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Sensitivity to interaural time difference and representation of azimuth in central nucleus of inferior colliculus in the barn owl

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Abstract

Standard electrophysiology and virtual auditory stimuli were used to investigate the influence of interaural time difference on the azimuthal tuning of neurons in the core and the lateral shell of the central nucleus of the inferior colliculus of the barn owl. The responses of the neurons to virtual azimuthal stimuli depended in a periodic way on azimuth. Fixation of the interaural time difference, while leaving all other spatial cues unchanged, caused a loss of periodicity and a broadening of azimuthal tuning. This effect was studied in more detail in neurons of the core. The azimuthal range tested and the frequency selectivity of the neurons were additional parameters influencing the changes induced by fixating the interaural time difference. The addition of an interaural time difference to the virtual stimuli resulted in a shift of the tuning curves that correlated with the interaural time difference added. In this condition, tuning strength did not change. These results suggest that interaural time difference is an important determinant of azimuthal tuning in all neurons of the core and lateral shell of the central nucleus of the inferior colliculus, and is the only determinant in many of the neurons from the core.

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Abbreviations

ABL:

Average binaural level

AddT x :

Manipulated virtual stimuli with additional ITD with x denoting the value of the additional ITD

FixT1–FixT4:

Different types of virtual stimuli with fixed ITD

HRIR:

Head related impulse response

HRTF:

Head related transfer function

IC:

Inferior colliculus

ICC:

Central nucleus of the IC

ICCc:

Core of the ICC

ICCls:

Lateral shell of the ICC

ICX:

External nucleus of the IC

ILD:

Interaural level difference

IR:

Impulse response

ITD:

Interaural time difference

RAF:

Rate azimuth function

References

  • Adolphs (1993) Bilateral inhibition generates neuronal responses tuned to interaural level differences in the auditory brainstem of the barn owl. J Neurosci 13:3647–3668

    PubMed  CAS  Google Scholar 

  • Brainard MS, Knudsen EI, Esterly SD (1992) Neural derivation of sound source location: resolution of spatial ambiguities in binaural cues. J Acoust Soc Am 91:1015–1027

    Article  PubMed  CAS  Google Scholar 

  • Brand A, Behrend O, Marquardt T, McAlpine D, Grothe B (2002) Precise inhibition is essential for microsecond interaural time difference coding. Nature 417:543–547

    Article  PubMed  CAS  Google Scholar 

  • Delgutte B, Joris PX, Litovsky RY, Yin TC (1999) Receptive fields and binaural interactions for virtual-space stimuli in the cat inferior colliculus. J Neurophysiol 81:2833–2851

    PubMed  CAS  Google Scholar 

  • Egnor R (2001) Effects of binaural decorrelation on neural and behavioral processing of interaural level differences in the barn owl (Tyto alba). J Comp Physiol A187:589–595

    Article  Google Scholar 

  • Euston DR, Takahashi TT (2002) From spectrum to space: the contribution of level difference cues to spatial receptive fields in the barn owl inferior colliculus. J Neurosci 22:284–293

    PubMed  CAS  Google Scholar 

  • Fujita I, Konishi M (1991) The role of GABAergic inhibition in processing of interaural time difference in the owl’s auditory system. J Neurosci 11:722–739

    PubMed  CAS  Google Scholar 

  • Hancock KE, Delgutte B (2004) A physiologically based model of interaural time difference discrimination. J Neurosci 24:7110–7117

    Article  PubMed  CAS  Google Scholar 

  • Hartmann WM, Wittenberg A (1996) On the externalization of sound sources. J Acoust Soc Am 99:3678–3688

    Article  PubMed  CAS  Google Scholar 

  • Keller CH, Takahashi TT (2005) Localization and identification of concurrent sounds in the owl’s auditory space map. J Neurosci 25:10446–10461

    Article  PubMed  CAS  Google Scholar 

  • Keller CH, Hartung K, Takahashi TT (1998) Head-related transfer functions of the barn owl: measurement and neural responses. Hear Res 118:13–34

