Abstract
Barn owls do not immediately approach a source after they hear a sound, but wait for a second sound before they strike. This represents a gain in striking behavior by avoiding responses to random incidents. However, the first stimulus is also expected to change the threshold for perceiving the subsequent second sound, thus possibly introducing some costs. We mimicked this situation in a behavioral double-stimulus paradigm utilizing saccadic head turns of owls. The first stimulus served as an adapter, was presented in frontal space, and did not elicit a head turn. The second stimulus, emitted from a peripheral source, elicited the head turn. The time interval between both stimuli was varied. Data obtained with double stimulation were compared with data collected with a single stimulus from the same positions as the second stimulus in the double-stimulus paradigm. Sound-localization performance was quantified by the response latency, accuracy, and precision of the head turns. Response latency was increased with double stimuli, while accuracy and precision were decreased. The effect depended on the inter-stimulus interval. These results suggest that waiting for a second stimulus may indeed impose costs on sound localization by adaptation and this reduces the gain obtained by waiting for a second stimulus.
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References
Bee MA, Klump GM (2004) Primitive auditory stream segregation: a neurophysiological study in the songbird forebrain. J Neurophysiol 92:1088–1104. doi:10.1152/jn.00884.2003
Bee MA, Klump GM (2005) Auditory stream segregation in the songbird forebrain: effects of time intervals on responses to interleaved tone sequences. Brain Behav Evol 66:197–214. doi:10.1159/000087854
Bee MA, Micheyl C, Oxenham AJ, Klump GM (2011) Neural adaptation to tone sequences in the songbird forebrain: patterns, determinants, and relation to the build-up of auditory streaming. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 196:543–557. doi:10.1007/s00359-010-0542-4
Culling JF, Summerfield Q (1998) Measurements of the binaural temporal window. Acoust Soc Am 103:3540–3553
Deatherage BH, Evans TR (1969) Binaural masking: backward, forward, and simultaneous effects. J Acoust Soc Am 46:362–371
Dyson ML, Klump GM, Gauger B (1998) Absolute hearing thresholds and critical masking ratios in the European barn owl: a comparison with other owls. J Comp Physiol A 182:695–702
Finlayson PG (1999) Post-stimulatory suppression, facilitation and tuning for delays shape responses of inferior colliculus neurons to sequential pure tones. Hear Res 131:177–194
Finlayson PG, Adam TJ (1997) Excitatory and inhibitory response adaptation in the superior olive complex affects binaural acoustic processing. Hear Res 103:1–18. doi:10.1016/S0378-5955(96)00158-X
Fischer BJ, Peña JL (2011) Owl’s behavior and neural representation predicted by Bayesian inference. Nat Neurosci. doi:10.1038/nn.2872
Gai Y, Ruhland JL, Yin TCT (2013) Effects of forward masking on sound localization in cats: basic findings with broadband maskers. J Neurophysiol 110:1600–1610. doi:10.1152/jn.00255.2013
Gutfreund Y, Knudsen EI (2006) Adaptation in the auditory space map of the barn owl. J Neurophysiol 96:813–825. doi:10.1152/jn.01144.2005
Hafter ER, Carrier SC (1970) Masking-level differences obtained with a tonal masker. J Acoust Soc Am 47:1041–1047
Hausmann L, von Campenhausen M, Endler F et al (2009) Improvements of sound localization abilities by the facial ruff of the barn owl (Tyto alba) as demonstrated by virtual ruff removal. PLoS One 4:e7721. doi:10.1371/journal.pone.0007721
Ingham NJ, McAlpine D (2004) Spike-frequency adaptation in the inferior colliculus. J Neurophysiol 91:632–645. doi:10.1152/jn.00779.2003
Itatani N, Klump GM (2009) Auditory streaming of amplitude-modulated sounds in the songbird forebrain. J Neurophysiol 101:3212–3225. doi:10.1152/jn.91333.2008
Johnen A, Wagner H, Gaese BH (2001) Spatial attention modulates sound localization in barn owls. J Neurophysiol 85:1009–1012
