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Journal of the Association for Research in Otolaryngology

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01-12-2009

Processing Temporal Modulations in Binaural and Monaural Auditory Stimuli by Neurons in the Inferior Colliculus and Auditory Cortex

Authors: Douglas C. Fitzpatrick, Jason M. Roberts, Shigeyuki Kuwada, Duck O. Kim, Blagoje Filipovic

Published in: Journal of the Association for Research in Otolaryngology | Issue 4/2009

Abstract

Processing dynamic changes in the stimulus stream is a major task for sensory systems. In the auditory system, an increase in the temporal integration window between the inferior colliculus (IC) and auditory cortex is well known for monaural signals such as amplitude modulation, but a similar increase with binaural signals has not been demonstrated. To examine the limits of binaural temporal processing at these brain levels, we used the binaural beat stimulus, which causes a fluctuating interaural phase difference, while recording from neurons in the unanesthetized rabbit. We found that the cutoff frequency for neural synchronization to the binaural beat frequency (BBF) decreased between the IC and auditory cortex, and that this decrease was associated with an increase in the group delay. These features indicate that there is an increased temporal integration window in the cortex compared to the IC, complementing that seen with monaural signals. Comparable measurements of responses to amplitude modulation showed that the monaural and binaural temporal integration windows at the cortical level were quantitatively as well as qualitatively similar, suggesting that intrinsic membrane properties and afferent synapses to the cortical neurons govern the dynamic processing. The upper limits of synchronization to the BBF and the band-pass tuning characteristics of cortical neurons are a close match to human psychophysics.

Alexander C, Sadiku M. Fundamentals of Electric Circuits. New York, McGraw-Hill Higher Education, 2006.

Anderson DJ, Rose JE, Hind JE, Brugge JF. Temporal position of discharges in single auditory nerve fibers within the cycle of a sine-wave stimulus: frequency and intensity effects. J. Acoust. Soc. Am. 49:1131–1139, 1971.CrossRefPubMed

Batra R, Kuwada S, Stanford TS. High-frequency neurons in the inferior colliculus that are sensitive to interaural delays of amplitude-modulated tones: evidence for dual binaural influences. J. Neurophysiol. 70:64–80, 1993.PubMed

Blanks DA, Roberts JM, Buss E, Hall JW, Fitzpatrick DC. Neural and behavioral sensitivity to interaural time differences using amplitude modulated tones with mismatched carrier frequencies. J. Assoc. Res. Otolaryngol. 8:393–408, 2007.CrossRefPubMed

Bradley JS, Reich RD, Norcross SG. On the combined effects of early- and late-arriving sound on spatial impression in concert halls. J. Acoust. Soc. Am. 108:651–661, 2000.CrossRefPubMed

Carlile S, Hyams S, Delaney S. Systematic distortions of auditory space perception following prolonged exposure to broadband noise. J. Acoust. Soc. Am. 110:416–424, 2001.CrossRefPubMed

Covey E, Kauer JA, Casseday JH. Whole-cell patch-clamp recording reveals subthreshold sound-evoked postsynaptic currents in the inferior colliculus of awake bats. J. Neurosci. 16:3009–3018, 1996.PubMed

Creutzfeldt O, Hellweg FC, Schreiner C. Thalamocortical transformation of responses to complex auditory stimuli. Exp. Brain. Res. 39:87–104, 1980.CrossRefPubMed

Eggermont JJ. The magnitude and phase of temporal modulation transfer functions in cat auditory cortex. J. Neurosci. 19:2780–2788, 1999.PubMed

Eggermont JJ. Temporal modulation transfer functions in cat primary auditory cortex: separating stimulus effects from neural mechanisms. J. Neurophysiol. 87:305–321, 2002.PubMed

Faller C, Merimaa J. Source localization in complex listening situations: selection of binaural cues based on interaural coherence. J. Acoust. Soc. Am. 116:3075–3089, 2004.CrossRefPubMed

Faure PA, Fremouw T, Casseday JH, Covey E. Temporal masking reveals properties of sound-evoked inhibition in duration-tuned neurons of the inferior colliculus. J. Neurosci. 23:3052–3065, 2003.PubMed

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

Fitzpatrick DC, Kuwada S, Batra R. Neural sensitivity to interaural time differences: beyond the Jeffress model. J. Neurosci. 20:1605–1615, 2000.PubMed

Fitzpatrick DC, Batra R, Stanford TR, Kuwada S. A neuronal population code for sound localization. Nature 388:871–874, 1997.CrossRefPubMed

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

Goldstein JL, Baer T, Kiang NYS. A theoretical treatment of latency, group delay, and tuning characteristics for auditory-nerve responses to clicks and tones. In: Sachs MB (ed) Physiology of the Auditory System. Baltimore, MD, National Educational Consultants, pp. 133–141, 1971.

