851, 2001.PubMed

Fitzpatrick DC, Batra R, et al. A neuronal population code for sound localization. Nature. 388:871–874, 1997.PubMedCrossRef

Fitzpatrick DC., Kuwada SK, et al. Transformations in processing interaural time differences between the superior olivary complex and inferior colliculus: beyond the Jeffress model. Hear. Res. 168:79–89, 2002.PubMedCrossRef

Goldberg JM, Brown PB. Response of binaural neurons of dog superior olivary complex to dichotic tonal stimuli: some physiological mechanisms of sound localization. J. Neurophysiol. 32:613–636, 1969.PubMed

Henning GB. Detectability of interaural delay in high-frequency complex waveforms. J. Acoust. Soc. Am. 55:84–90, 1974.PubMedCrossRef

Jeffress LA. A place theory of sound localization. J. Comp. Physiol. Psychol. 41:35–39, 1948.

Joris PX. Interaural time sensitivity dominated by cochlea-induced envelope patterns. J. Neurosci. 23(15):6345–6350, 2003.PubMed

Joris PX, Yin TCT. Responses to amplitude-modulated tones in the auditory nerve of the cat. J. Acoust. Soc. Am. 91(1):215–232, 1992.PubMedCrossRef

Joris PX, Smith PH, Yin TCT. Coincidence detection in the auditory system: 50 years after Jeffress. Neuron 21:1235–1238, 1998.

Joris PX, Carney LH, et al. Enhancement of neural synchronization in the anteroventral cochlear nucleus. I. Responses to tones at the characteristic frequency. J. Neurophysiol. 71(3):1022–1036, 1994a.PubMed

Joris PX, Smith PH, et al. Enhancement of neural synchronization in the anteroventral cochlear nucleus. II. Responses in the tuning curve tail. J. Neurophysiol. 71(3):1037–1051, 1994b.PubMed

Joris PX, van de Sande B, et al. Auditory midbrain and nerve responses to sinusoidal variations in interaural correlation. J. Neurosci. 26(1):279–289, 2006.PubMedCrossRef

Kiss A, Majorossy K. Neuron morphology and synaptic architecture in the medial superior olivary nucleus. Exp. Brain Res. 52:315–327, 1983.PubMedCrossRef

Klumpp RG, Eady HR. Some measurements of interaural time difference thresholds. J. Acoust. Soc. Am. 28:859–860, 1957.CrossRef

Kohlrausch A. Comment on “Temporal modulation transfer functions in patients with cochlear implants” [J. Acoust. Soc. Am. 91,2156–2164 (1992)]. J. Acoust. Soc. Am. 93(3):1649–1652, 1993.PubMedCrossRef

Kollmeier B, Gilkey RH. Binaural forward and backward masking: evidence for sluggishness in binaural detection. J. Acoust. Soc. Am. 87(4):1709–1719, 1990.PubMedCrossRef

Kuwada S, Stanford TR, et al. Interaural phase sensitive units in the inferior colliculus of the unanesthetized rabbit. Effects of changing frequency. J. Neurophysiol. 57:1338–1360, 1987.PubMed

Langner G, Schreiner CE. Periodicity coding in the inferior colliculus of the cat. I. Neuronal mechanisms. J. Neurophysiol. 60(6):1799–1822, 1988.PubMed

Lawson DT, Wilson BS, et al. Bilateral cochlear implants controlled by a single speech processor. Am. J. Otol. 19(6):758–761, 1998.PubMed

Litovsky RY, Arcaroli J, et al. Effect of experience on sound localization and speech intelligibility in noise in adults and children with bilateral cochlear implants. J. Assoc. Res. Otolaryngol. Abstract 87, 2004.

Litovsky R, Parkinson A, et al. Simultaneous bilateral cochlear implantation in adults: a multicenter clinical study. Ear Hear. 27(6):714–731, 2006.PubMedCrossRef

Litvak L, Delgutte B, et al. Auditory nerve fiber responses to electric stimulation: modulated and unmodulated pulse trains. J. Acoust. Soc. Am. 110(1):368–379, 2001.PubMedCrossRef

Litvak LM, Delgutte B, et al. Improved temporal coding of sinusoids in electric stimulation of the auditory nerve using desynchronizing pulse trains. J. Acoust. Soc. Am. 114(4 Pt 1):2079–2098, 2003.PubMedCrossRef

Long CJ, Eddington DK, et al. Binaural sensitivity as a function of interaural electrode position with a bilateral cochlear implant user. J. Acoust. Soc. Am. 114(3):1565–1574, 2003.PubMedCrossRef

Majorossy K, Kiss A. Types of neurons and synaptic relations in the lateral superior olive of the cat: normal structure and experimental observations. Acta Morphol. Hung. 38(3–4):207–215, 1990.PubMed

Mardia KV, Jupp PE. Directional Statistics. New York, Wiley, 1999.