Knudsen EI (2007) Fundamental components of attention. Annu Rev Neurosci 30:57–78. doi:10.1146/annurev.neuro.30.051606.094256
Knudsen EI, Konishi M (1979) Mechanisms of sound localization in the barn owl (Tyto alba). J Comp Physiol A 133:13–21
Knudsen EI, Blasdel GG, Konishi M (1979) Sound localization by the barn owl (Tyto alba) measured with the search coil technique. J Comp Physiol A 133:1–11
Kollmeier B, Gilkey RH (1990) Binaural forward and backward masking: evidence for sluggishness in binaural detection. J Acoust Soc Am 87:1709–1719
Konishi M (1973) How the owl tracks its prey. Am Sci 61:414–424
Marín GJ, Durán E, Morales C et al (2012) Attentional capture? Synchronized feedback signals from the isthmi boost retinal signals to higher visual areas. J Neurosci 32:1110–1122. doi:10.1523/JNEUROSCI.4151-11.2012
May BJ, Huang AY (1996) Sound orientation behavior in cats. I. Localization of broadband noise. J Acoust Soc Am 100:1059–1069
Nelson PC, Smith ZM, Young ED (2009) Wide-dynamic-range forward suppression in marmoset inferior colliculus neurons is generated centrally and accounts for perceptual masking. J Neurosci 29:2553–2562. doi:10.1523/JNEUROSCI.5359-08.2009
Nodal FR, Bajo VM, Parsons CH et al (2008) Sound localization behavior in ferrets: comparison of acoustic orientation and approach-to-target responses. Neuroscience 154:397–408. doi:10.1016/j.neuroscience.2007.12.022
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
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
Posner MI (1980) Orienting of attention. Q J Exp Psychol 32:3–25
Singheiser M, Ferger R, von Campenhausen M, Wagner H (2012) Adaptation in the auditory midbrain of the barn owl (Tyto alba) induced by tonal double stimulation. Eur J Neurosci 35:445–456. doi:10.1111/j.1460-9568.2011.07967.x
Smiarowski RA, Carhart R (1975) Relations among temporal resolution, forward masking, and simultaneous masking. J Acoust Soc Am 57:1169–1174
Takahashi TT, Keller CH (1992) Simulated motion enhances neuronal selectivity for a sound localization cue in background noise. J Neurosci 12:4381–4390
Takahashi TT, Konishi M (1986) Selectivity for interaural time difference in the owl’s midbrain. J Neurosci 6:3413–3422
Tollin DJ, Populin LC, Moore JM et al (2005) Sound-localization performance in the cat: the effect of restraining the head. J Neurophysiol 93:1223–1234. doi:10.1152/jn.00747.2004
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
Wagner H (1993) Sound-localization deficits induced by lesions in the barn owl’s auditory space map. J Neurosci 13:371–386
Wagner H, Trinath T, Kautz D (1994) Influence of stimulus level on acoustic motion-direction sensitivity in barn owl midbrain neurons. J Neurophysiol 71:1907–1916
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, Kettler L, Orlowski J, Tellers P (2012) Neuroethology of prey capture in the barn owl (Tyto alba L.). J Physiol Paris 107:51–61. doi:10.1016/j.jphysparis.2012.03.004
Wang Y, Peña JL (2013) Direction selectivity mediated by adaptation in the owl’s inferior colliculus. J Neurosci 33:19167–19175. doi:10.1523/JNEUROSCI.2920-13.2013
Winkowski DE, Knudsen EI (2006) Top-down gain control of the auditory space map by gaze control circuitry in the barn owl. Nature 439:336–339. doi:10.1038/nature04411
Zwislocki J, Pirodda E, Rubin H (1958) On some poststimulatory effects at the threshold of audibility. J Acoust Soc Am 31:9–14
Acknowledgments
The authors thank S. Brill and D. Zaehringer for technical assistance and logistical support. This work is supported by the Deutsche Forschungsgemeinschaft (Grant WA 606/20-2).
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The authors declare that they have no conflict of interest.
Ethical standard
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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Kettler, L., Wagner, H. Influence of double stimulation on sound-localization behavior in barn owls. J Comp Physiol A 200, 1033–1044 (2014). https://doi.org/10.1007/s00359-014-0953-8
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DOI: https://doi.org/10.1007/s00359-014-0953-8