Goupell MJ, Hartmann WM. Interaural fluctuations and the detection of interaural incoherence: bandwidth effects. J. Acoust. Soc. Am. 119:3971–3986, 2006.CrossRefPubMed

Grantham DW. Detectability of time-varying interaural correlation in narrow-band noise stimuli. J. Acoust. Soc. Am. 72:1178–1184, 1982.CrossRefPubMed

Grantham DW. Motion aftereffects with horizontally moving sound sources in the free field. Percept. Psychophysiol. 45:129–136, 1989.

Grantham DW, Wightman FL. Detectability of varying interaural temporal differences. J. Acoust. Soc. Am. 63:511–523, 1978.CrossRefPubMed

Greenwood DD, Joris PX. Mechanical and “temporal” filtering as codeterminants of the response by cat primary fibers to amplitude-modulated signals. J. Acoust. Soc. Am. 99:1029–1039, 1996.CrossRefPubMed

Heil P. First-spike latency of auditory neurons revisited. Curr. Opin. Neurobiol. 14:461–467, 2004.CrossRefPubMed

Ingham NJ, McAlpine D. Spike-frequency adaptation in the inferior colliculus. J. Neurophysiol. 91:632–645, 2004.CrossRefPubMed

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

Joris PX, Schreiner CE, Rees A. Neural processing of amplitude-modulated sounds. Physiol. Rev. 84:541–577, 2004.CrossRefPubMed

Joris PX, van de Sande B, Recio-Spinoso A, van der Heijden M. Auditory midbrain and nerve responses to sinusoidal variations in interaural correlation. J. Neurosci. 26:279–289, 2006.CrossRefPubMed

Kim DO, Molnar CE. A population study of cochlear nerve fibers: comparison of spatial distributions of average-rate and phase-locking measures of responses to single tones. J. Neurophysiol. 42:16–30, 1979.PubMed

Krishna BS, Semple MN. Auditory temporal processing: responses to sinusoidally amplitude-modulated tones in the inferior colliculus. J. Neurophysiol. 84:255–273, 2000.PubMed

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

Kuwada S, Batra R, Yin TCT, Oliver DL, Haberly LB, Stanford TR. Intracellular recordings in response to monaural and binaural stimulation of neurons in the inferior colliculus of the cat. J. Neurosci. 17:7565–7581, 1997.PubMed

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

Licklider JCR, Webster JC, Hedlun JM. On the frequency limits of binaural beats. J. Acoust. Soc. Am. 22:468–473, 1950.CrossRef

Malone BJ, Scott BH, Semple MN. Context-dependent adaptive coding of interaural phase disparity in the auditory cortex of awake macaques. J. Neurosci. 22:4625–4638, 2002.PubMed

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

McAlpine D, Jiang D, Palmer AR. A neural code for low-frequency sound localization in mammals. Nat. Neurosci. 4:396–401, 2001.CrossRefPubMed

McAlpine D, Jiang D, Shackleton TM, Palmer AR. Responses of neurons in the inferior colliculus to dynamic interaural phase cues: evidence for a mechanism of binaural adaptation. J. Neurophysiol. 83:1356–1365, 2000.PubMed

McMullen NT, Glaser EM. Tonotopic organization of rabbit auditory cortex. Exp. Neurol. 75:208–220, 1982.CrossRefPubMed

Middlebrooks JC. Auditory cortex phase locking to amplitude-modulated cochlear implant pulse trains. J. Neurophysiol. 100:76–91, 2008.CrossRefPubMed

Miller LM, Escabi MA, Read HL, Schreiner CE. Spectrotemporal receptive fields in the lemniscal auditory thalamus and cortex. J. Neurophysiol. 87:516–527, 2002.PubMed

Nelson PC, Carney LH. Neural rate and timing cues for detection and discrimination of amplitude-modulated tones in the awake rabbit inferior colliculus. J. Neurophysiol. 97:522–539, 2007.CrossRefPubMed

Palmer AR, Rees A, Caird D. Interaural delay sensitivity to tones and broad band signals in the guinea-pig inferior colliculus. Hear. Res. 50:71–86, 1990.CrossRefPubMed

Papoulis A. Signal Processing. New York, McGraw-Hill, 1962.