McAlpine D, Jiang D, et al. A neural code for low-frequency sound localization in mammals. Nat. Neurosci. 4(4):396–401, 2001.PubMedCrossRef

McFadden D, Pasanen EG. Binaural beats at high frequencies. Science. 190:394–396, 1975.PubMedCrossRef

Muller J, Schon F, et al. Speech understanding in quiet and noise in bilateral users of the MED-EL COMBI 40/40+ cochlear implant system. Ear Hear. 23(3):198–206, 2002.PubMedCrossRef

Neutzel JM, Hafter ER. Discrimination of interaural delays in complex waveforms: spectral effects. J. Acoust. Soc. Am. 69:1112–1118, 1981.CrossRef

Rose JE, Brugge JF, et al. Phase-locked response to low-frequency tones in single auditory nerve fibers of the squirrel monkey. J. Neurophysiol. 30(4):769–793, 1967.PubMed

Rubinstein JT, Wilson BS, et al. Pseudospontaneous activity: stochastic independence of auditory nerve fibers with electrical stimulation. Hear. Res. 127(1–2):108–118, 1999.PubMedCrossRef

Schoen F, Mueller J, et al. Sound localization and sensitivity to interaural cues in bilateral users of the Med-El Combi 40/40+cochlear implant system. Otol. Neurotol. 26(3):429–437, 2005.PubMedCrossRef

Shannon RV. Temporal modulation transfer functions in patients with cochlear implants. J. Acoust. Soc. Am. 91(4 Pt 1):2156–2164, 1992.PubMedCrossRef

Smith RL, Brachman ML. Response modulation of auditory-nerve fibers by AM stimuli: effects of average intensity. Hear. Res. 2:123–133, 1980.PubMedCrossRef

Stern RM, Colburn HS. Theory of binaural interaction based on auditory-nerve data IV. A model for subjective lateral position. J. Acoust. Soc. Am. 64:127–140, 1978.PubMedCrossRef

Strickland EA, Viemeister NF, et al. Within- versus cross-channel mechanisms in detection of envelope phase disparity. J. Acoust. Soc. Am. 86(6):2160–2166, 1989.PubMedCrossRef

Sutter ML, et al. Topography of intensity tuning in cat primary auditory cortex: single-neuron versus multiple-neuron recordings. J. Neurophysiol. 73(1):190–204, 1995.PubMed

van den Honert C, Stypulkowski PH. Physiological properties of the electrically stimulated auditory nerve. II. Single fiber recordings. Hear. Res. 14(3):225–243, 1984.PubMedCrossRef

van der Heijden M, Joris PX. Panoramic measurements of the apex of the cochlea. J. Neurosci. 26(44):11462–11473, 2006.PubMedCrossRef

van Hoesel RJ. Exploring the benefits of bilateral cochlear implants. Audiol. Neuro-otol. 9(4):234–246, 2004.CrossRef

van Hoesel RJ, Clark GM. Fusion and lateralization study with two binaural cochlear implant patients. Ann. Otol. Rhinol. Laryngol. Suppl. 166:233–235, 1995.PubMed

van Hoesel RJ, Clark GM. Psychophysical studies with two binaural cochlear implant subjects. J. Acoust. Soc. Am. 102(1):495–507, 1997.PubMedCrossRef

van Hoesel RJ, Tyler RS. Speech perception, localization, and lateralization with bilateral cochlear implants. J. Acoust. Soc. Am. 113(3):1617–1630, 2003.PubMedCrossRef

Viemeister NF. Temporal modulation transfer functions based upon modulation thresholds. J. Acoust. Soc. Am. 66(5):1364–1380, 1979.PubMedCrossRef

Wilson BS, Lawson DT. Speech Processors for Auditory Prostheses. Final Report, NIH Project N01-DC-8-2105, 2006.

Wilson BS, Lawson DT, et al. Cochlear implants: some likely next steps. Annu. Rev. Biomed. Eng. 5:207–249, 2003.PubMedCrossRef

Yin TCT, Kuwada S. Binaural interaction in low-frequency neurons in inferior colliculus of the cat. II. Effects of changing rate and direction of interaural phase. J. Neurophysiol. 50:1000–1019, 1983.PubMed

Yin TCT, Kuwada S, et al. Interaural time sensitivity of high-frequency neurons in the inferior colliculus. J. Acoust. Soc. Am. 76:1401–1410, 1984.PubMedCrossRef

Yin TCT, Chan JCK, et al. Effects of interaural time delays of noise stimuli on low-frequency cells in the cat’s inferior colliculus. I. Responses to wideband noise. J. Neurophysiology. 55(2):280–300, 1986.

Zeng FG. Temporal pitch in electric hearing. Hear. Res. 174(1–2):101–106, 2002.PubMedCrossRef

Zwislocki J, Feldman RS. Just noticeable differences in dichotic phase. J. Acoust. Soc. Am. 28(5):860–864, 1956.CrossRef

Title: Neural and Behavioral Sensitivity to Interaural Time Differences Using Amplitude Modulated Tones with Mismatched Carrier Frequencies
Authors: Deidra A. Blanks
Jason M. Roberts
Emily Buss
Joseph W. Hall
Douglas C. Fitzpatrick
Publication date: 01-09-2007
Publisher: Springer-Verlag
Published in: Journal of the Association for Research in Otolaryngology / Issue 3/2007
Print ISSN: 1525-3961
Electronic ISSN: 1438-7573
DOI: https://doi.org/10.1007/s10162-007-0088-5

At a glance: The STEP trials

Springer Medicine

Neural and Behavioral Sensitivity to Interaural Time Differences Using Amplitude Modulated Tones with Mismatched Carrier Frequencies

Abstract

At a glance: The STEP trials

Springer Medicine

Abstract

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