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The Interaural Time Difference Pathway: a Comparison of Spectral Bandwidth and Correlation Sensitivity at Three Anatomical Levels

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ABSTRACT

Temporal differences between the two ears are critical for spatial hearing. They can be described along axes of interaural time difference (ITD) and interaural correlation, and their processing starts in the brainstem with the convergence of monaural pathways which are tuned in frequency and which carry temporal information. In previous studies, we examined the bandwidth (BW) of frequency tuning at two stages: the auditory nerve (AN) and inferior colliculus (IC), and showed that BW depends on characteristic frequency (CF) but that there is no difference in the mean BW of these two structures when measured in a binaural, temporal framework. This suggested that there is little frequency convergence in the ITD pathway between AN and IC and that frequency selectivity determined by the cochlear filter is preserved up to the IC. Unexpectedly, we found that AN and IC neurons can be similar in CF and BW, yet responses to changes in interaural correlation in the IC were different than expected from coincidence patterns (“pseudo-binaural” responses) in the AN. To better understand this, we here examine the responses of bushy cells, which provide monaural inputs to binaural neurons. Using broadband noise, we measured BW and correlation sensitivity in the cat trapezoid body (TB), which contains the axons of bushy cells. This allowed us to compare these two metrics at three stages in the ITD pathway. We found that BWs in the TB are similar to those in the AN and IC. However, TB neurons were found to be more sensitive to changes in stimulus correlation than AN or IC neurons. This is consistent with findings that show that TB fibers are more temporally precise than AN fibers, but is surprising because it suggests that the temporal information available monaurally is not fully exploited binaurally.

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REFERENCES

  • Agmon-Snir H, Carr CE, Rinzel J (1998) The role of dendrites in auditory coincidence detection. Nature 393:268–272

    Article  CAS  PubMed  Google Scholar 

  • Albeck Y, Konishi M (1995) Reponses of neurons in the auditory pathway of the barn owl to partially correlated binaural signals. J Neurophysiol 74:1689–1700

    CAS  PubMed  Google Scholar 

  • Batra R, Kuwada S, Fitzpatrick DC (1997) Sensitivity to interaural temporal disparities of low- and high-frequency neurons in the superior olivary complex. I. Heterogeneity of responses. J Neurophysiol 78:1222–1236

    CAS  PubMed  Google Scholar 

  • Beckius GE, Batra R, Oliver DL (1999) Axons from anteroventral cochlear nucleus that terminate in medial superior olive of cat: observations related to delay lines. J Neurosci 19:3146–3161

    Google Scholar 

  • Bourbon WT, Jeffress LA (1965) Effect of bandwidth of masking noise on the detection of homophasic and anitphasic tonal signals. J Acoust Soc Am 37:1180–1181

    Article  Google Scholar 

  • Bremen P, Joris PX (2013) Axonal recordings from medial superior olive neurons obtained from the lateral lemniscus of the chinchilla. J Neurosci 33(44):17506–17518

    Google Scholar 

  • 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 60:457–474

    Article  PubMed  Google Scholar 

  • Carney LHC, Yin TCT (1988) Temporal coding of resonances by low-frequency auditory nerve fibers: single-fiber responses and a population model. J Neurophysiol 60:1653–1677

    CAS  PubMed  Google Scholar 

  • Cleveland WS, Devlin SJ (1988) Locally weighted regression: an approach to regression analysis by local fitting. J Am Stat Assoc 83:596–610

    Article  Google Scholar 

  • Coffey CS, Ebert CS Jr, Marshall AF, Skaggs JD, Falk SE, Crocker WD, Pearson JM, Fitzpatrick DC (2006) Detection of interaural correlation by neurons in the superior olivary complex, inferior colliculus and auditory cortex of the unanesthetized rabbit. Hear Res 221:1–16

    Article  PubMed  Google Scholar 

  • Couchman K, Grothe B, Felmy F (2010) Medial superior olivary neurons receive surprisingly few excitatory and inhibitory inputs with balanced strength and short-term dynamics. J Neurosci 30:17111–17121