    Article  PubMed  CAS  Google Scholar 

  • Knudsen EI (1983) Subdivisions of the inferior colliculus in the barn owl (Tyto alba). J Comp Neurol 218:174–186

    Article  PubMed  CAS  Google Scholar 

  • Knudsen EI (1984) Synthesis of a neural map of auditory space in the owl. In: Edelman GM, Gall WE, Cowan WM (eds) Dynamic aspects of neocortical function. Wiley, New York, pp 375–395

    Google Scholar 

  • Knudsen EI, Konishi M (1978a) A neural map of auditory space in the owl. Science 200:795–797

    Article  CAS  Google Scholar 

  • Knudsen EI, Konishi M (1978b) Space and frequency are represented separately in auditory midbrain of the owl. J Neurophysiol 41:870–884

    CAS  Google Scholar 

  • Knudsen EI, Knudsen PF, Masino T (1993) Parallel pathways mediating both sound localization and gaze control in the forebrain and midbrain of the barn owl. J Neurosci 13:2837–2852

    PubMed  CAS  Google Scholar 

  • Mazer JA (1998) How the owl resolves auditory coding ambiguity. Proc Natl Acad Sci USA 95:10932–10937

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Miller GL, Knudsen EI (1999) Early visual experience shapes the representation of auditory space in the forebrain gaze fields of the barn owl. J Neurosci 19:2326–2336

    PubMed  CAS  Google Scholar 

  • Moiseff A (1989) Bi-coordinate sound localization by the barn owl. J Comp Physiol A 164:637–644

    Article  PubMed  CAS  Google Scholar 

  • Moiseff A, Konishi M (1981) Neuronal and behavioral sensitivity to binaural time differences in the owl. J Neurosci 1:40–48

    PubMed  CAS  Google Scholar 

  • Moiseff A, Konishi M (1983) Binaural characteristics of units in the owl’s brainstem auditory pathway: precursors of restricted spatial receptive fields. J Neurosci 3:2553–2562

    PubMed  CAS  Google Scholar 

  • Nelken I, Bar Yosef O, Young ED (1998) Responses of field AES neurons to virtual space stimuli. In: Palmer AR, Rees A, Summerfield AQ, Meddis R (eds) Psychophysical, physiological advances in hearing, Whurr Publ, London, pp 504–512

    Google Scholar 

  • Olsen JF, Knudsen EI, Esterly SD (1989) Neural maps of interaural time and intensity difference in the optic tectum of the barn owl. J Neurosci 9:2591–2605

    PubMed  CAS  Google Scholar 

  • Pena JL, Konishi M (2001) Auditory spatial receptive fields created by multiplication. Science 292:249–252

    Article  PubMed  CAS  Google Scholar 

  • Pena JL, Viete S, Albeck Y, Konishi M (1996) Tolerance to sound intensity of binaural coincidence detection in the nucleus laminaris of the owl. J Neurosci 16:7046–7054

    PubMed  CAS  Google Scholar 

  • Poganiatz I, Wagner H (2001) Sound-localization experiments with barn owls in virtual space: influence of broadband interaural level difference on head-turning behavior. J Comp Physiol 187:225–233

    Article  CAS  Google Scholar 

  • Poganiatz I, Nelken I, Wagner H (2001) Sound-localization experiments with barn owls in virtual space: influence of interaural time difference on head-turning behavior. J Assoc Res Otolaryngol 2:1–21

    PubMed  CAS  Google Scholar 

  • Rice JJ, May BJ, Spirou GA, Young ED (1992) Pinna-based spectral cues for sound localization in cat. Hear Res 58:132–152

    Article  PubMed  CAS  Google Scholar 

  • Saberi K, Farahbod H, Konishi M (1998) How do owls localize interaurally phase-ambiguous signals? Proc Natl Acad Sci USA 95:6465–6468

    Article  PubMed  CAS  Google Scholar 

  • Saberi K, Takahashi Y, Farahbod H, Konishi M (1999) Neural bases of an auditory illusion and its elimination in owls. Nat Neurosci 2:656–659

