Sound localization in barn owls studied with manipulated head-related transfer functions: beyond broadband interaural time and level differences.
Auditory
Head-related transfer function
Interaural time disparity
Midbrain
Sound localization
Journal
Journal of comparative physiology. A, Neuroethology, sensory, neural, and behavioral physiology
ISSN: 1432-1351
Titre abrégé: J Comp Physiol A Neuroethol Sens Neural Behav Physiol
Pays: Germany
ID NLM: 101141792
Informations de publication
Date de publication:
07 2020
07 2020
Historique:
received:
22
07
2019
accepted:
13
02
2020
revised:
06
02
2020
pubmed:
7
3
2020
medline:
8
9
2021
entrez:
7
3
2020
Statut:
ppublish
Résumé
Interaural time and level differences are important cues for sound localization. We wondered whether the broadband information contained in these two cues could fully explain the behavior of barn owls and responses of midbrain neurons in these birds. To tackle this problem, we developed a novel approach based on head-related transfer functions. These filters contain the complete information present at the eardrum. We selected positions in space characterized by equal broadband interaural time and level differences. Stimulation from such positions provides reduced information to the owl. We show that barn owls are able to discriminate between such positions. In many cases, but not all, the owls may have used spectral components of interaural level differences that exceeded the known behavioral resolution and variability for discrimination. Alternatively, the birds may have used template matching. Likewise, neurons in the optic tectum of the barn owl, a nucleus involved in sensorimotor integration, contained more information than is available in the broadband interaural time and level differences. Thus, these data show that more information is available and used by barn owls for sound localization than carried by broadband interaural time and level differences.
Identifiants
pubmed: 32140774
doi: 10.1007/s00359-020-01410-0
pii: 10.1007/s00359-020-01410-0
doi:
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
477-498Références
Alves-Pinto A, Palmer AR, Lopez-Poveda EA (2014) Perception and coding of high-frequency spectral notches: potential implications for sound localization. Front Neurosci 8:112. https://doi.org/10.3389/fnins.2014.00112.eCollection
doi: 10.3389/fnins.2014.00112.eCollection
pubmed: 24904258
pmcid: 4034511
Anbuhl KL, Benichoux V, Greene NTR, Brown AD, Tollin DJ (2017) Development of the head, pinnae, and acoustical cues to sound location in a precocial species, the guinea pig (Cavia porcellus). Hear Res 356:35–50
pubmed: 29128159
pmcid: 5705338
Arthur BJ (2004) Sensitivity to spectral interaural intensity difference cues in space-specific neurons of the barn owl. J Comp Physiol A 190:91–104
Bala AD, Spitzer MW, Takahashi TT (2003) Prediction of auditory spatial acuity from neural images on the owl's auditory space map. Nature 424:771–774
pubmed: 12917684
Blauert J (1997) Spatial hearing. Revised edition. MIT Press, Cambridge
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
pubmed: 1556303
Bremen P, Poganiatz I, von Campenhausen H, Wagner H (2007) 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
Cazettes F, Fischer BJ, Pena JL (2014) Spatial cue reliability drives frequency tuning in the barn owl's midbrain. eLife 3:e04854
pubmed: 25531067
pmcid: 4291741
Cazettes F, Fischer BJ, Pena JL (2016) Cue reliability represented in the shape of tuning curves in the owl’s sound localization system. J Neurosci 36:2101–2110
pubmed: 26888922
pmcid: 4756150
Cazettes F, Fischer BJ, Beckert MV, Pena JL (2018) Emergence of an adaptive command from orienting behaviour in premotor brainstem neurons of barn owls. J Neurosci 38:7270–7279
pubmed: 30012694
pmcid: 6096042
Day ML, Delgutte B (2013) Decoding sound source location and separation using neural population activity patterns. J Neurosci 33:15837–15847