    Article  CAS  PubMed  Google Scholar 

  • Day ML, Semple MN (2011) Frequency-dependent interaural delays in the medial superior olive: implications for interaural cochlear delays. J Neurophysiol 106:1985–1999

    Article  PubMed  Google Scholar 

  • De Boer E, de Jongh HR (1978) On cochlear encoding: potentialities and limitations of the reverse correlation technique. J Acoust Soc Am 63:115–135

    Article  PubMed  Google Scholar 

  • Devore S, Ihlefeld A, Hancock K, Shinn-Cunningham B, Delgutte B (2009) Accurate sound localization in reverberant environments is mediated by robust encoding of spatial cues in the auditory midbrain. Neuron 62:123–134

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Durlach NI, Colburn HS (1978) Binaural phenomena. In: Carterette E, Friedman M (eds) Handbook of perception, IVth edn. Academic, New York, pp 365–465

    Google Scholar 

  • Evans EF (1977) Frequency selectivity at high signal levels of single units in cochlear nerve and nucleus. In: Evans EF, Wilson JP (eds) Psychophysics and physiology of hearing. Academic, London, pp 185–192

    Google Scholar 

  • Finlayson PG, Caspary DM (1991) Low-frequency neurons in the lateral superior olive exhibit phase-sensitive binaural inhibition. J Neurophysiol 65:598–605

    CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Franken TP, Joris PX (2012) Auditory nerve and trapezoid body spiketrains as inputs to a coincidence detector. Assoc Res Otolaryngol Abs 35:73

    Google Scholar 

  • Franken TP, Roberts MT, Wei L, Golding NL, Joris PX (2013) In vivo whole-cell recordings from principal neurons of the medial superior olive. Assoc Res Otolaryngol Abs 36:353

    Google Scholar 

  • Gabriel KG, Colburn HS (1981) Interaural correlation discrimination: I. Bandwidth and level dependence. J Acoust Soc Am 69:1394–1401

    Article  CAS  PubMed  Google Scholar 

  • Geesa BH, Langford TL (1976) Binaural interaction in cat and man. II. Interaural noise correlation and signal detection. J Acoust Soc Am 59:1195–1196

    Article  CAS  PubMed  Google Scholar 

  • Goldberg JM, Brown PB (1968) Functional organization of the dog superior olivary complex: an anatomical and electrophysiological study. J Neurophysiol 31:639–656

    CAS  PubMed  Google Scholar 

  • Goldberg JM, Brown PB (1969) Response of binaural neurons of dog superior olivary complex to dichotic tonal stimuli: some physiological mechanisms of sound localization. J Neurophysiol 22:613–636

    Google Scholar 

  • Hall JW, Tyler RS, Fernandes MA (1983) Monaural and binaural auditory frequency resolution measured using bandlimited noise and notched-noise masking. J Acoust Soc Am 73:894–898

    Article  CAS  PubMed  Google Scholar 

  • Hoppe SA, Langford TL (1974) Binaural interaction in cat and man. I. Signal detection and noise cross correlation. J Acoust Soc Am 55:1263–1265

    Article  CAS  PubMed  Google Scholar 

  • Jennings TR, Colburn HS (2009) Models of the superior olivary complex. In: Meddis R, Lopez-Poveda EA, Popper AN, Fay R (eds) Computational models of the auditory system. Springer, New York

    Google Scholar 

  • Joris PX (1996) Envelope coding in the lateral superior olive. II. Characteristic delays and comparison with responses in the medial superior olive. J Neurophysiol 76:2137–2156

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Joris PX, Smith PH (2008) The volley theory and the spherical cell puzzle. Neuroscience 154:65–76

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Joris PX, Yin TC (1995) Envelope coding in the lateral superior olive. I. Sensitivity to interaural time differences. J Neurophysiol 73:1043–1062