    Article  PubMed  CAS  Google Scholar 

  • Spezio ML, Takahashi TT (2003) Frequency-specific interaural level difference tuning predicts spatial response patterns of space-specific neurons in the barn owl inferior colliculus. J Neurosci 23:4677–4688

    PubMed  CAS  Google Scholar 

  • Takahashi TT, Konishi M (1986) Selectivity for interaural time difference in the owl’s midbrain. J Neurosci 6:3413–3422

    PubMed  CAS  Google Scholar 

  • Takahashi TT, Konishi M (1988) Projections of the cochlear nuclei and nucleus laminaris to the inferior colliculus of the barn owl. J Comp Neurol 274:190–211

    Article  PubMed  CAS  Google Scholar 

  • Takahashi T, Moiseff A, Konishi M (1984) Time and intensity cues are processed independently in the auditory system of the owl. J Neurosci 4:1781–1786

    PubMed  CAS  Google Scholar 

  • Takahashi TT, Wagner H, Konishi M (1989) Role of commissural projections in the representation of bilateral auditory space in the barn owl’s inferior colliculus. J Comp Neurol 281:545–554

    Article  PubMed  CAS  Google Scholar 

  • Tollin DJ, Yin TC (2002) The coding of spatial location by single units in the lateral superior olive of the cat. II. The determinants of spatial receptive fields in azimuth. J Neurosci 22:1468–1479

    PubMed  CAS  Google Scholar 

  • Wagner H (1990) Receptive fields of neurons in the owl’s auditory brainstem change dynamically. Eur J Neurosci 2:949–959

    Article  PubMed  Google Scholar 

  • Wagner H (1993) Sound-localization deficits induced by lesions in the barn owl’s auditory space map. J Neurosci 13:371–386

    PubMed  CAS  Google Scholar 

  • Wagner H, Takahashi TT, Konishi M (1987) Representation of interaural time difference in the central nucleus of the barn owl’s inferior colliculus. J Neurosci 7:3105–3116

    PubMed  CAS  Google Scholar 

  • Wagner H, Mazer JA, von Campenhausen M (2002) Response properties of neurons in the core of the central nucleus of the inferior colliculus of the barn owl. Eur J Neurosci 15:1343–1352

    Article  PubMed  Google Scholar 

  • Wagner H, Güntürkün O, Nieder B (2003) Anatomical markers for the subdivisions of the barn owl’s inferior-collicular complex and adjacent peri- and subventricular structures. J Comp Neurol 465:145–159

    Article  PubMed  Google Scholar 

  • Wagner H, Brill S, Kempter R, Carr CE (2005) Microsecond precision of phase delay in the auditory system of the barn owl. J Neurophysiol 94:1655–1658

    Article  PubMed  Google Scholar 

  • Wightman FL, Kistler DJ (1989a) Headphone simulation of free-field listening I. Stimulus synthesis. J Acoust Soc Am 85:858–867

    Article  CAS  Google Scholar 

  • Wightman FL, Kistler DJ (1989b) Headphone simulation of free-field listening II. Psychophysical validation. J Acoust Soc Am 85:868–878

    Article  CAS  Google Scholar 

  • Wightman FL, Kistler DJ (1992) The dominant role of low-frequency interaural time differences in sound localization. J Acoust Soc Am 91:1648–1661

    Article  PubMed  CAS  Google Scholar 

  • Yin TC, Kuwada S (1984) Neuronal mechanisms of binaural interactions. In: Edelman GM, Gall WE, Cowan WM (eds) Dynamic aspects of neocortical function. Wiley, New York, pp 263–313

    Google Scholar 

Download references

Acknowledgments

All experiments were carried out in accordance with German law and were approved by the Regierungspräsidium Köln. We thank Sandra Brill for help with analyzing the data.

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Correspondence to Hermann Wagner.

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Bremen, P., Poganiatz, I., von Campenhausen, M. et al. Sensitivity to interaural time difference and representation of azimuth in central nucleus of inferior colliculus in the barn owl. J Comp Physiol A 193, 99–112 (2007). https://doi.org/10.1007/s00359-006-0172-z

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  • DOI: https://doi.org/10.1007/s00359-006-0172-z

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