Perrott DR, Nelson MA. Limits for the detection of binaural beats. J. Acoust. Soc. Am. 46:1477–1481, 1969.CrossRefPubMed

Pfeiffer RR, Molnar CE. Cochlear nerve fiber discharge patterns: relationship to the cochlear microphonic. Science 167:1614–1616, 1970.CrossRefPubMed

Reale RA, Brugge JF. Auditory cortical neurons are sensitive to static and continuously changing interaural phase cues. J. Neurophysiol. 64:1247–1260, 1990.PubMed

Rees A, Moller AR. Stimulus properties influencing the responses of inferior colliculus neurons to amplitude-modulated sounds. Hear. Res. 27:129–143, 1987.CrossRefPubMed

Rhode WS. A digital system for auditory neurophysiological research. In: Brown P (ed) Current Computer Technology in Neurobiology. Washington D.C., Hemisphere, pp. 543–567, 1976.

Rose HJ, Metherate R. Auditory thalamocortical transmission is reliable and temporally precise. J. Neurophysiol. 94:2019–2030, 2005.CrossRefPubMed

Schreiner CE, Urbas JV. Representation of amplitude modulation in the auditory cortex of the cat. II. Comparison between cortical fields. Hear. Res. 32:49–63, 1988.CrossRefPubMed

Sivaramakrishnan S, Oliver DL. Neuronal responses to lemniscal stimulation in laminar brain slices of the inferior colliculus. J. Assoc. Res. Otolaryngol. 7:1–14, 2006.CrossRefPubMed

Siveke I, Ewert SD, Grothe B, Wiegrebe L. Psychophysical and physiological evidence for fast binaural processing. J. Neurosci. 28:2043–2052, 2008.CrossRefPubMed

Spitzer MW, Semple MN. Responses of inferior colliculus neurons to time-varying interaural phase disparity: effects of shifting the locus of virtual motion. J. Neurophysiol. 69:1245–1263, 1993.PubMed

Stecker GC, Harrington IA, Middlebrooks JC. Location coding by opponent neural populations in the auditory cortex. PLoS Biol. 3:e78, 2005.CrossRefPubMed

Ter-Mikaelian M, Sanes DH, Semple MN. Transformation of temporal properties between auditory midbrain and cortex in the awake Mongolian gerbil. J. Neurosci. 27:6091–6102, 2007.CrossRefPubMed

Viemeister NF. Temporal factors in audition: a system analysis approach. In: Evans Wilson EFJP (ed) Psychophysics and Physiology of Hearing. London, Academic, 1977.

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

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, 1983a.PubMed

Yin TCT, Kuwada S. Binaural interaction in low-frequency neurons in inferior colliculus of the cat. III. Effects of changing frequency. J. Neurophysiol. 50:1020–1042, 1983b.PubMed

Yin TCT, Chan JCK. Interaural time sensitivity in medial superior olive of cat. J. Neurophysiol. 64:465–488, 1990.PubMed

Title: Processing Temporal Modulations in Binaural and Monaural Auditory Stimuli by Neurons in the Inferior Colliculus and Auditory Cortex
Authors: Douglas C. Fitzpatrick
Jason M. Roberts
Shigeyuki Kuwada
Duck O. Kim
Blagoje Filipovic
Publication date: 01-12-2009
Publisher: Springer-Verlag
Published in: Journal of the Association for Research in Otolaryngology / Issue 4/2009
Print ISSN: 1525-3961
Electronic ISSN: 1438-7573
DOI: https://doi.org/10.1007/s10162-009-0177-8

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Processing Temporal Modulations in Binaural and Monaural Auditory Stimuli by Neurons in the Inferior Colliculus and Auditory Cortex

Abstract

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