Abstract
The middle ears of birds are typically connected by interaural cavities that form a cranial canal. Eardrums coupled in this manner may function as pressure difference receivers rather than pressure receivers. Hereby, the eardrum vibrations become inherently directional. The barn owl also has a large interaural canal, but its role in barn owl hearing and specifically in sound localization has been controversial so far. We discuss here existing data and the role of the interaural canal in this species and add a new dataset obtained by laser Doppler vibrometry in a free-field setting. Significant sound transmission across the interaural canal occurred at low frequencies. The sound transmission induces considerable eardrum directionality in a narrow band from 1.5 to 3.5 kHz. This is below the frequency range used by the barn owl for locating prey, but may conceivably be used for locating conspecific callers.
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Bierman HS, Thornton JL, Jones HG et al (2014) Biophysics of directional hearing in the American alligator (Alligator mississippiensis). J Exp Biol 217:1094–1107. doi:10.1242/jeb.092866
Bühler P, Epple W (1980) Die Lautäußerungen der Schleiereule (Tyto alba). J Ornithol 121(1):36–70
Calford MB (1988) Constraints on the coding of sound frequency imposed by the avian interaural canal. J Comp Physiol A 162:491–502. doi:10.1007/BF00612514
Calford MB, Piddington RW (1988) Avian interaural canal enhances interaural delay. J Comp Physiol A 162:503–510. doi:10.1007/BF00612515
Cazettes F, Fischer BJ, Peña JL (2014) Spatial cue reliability drives frequency tuning in the barn Owl’s midbrain. Elife. doi:10.7554/eLife.04854
Christensen-Dalsgaard J (2011) Vertebrate pressure-gradient receivers. Hear Res 273:37–45. doi:10.1016/j.heares.2010.08.007
Christensen-Dalsgaard J, Manley G (2005) Directionality of the lizard ear. J Exp Biol 208:1209–1217. doi:10.1242/jeb.01511
Christensen-Dalsgaard J, Manley GA (2008) Acoustical coupling of lizard eardrums. J Assoc Res Otolaryngol 9:407–416. doi:10.1007/s10162-008-0130-2
Christensen-Dalsgaard J, Tang Y, Carr CE (2011) Binaural processing by the gecko auditory periphery. J Neurophysiol 105:1992–2004. doi:10.1152/jn.00004.2011
Coles RB, Guppy A (1988) Directional hearing in the barn owl (Tyto alba). J Comp Physiol A 163:117–133
Counter SA, Borg E (1979) Physiological activation of the stapedius muscle in Gallus gallus. Acta Otolaryngol 403:13–19
Dyson M, Klump G, Gauger B (1998) Absolute hearing thresholds and critical masking ratios in the European barn owl: a comparison with other owls. J Comp Physiol A 182(5):695–702
Hausmann L, von Campenhausen M, Wagner H (2010) Properties of low-frequency head-related transfer functions in the barn owl (Tyto alba). J Comp Physiol A 169(9):601–612. doi:10.1007/s00359-010-0546-0
Keller CH, Hartung K, Takahashi TT (1998) Head-related transfer functions of the barn owl: measurement and neural responses. Hear Res 118:13–34. doi:10.1016/S0378-5955(98)00014-8
Kettler L, Wagner H (2014) Influence of double stimulation on sound-localization behavior in barn owls. J Comp Physiol A 200(12):1033–1044. doi:10.1007/s00359-014-0953-8
Knudsen EI, Konishi M (1979) Mechanisms of sound localization in the barn owl (Tyto alba). J Comp Physiol A 133:13–21
Konishi M (1973) How the owl tracks its prey. Am Sci 61:414–424
Köppl C, Carr CE (2003) Computational diversity in the cochlear nucleus angularis of the barn owl. J Neurophysiol 89:2313–2329. doi:10.1152/jn.00635.2002
Larsen ON, Dooling RJ, Michelsen A (2006) The role of pressure difference reception in the directional hearing of budgerigars (Melopsittacus undulatus). J Comp Physiol A 192(10):1063–1072. doi:10.1007/s00359-006-0138-1
Larsen ON, Dooling RJ, Ryals BM (1997) Roles of intracranial air pressure in bird audition. In: Lewis ER, Long JR, Lyon RF et al (eds) Diversity in auditory mechanics. World Scientific, Singapore, pp 11–17
Michelsen A, Heller KG, Stumpner A, Rohrseitz K (1994) A new biophysical method to determine the gain of the acoustic trachea in bush-crickets. J Comp Physiol A 175:145–151. doi:10.1007/bf00215110
Michelsen A, Larsen ON (2008) Pressure difference receiving ears. Bioinspir Biomim 3:011001. doi:10.1088/1748-3182/3/1/011001
Moiseff A, Konishi M (1981) The owl’s interaural pathway is not involved in sound localization. J Comp Neurol 144:299–304
Norberg RA (1968) Physical factors in directional hearing in Aegolius funereus (Linné) (Strigiformes), with special reference to the significance of the asymmetry of the external ears. Ark Zool 20:181–204
Payne RS (1971) Acoustic location of prey by barn owls (Tyto alba). J Exp Biol 54:535–573
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 A 187:225–233
Singheiser M, Plachta DTT, Brill S et al (2010) Target-approaching behavior of barn owls (Tyto alba): influence of sound frequency. J Comp Physiol A 196:227–240. doi:10.1007/s00359-010-0508-6
Stellbogen E (1930) Über das äußere und mittlere Ohr des Waldkauzes (Syrnium Aluco L.). Zeitschrift für Morphol und Ökologie der Tiere 19:686–731
Takahashi TT, Moiseff A, Konishi M (1984) Time and intensity cues are processed independently in the auditory system of the owl. J Neurosci 4:1781–1786
Vonderschen K, Wagner H (2009) Tuning to interaural time difference and frequency differs between the auditory arcopallium and the external nucleus of the inferior colliculus. J Neurophysiol 101:2348–2361. doi:10.1152/jn.91196.2008
Vonderschen K, Wagner H (2012) Transformation from a pure time delay to a mixed time and phase delay representation in the auditory forebrain pathway. J Neurosci 32:5911–5923. doi:10.1523/JNEUROSCI.5429-11.2012
Vossen C, Christensen-Dalsgaard J, van Hemmen JL (2010) Analytical model of internally coupled ears. J Acoust Soc Am 128:909–918. doi:10.1121/1.3455853
Wagner H, Kettler L, Orlowski J, Tellers P (2013) Neuroethology of prey capture in the barn owl (Tyto alba L.). J Physiol 107:51–61. doi:10.1016/j.jphysparis.2012.03.004
White LB, Boashash B (1990) Cross spectral analysis of nonstationary processes. IEEE Trans Inf Theory 36:830–835. doi:10.1109/18.53742
Acknowledgments
The authors thank S. Brill for technical assistance and logistical support and K.L. Willis and C.E. Carr for providing a 3D-reconstruction of the interaural canal. This work was supported by the Deutsche Forschungsgemeinschaft (Grant WA 606/20-2).
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The owls were treated and cared for in accordance with the guidelines of the “Landespräsidium für Natur, Umwelt und Verbraucherschutz Nordrhein-Westfalen, Recklinghausen, Germany”.
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This article belongs to a Special Issue on Internally Coupled Ears.
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Kettler, L., Christensen-Dalsgaard, J., Larsen, O.N. et al. Low frequency eardrum directionality in the barn owl induced by sound transmission through the interaural canal. Biol Cybern 110, 333–343 (2016). https://doi.org/10.1007/s00422-016-0689-3
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DOI: https://doi.org/10.1007/s00422-016-0689-3