pubmed: 24089491
pmcid: 3787502
De Bello WM, Knudsen EI (2004) Multiple sites of adaptive plasticity in the owl's auditory localization pathway. J Neurosci 24:6853–6861
Dietz M, Lestang JH, Majdak P, Stern RM, Marquardt T, Ewert SD, Hartmann WM, Goodman DFM (2018) A framework for testing and comparing binaural models. Hear Res 360:92–106
pubmed: 29208336
Du Lac S, Knudsen EI (1990) Neural maps of head movement vector and speed in the optic tectum of the barn owl. J Neurophysiol 63:131–146
pubmed: 2299378
Dyson ML, Klump GM, Gauger B (1998) Absolute hearing thresholds and critical masking ratios in the barn owl: a comparison with other owls. J Comp Physiol A 182:695–702
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 A 187:589–595
pubmed: 11763957
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: 11756512
pmcid: 6757622
Ferger R, Pawlowsky K, Singheiser M, Wagner H (2018) Response adaptation in the barn owl's auditory space map. J Neurophysiol 119:1235–1247
pubmed: 29357460
Fischer BJ, Pena JL (2011) Owl's behavior and neural representation predicted by Bayesian inference. Nat Neurosci 14:1061–1066
pubmed: 21725311
pmcid: 3145020
Fischer BJ, Pena JL (2017) Optimal nonlinear cue integration for sound localization. J Comput Neurosci 42:37–52. https://doi.org/10.1007/s10827-016-0626-4
doi: 10.1007/s10827-016-0626-4
pubmed: 27714569
Grothe B (2018) How the barn owl computes auditory space. Trends Neurosci 41:115–117. https://doi.org/10.1016/j.tins.2018.01.004
doi: 10.1016/j.tins.2018.01.004
pubmed: 29499770
Hausmann L, von Campenhausen M, Endler F, Singheiser M, Wagner H (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
pubmed: 19890389
pmcid: 2766829
Keating P, Nodal FR, Gananandan K, Schulz AL, King AJ (2013) Behavioral sensitivity to broadband binaural localization cues in the ferret. J Assoc Res Otolaryngol 14:561–572
pubmed: 23615803
pmcid: 3705081
Keating P, Nodal FR, King AJ (2014) Behavioural sensitivity to binaural spatial cues in ferrets: evidence for plasticity in the duplex theory of sound localization. Eur J Neurosci 39:197–206
pubmed: 24256073
Keller CH, Hartung K, Takahashi TT (1998) Head-related transfer functions of the barn owl: measurement and neural responses. Hear Res 118:13–34
pubmed: 9606058
Kettler L, Griebel H, Ferger R, Wagner H (2017) Combination of interaural level and time difference in azimuthal sound localization in owls. eNeuro 4:1–13. https://doi.org/10.1523/ENEURO.0238-17.2017
doi: 10.1523/ENEURO.0238-17.2017
Knudsen EI (1982) Auditory and visual maps of space in the optic tectum of the owl. J Neurosci 2:1177–1194
pubmed: 7119872
pmcid: 6564311
Knudsen EI, Konishi M (1978) A neural map of auditory space in the owl. Science 200:795–797
pubmed: 644324
Knudsen EI, Blasdel GG, Konishi M (1979) Sound localization by the barn owl measured with the search coil technique. J Comp Physiol 133:1–11
Koka K, Jones HG, Thornton JL, Lupo JE, Tollin DJ (2011) Sound pressure transformations by the head and pinnae of the adult Chinchilla (Chinchilla lanigera). Hear Res 272:135–147
pubmed: 20971180
Koka K, Read HL, Tollin DJ (2008) The acoustical cues to sound location in the rat: measurements of directional transfer functions. J Acoust Soc Am 123:4297–4309
pubmed: 18537381
pmcid: 2579256
Konishi M (1973) How the owl tracks its prey. Am Sci 61:414–424
Konishi M, Kenuk AS (1975) Discrimination of noise spectra by memory in the barn owl. J Comp Physiol 97:55–58
Krumm B, Klump GM, Koeppl C, Langemann U (2019) The barn owls‘ minimum audible angle. PLos One 14(8):e0220652
Majdak P, Walder T, Laback B (2013) Effect of long-term training on sound localization performance with spectrally warped and band-limited head-related transfer functions. J Acoust Soc Am 134:2148–2159
pubmed: 23967945
Middlebrooks JC (2015) Sound localization. Handb Clin Neurol 129:99–116
pubmed: 25726265