    CAS  PubMed  Google Scholar 

  • Joris PX, Smith PH, Yin TCT (1994a) Enhancement of synchronization in the anteroventral cochlear nucleus. II. Responses to tonebursts in the tuning-curve tail. J Neurophysiol 71:1037–1051

    CAS  PubMed  Google Scholar 

  • Joris PX, Carney LHC, Smith PH, Yin TCT (1994b) Enhancement of synchronization in the anteroventral cochlear nucleus. I. Responses to tonebursts at characteristic frequency. J Neurophysiol 71:1022–1036

    CAS  PubMed  Google Scholar 

  • Joris PX, Van de Sande B, van der Heijden M (2005) Temporal damping in response to broadband noise. I. Inferior colliculus. J Neurophysiol 93:1857–1870

    Article  PubMed  Google Scholar 

  • Joris PX, Louage DH, Cardoen L, van der Heijden M (2006a) Correlation index: a new metric to quantify temporal coding. Hear Res 216–217:19–30

    Article  PubMed  Google Scholar 

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

    Google Scholar 

  • Joris PX, Van de Sande B, Louage DH, van der Heijden M (2006c) Binaural and cochlear disparities. Proc Natl Acad Sci U S A 103:12917–12922

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Joris PX, Louage DH, van der Heijden M (2008) Temporal damping in response to broadband noise. II. Auditory nerve. J Neurophysiol 99:1942–1952

    Article  PubMed  Google Scholar 

  • Joris PX, Bergevin C, Kalluri R, Mc Laughlin M, Michelet P, van der Heijden M, Shera CA (2011) Frequency selectivity in Old-World monkeys corroborates sharp cochlear tuning in humans. Proc Natl Acad Sci U S A 108:17516–17520

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Karino S, Smith PH, Yin TC, Joris PX (2011) Axonal branching patterns as sources of delay in the mammalian auditory brainstem: a re-examination. J Neurosci 31:3016–3031

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kiang NYS, Watanabe T, Thomas EC, Clark LF (1965) Discharge patterns of single fibers in the cat’s auditory nerve, 35th edn. Research Monograph No 35, MIT, Cambridge

    Google Scholar 

  • Kohlrausch A (1988) Auditory filter shape derived from binaural masking experiments. J Acoust Soc Am 84:573–583

    Article  CAS  PubMed  Google Scholar 

  • Kollmeier B, Holube I (1992) Auditory filter bandwidths in binaural and monaural listening conditions. J Acoust Soc Am 92:1889–1901

    Article  CAS  PubMed  Google Scholar 

  • Kuenzel T, Borst JG, van der Heijden M (2011) Factors controlling the input-output relationship of spherical bushy cells in the gerbil cochlear nucleus. J Neurosci 31:4260–4273

    Google Scholar 

  • Liberman MC (1978) Auditory-nerve response from cats raised in a low-noise chamber. J Acoust Soc Am 63:442–455

    Article  CAS  PubMed  Google Scholar 

  • Lingner A, Wiegrebe L, Grothe B (2012) Sound localization in noise by gerbils and humans. J Assoc Res Otolaryngol 13:237–248

    Article  PubMed Central  PubMed  Google Scholar 

  • Louage DH, van der Heijden M, Joris PX (2004) Temporal properties of responses to broadband noise in the auditory nerve. J Neurophysiol 91:2051–2065

    Article  PubMed  Google Scholar 

  • Louage DH, van der Heijden M, Joris PX (2005) Enhanced temporal response properties of anteroventral cochlear nucleus neurons to broadband noise. J Neurosci 25:1560–1570

    Article  CAS  PubMed  Google Scholar 

  • Louage DH, Joris PX, van der Heijden M (2006) Decorrelation sensitivity of auditory nerve and anteroventral cochlear nucleus fibers to broadband and narrowband noise. J Neurosci 26:96–108

