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
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
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
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
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
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
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
Hancock KE, Delgutte B (2004) A physiologically based model of interaural time difference discrimination. J Neurosci 24:7110–7117
Hartmann WM, Wittenberg A (1996) On the externalization of sound sources. J Acoust Soc Am 99:3678–3688
Keller CH, Takahashi TT (2005) Localization and identification of concurrent sounds in the owl’s auditory space map. J Neurosci 25:10446–10461
Keller CH, Hartung K, Takahashi TT (1998) Head-related transfer functions of the barn owl: measurement and neural responses. Hear Res 118:13–34
Knudsen EI (1983) Subdivisions of the inferior colliculus in the barn owl (Tyto alba). J Comp Neurol 218:174–186
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
Knudsen EI, Konishi M (1978a) A neural map of auditory space in the owl. Science 200:795–797
Knudsen EI, Konishi M (1978b) Space and frequency are represented separately in auditory midbrain of the owl. J Neurophysiol 41:870–884
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
Mazer JA (1998) How the owl resolves auditory coding ambiguity. Proc Natl Acad Sci USA 95:10932–10937
McAlpine D, Jiang D, Palmer AR (2001) A neural code for low-frequency sound localisation in mammals. Nat Neurosci 4:396–401
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
Moiseff A (1989) Bi-coordinate sound localization by the barn owl. J Comp Physiol A 164:637–644
Moiseff A, Konishi M (1981) Neuronal and behavioral sensitivity to binaural time differences in the owl. J Neurosci 1:40–48
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
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
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
Pena JL, Konishi M (2001) Auditory spatial receptive fields created by multiplication. Science 292:249–252
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
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
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
Rice JJ, May BJ, Spirou GA, Young ED (1992) Pinna-based spectral cues for sound localization in cat. Hear Res 58:132–152
Saberi K, Farahbod H, Konishi M (1998) How do owls localize interaurally phase-ambiguous signals? Proc Natl Acad Sci USA 95:6465–6468
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
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
Takahashi TT, Konishi M (1986) Selectivity for interaural time difference in the owl’s midbrain. J Neurosci 6:3413–3422
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
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
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
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
Wagner H (1990) Receptive fields of neurons in the owl’s auditory brainstem change dynamically. Eur J Neurosci 2:949–959
Wagner H (1993) Sound-localization deficits induced by lesions in the barn owl’s auditory space map. J Neurosci 13:371–386
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
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
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
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
Wightman FL, Kistler DJ (1989a) Headphone simulation of free-field listening I. Stimulus synthesis. J Acoust Soc Am 85:858–867
Wightman FL, Kistler DJ (1989b) Headphone simulation of free-field listening II. Psychophysical validation. J Acoust Soc Am 85:868–878
Wightman FL, Kistler DJ (1992) The dominant role of low-frequency interaural time differences in sound localization. J Acoust Soc Am 91:1648–1661
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
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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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