Mogdans J, Knudsen EI (1992) Adaptive adjustment of unit tuning to sound localization cues in response to monaural occlusion in developing owl optic tectum. J Neurosci 12:3473–3484
pubmed: 1527591
pmcid: 6575736
Moiseff A (1989a) Binaural disparity cues available to the barn owl for sound localization. J Comp Physiol A 164:629–636
pubmed: 2590278
Moiseff A (1989b) Bi-coordinate sound localization by the barn owl. J Comp Physiol A 164:637–644
pubmed: 2709344
Moiseff A, Konishi M (1981) Neuronal and behavioral sensitivity to binaural time differences in the owl. J Neurosci 1:40–48
pubmed: 7346557
pmcid: 6564159
Olsen JF, Knudsen EI, Esterly SD (1989) Neural maps of interaural time and intensity differences in the optic tectum of the barn owl. J Neurosci 9:2591–2605
pubmed: 2746340
pmcid: 6569751
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
pubmed: 11401202
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 Ass Res Otolaryng 2:1–21
Quine DB, Konishi M (1974) Absolute frequency discrimination in the barn owl. J comp Physiol 93:347–360
Rice JJ, May BJ, Spirou GA, Young ED (1992) Pinna-based spectral cues for sound localization in cat. Hear Res 58:132–152
pubmed: 1568936
Schnyder HA, Vanderelst D, Bartenstein S, Firzlaff U, Luksch H (2014) The avian head induces cues for sound localization in elevation. PLoS One 9:e112178
pubmed: 25390036
pmcid: 4229125
Singheiser M, Plachta DTT, Brill S, Bremen P, van der Willigen R, Wagner H (2010) Target-approaching behavior of barn owls (Tyto alba): influence of sound frequency. J Comp Physiol A 196:227–240
Slee SJ, Young ED (2010) Sound localization cues in the marmoset monkey. Hear Res 260:96–108
pubmed: 19963054
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: 12805307
pmcid: 6740778
Spezio ML, Keller CH, Marrocco RT, Takahashi TT (2000) Head-related transfer functions of the Rhesus monkey. Hear Res 144:73–88
pubmed: 10831867
Sterbing SJ, Hartung K, Hoffmann KP (2003) Spatial tuning to virtual sounds in the inferior colliculus of the guinea pig. J Neurophysiol 90:2648–2659
pubmed: 12840079
Takahashi TT (2010) How the owl tracks its prey–II. J Exp Biol 213:3399–3408. https://doi.org/10.1242/jeb.031195
doi: 10.1242/jeb.031195
pubmed: 20889819
pmcid: 2948474
Van Opstal AJ, Vliegen J, van Esch T (2017) Reconstructing spectral cues for sound localization from responses to rippled noise stimuli. PLoS One 12:e0174185
pubmed: 28333967
pmcid: 5363849
von Campenhausen M, Wagner H (2006) Influence of the facial ruff on the sound-receiving characteristics of the barn owl's ears. J Comp Physiol A 192:1073–1082
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
pubmed: 19261709
Wagner H (1993) Sound-localization deficits induced by lesions in the barn owl's space map. J Neurosci 13:371–386
pubmed: 8423481
pmcid: 6576322
Wagner H, Asadollahi A, Bremen P, Endler F, Vonderschen K, von Campenhausen M (2007) Distribution of interaural time difference in the barn owl’s inferior colliculus in the low- and high-frequency ranges. J Neurosci 27:4191–4200
pubmed: 17428997
pmcid: 6672542
Wagner H, Kettler L, Orlowski J, Tellers P (2013) Neuroethology of prey capture in the barn owl (Tyto alba L.). J Physiol (Paris) 107:51–61
Wightman FL, Kistler DJ (1989a) Headphone simulation of free field listening. I: stimulus synthesis. J Acoust Soc Am 85:858–867
pubmed: 2926000
Wightman FL, Kistler DJ (1989b) Headphone simulation of free-field listening. II: Psychophysical validation. J Acoust Soc Am 85:868–878
pubmed: 2926001
Wood KC, Town SM, Bizley JK (2019) Neurons in primary auditory cortex represent sound source location in a cue-invariant manner. Nat Commun 10:3019. https://doi.org/10.1038/s41467-019-10868-9
doi: 10.1038/s41467-019-10868-9
pubmed: 31289272
pmcid: 6616358
Young ED, Rice JJ, Tong SC (1996) Effects of pinna position on head-related transfer functions in the cat. J Acoust Soc Am 99:3064–3076
pubmed: 8642117