    Google Scholar 

  • Mc Laughlin M, Van de Sande B, van der Heijden M, Joris PX (2007) Comparison of bandwidths in the inferior colliculus and the auditory nerve. I. Measurement using a spectrally manipulated stimulus. J Neurophysiol 98:2566–2579

    Article  PubMed  Google Scholar 

  • Mc Laughlin M, Chabwine JN, van der Heijden M, Joris PX (2008) Comparison of bandwidths in the inferior colliculus and the auditory nerve. II: Measurement using a temporally manipulated stimulus. J Neurophysiol 100:2312–2327

    Article  PubMed  Google Scholar 

  • Palmer AR, Kuwada S (2005) Binaural and spatial coding in the inferior colliculus. In: Winer JA, Schreiner CE (eds) The inferior colliculus. Springer, New York, pp 377–410

    Chapter  Google Scholar 

  • Palmer AR, Jiang D, McAlpine D (2000) Neural responses in the inferior colliculus to binaural masking level differences created by inverting the noise in one ear. J Neurophysiol 84:844–852

    CAS  PubMed  Google Scholar 

  • Pfeiffer RR, Kim DO (1972) Response patterns of single cochlear nerve fibers to click stimuli: descriptions for cat. J Acoust Soc Am 52:1669–1677

    Article  CAS  PubMed  Google Scholar 

  • Pickles JO (1979) Psychophysical frequency resolution in the cat as determined by simultaneous masking and its relation to auditory-nerve resolution. J Acoust Soc Am 66:1725–1732

    Article  CAS  PubMed  Google Scholar 

  • Recio-Spinoso A (2012) Enhancement and distortion in the temporal representation of sounds in the ventral cochlear nucleus of chinchillas and cats. PLoS ONE 7:e44286

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Rhode WR (1971) Observations of the vibration of the basilar membrane in squirrel monkeys using the Mossbauer technique. J Acoust Soc Am 4:1218–1231

    Article  Google Scholar 

  • Rhode WS, Smith PH (1985) Characteristics of tone-pip response patterns in relationship to spontaneous rate in cat auditory nerve fibers. Hear Res 18:159–168

    Article  CAS  PubMed  Google Scholar 

  • Robinson DE, Jeffress LA (1963) Effect of varying the interaural noise correlation on the detectability of tonal signals. J Acoust Soc Am 35:1947–1952

    Article  Google Scholar 

  • Rouiller EM, Cronin-Schreiber R, Fekete DM, Ryugo DK (1986) The central projections of intracellularly labeled auditory nerve fibers in cats: an analysis of terminal morphology. J Comp Neurol 249:261–278

    Article  CAS  PubMed  Google Scholar 

  • Ruggero MA (1973) Response to noise of auditory nerve fibers in the squirrel monkey. J Neurophysiol 36:569–587

    CAS  PubMed  Google Scholar 

  • 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 305:35–48

    Article  CAS  PubMed  Google Scholar 

  • Sento S, Ryugo DK (1989) Endbulbs of Held and spherical bushy cells in cats: morphological correlates with physiological properties. J Comp Neurol 280:553–562

    Article  CAS  PubMed  Google Scholar 

  • Shackleton TM, Arnott RH, Palmer AR (2005) Sensitivity to interaural correlation of single neurons in the inferior colliculus of guinea pigs. J Assoc Res Otolaryngol 6:244–259

    Article  PubMed Central  PubMed  Google Scholar 

  • Smith PH, Joris PX, Carney LHC, Yin TCT (1991) Projections of physiologically characterized globular bushy cell axons from the cochlear nucleus of the cat. J Comp Neurol 304:387–407

    Article  CAS  PubMed  Google Scholar 

  • Smith PH, Joris PX, Yin TCT (1993) Projections of physiologically characterized spherical bushy cell axons from the cochlear nucleus of the cat: evidence for delay lines to the medial superior olive. J Comp Neurol 331:245–260

    Article  CAS  PubMed  Google Scholar 

  • Sondhi MM, Guttman N (1966) Width of the spectrum effective in the binaural release of masking. J Acoust Soc Am 40:600–606

    Article  Google Scholar 

  • Spirou GA, Brownell WE, Zidanic M (1990) Recordings from cat trapezoid body and HRP labeling of globular bushy cell axons. J Neurophysiol 63:1169–1190

    CAS  PubMed  Google Scholar 

  • Spitzer MW, Semple MN (1998) Transformation of binaural response properties in the ascending auditory pathway: influence of time-varying interaural phase disparity. J Neurophysiol 80:3062–3076

    CAS  PubMed  Google Scholar 

  • Tollin DJ, Yin TC (2005) Interaural phase and level difference sensitivity in low-frequency neurons in the lateral superior olive. J Neurosci 25:10648–10657

    Google Scholar 

  • van der Heijden M, Trahiotis C (1998) Binaural detection as a function of interaural correlation and bandwidth of masking noise: implications for estimates of spectral resolution. J Acoust Soc Am 103:1609–1614

    Article  PubMed  Google Scholar 

  • van der Heijden M, Trahiotis C (1999) Masking with interaurally delayed stimuli: the use of “internal” delays in binaural detection. J Acoust Soc Am 105:388–399

    Article  PubMed  Google Scholar 

  • van der Heijden M, Louage DH, Joris PX (2011a) Responses of auditory nerve and anteroventral cochlear nucleus fibers to broadband and narrowband noise: implications for the sensitivity to interaural delays. J Assoc Res Otolaryngol 12:485–502

    Article  PubMed Central  PubMed  Google Scholar 

  • van der Heijden M, Lorteije JA, Plauska A, Roberts MT, Golding NL, Borst JG (2013) Directional hearing by linear summation of binaural inputs at the medial superior olive. Neuron 78:936–948

    Article  PubMed  Google Scholar 

  • Verschooten E, Desloovere C, Joris PX (2012) Neural tuning measured with compound action potentials in normal hearing human volunteers. Assoc Res Otolaryngol Abs 35:360

    Google Scholar 

  • Wakeford OS, Robinson DE (1974) Detection of binaurally masked tones by the cat. J Acoust Soc Am 56:952–956

    Article  CAS  PubMed  Google Scholar 

  • Watson CS (1963) Masking of tones by noise for the cat. J Acoust Soc Am 35:167–172

    Article  Google Scholar 

  • Yin TCT, Chan JK (1990) Interaural time sensitivity in medial superior olive of cat. J Neurophysiol 64:465–488

    CAS  PubMed  Google Scholar 

  • Yin TCT, Chan JK, Irvine DRF (1986) Effects of interaural time delays of noise stimuli on low-frequency cells in the cat’s inferior colliculus. I. Responses to wideband noise. J Neurophysiol 55:280–300

    CAS  PubMed  Google Scholar 

  • Zhou Y, Carney LH, Colburn HS (2005) A model for interaural time difference sensitivity in the medial superior olive: interaction of excitatory and inhibitory synaptic inputs, channel dynamics, and cellular morphology. J Neurosci 25:3046–3058

    Article  CAS  PubMed  Google Scholar 

  • Zurek PM, Durlach NI (1987) Masker-bandwidth dependence in homophasic and antiphasic tone detection. J Acoust Soc Am 81:459–464

    Article  CAS  PubMed  Google Scholar 

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ACKNOWLEDGMENTS

This research was supported by the Fund for Scientific Research—Flanders (G.0633.07, G.0714.09, G.0961.11) and Research Fund K.U.Leuven (OT/09/50).

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Correspondence to Philip X. Joris.

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Mc Laughlin, M., Franken, T.P., van der Heijden, M. et al. The Interaural Time Difference Pathway: a Comparison of Spectral Bandwidth and Correlation Sensitivity at Three Anatomical Levels. JARO 15, 203–218 (2014). https://doi.org/10.1007/s10162-013-0436-6

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  • DOI: https://doi.org/10.1007/s10162-013-0436-6

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