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Published in: Journal of the Association for Research in Otolaryngology 6/2016

01-12-2016 | Research Article

The Binaural Interaction Component in Barn Owl (Tyto alba) Presents few Differences to Mammalian Data

Authors: Nicolas Palanca-Castan, Geneviève Laumen, Darrin Reed, Christine Köppl

Published in: Journal of the Association for Research in Otolaryngology | Issue 6/2016

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Abstract

The auditory brainstem response (ABR) is an evoked potential that reflects the responses to sound by brainstem neural centers. The binaural interaction component (BIC) is obtained by subtracting the sum of the monaural ABR responses from the binaural response. Its latency and amplitude change in response to variations in binaural cues. The BIC is thus thought to reflect the activity of binaural nuclei and is used to non-invasively test binaural processing. However, any conclusions are limited by a lack of knowledge of the relevant processes at the level of individual neurons. The aim of this study was to characterize the ABR and BIC in the barn owl, an animal where the ITD-processing neural circuits are known in great detail. We recorded ABR responses to chirps and to 1 and 4 kHz tones from anesthetized barn owls. General characteristics of the barn owl ABR were similar to those observed in other bird species. The most prominent peak of the BIC was associated with nucleus laminaris and is thus likely to reflect the known processes of ITD computation in this nucleus. However, the properties of the BIC were very similar to previously published mammalian data and did not reveal any specific diagnostic features. For example, the polarity of the BIC was negative, which indicates a smaller response to binaural stimulation than predicted by the sum of monaural responses. This is contrary to previous predictions for an excitatory-excitatory system such as nucleus laminaris. Similarly, the change in BIC latency with varying ITD was not distinguishable from mammalian data. Contrary to previous predictions, this behavior appears unrelated to the known underlying neural delay-line circuitry. In conclusion, the generation of the BIC is currently inadequately understood and common assumptions about the BIC need to be reconsidered when interpreting such measurements.
Literature
go back to reference Calvo C, Moiseff A (1992) Neural correlates of interaural time processing in the auditory evoked potentials of the barn owl. Soc Neurosci Abstr 18:149 Calvo C, Moiseff A (1992) Neural correlates of interaural time processing in the auditory evoked potentials of the barn owl. Soc Neurosci Abstr 18:149
go back to reference Calvo C, Moiseff A (1993) Monitoring of the binaural interaction in the immature barn owl. Soc Neurosci Abstr 19:531 Calvo C, Moiseff A (1993) Monitoring of the binaural interaction in the immature barn owl. Soc Neurosci Abstr 19:531
go back to reference Carr CE, Konishi M (1990) A circuit for detection of interaural time differences in the brain stem of the barn owl. J Neurosci 10:3227–3246PubMed Carr CE, Konishi M (1990) A circuit for detection of interaural time differences in the brain stem of the barn owl. J Neurosci 10:3227–3246PubMed
go back to reference Gaumond RP, Psaltikidou M (1991) Models for the generation of the binaural difference response. J Acoust Soc Am 89:454–456CrossRefPubMed Gaumond RP, Psaltikidou M (1991) Models for the generation of the binaural difference response. J Acoust Soc Am 89:454–456CrossRefPubMed
go back to reference Goldberg JM, Brown PB (1968) Functional organization of the dog superior olivary complex: an anatomical and electrophysiological study. J Neurophysiol 31:639–656PubMed Goldberg JM, Brown PB (1968) Functional organization of the dog superior olivary complex: an anatomical and electrophysiological study. J Neurophysiol 31:639–656PubMed
go back to reference Goldberg JM, Brown PB (1969) Response of binaural neurons of dog superior olivary complex to dichotic tonal stimuli: some physiological mechanisms of sound localization. J Neurophysiol 32:613–636PubMed Goldberg JM, Brown PB (1969) Response of binaural neurons of dog superior olivary complex to dichotic tonal stimuli: some physiological mechanisms of sound localization. J Neurophysiol 32:613–636PubMed
go back to reference Granzow M, Riedel H, Kollmeier B (2001) Single-sweep-bades methods to improve the quality of auditory brain stem responses part I: optimized linear filtering. Z Audiol 40:32–44CrossRef Granzow M, Riedel H, Kollmeier B (2001) Single-sweep-bades methods to improve the quality of auditory brain stem responses part I: optimized linear filtering. Z Audiol 40:32–44CrossRef
go back to reference Grothe B (2000) The evolution of temporal processing in the medial superior olive, an auditory brainstem structure. Prog Neurobiol 61:581–610CrossRefPubMed Grothe B (2000) The evolution of temporal processing in the medial superior olive, an auditory brainstem structure. Prog Neurobiol 61:581–610CrossRefPubMed
go back to reference Huang CM, Buchwald JS (1978) Factors that affect the amplitudes and latencies of the vertex short latency acoustic responses in the cat. Electroencephalogr Clin Neurophysiol 44:179–186CrossRefPubMed Huang CM, Buchwald JS (1978) Factors that affect the amplitudes and latencies of the vertex short latency acoustic responses in the cat. Electroencephalogr Clin Neurophysiol 44:179–186CrossRefPubMed
go back to reference Jones SJ, Van der Poel JC (1990) Binaural interaction in the brain-stem auditory evoked potential: evidence for a delay line coincidence detection mechanism. Electroencephalogr Clin Neurophysiol Potentials Sect 77:214–224. doi:10.1016/0168-5597(90)90040-K CrossRef Jones SJ, Van der Poel JC (1990) Binaural interaction in the brain-stem auditory evoked potential: evidence for a delay line coincidence detection mechanism. Electroencephalogr Clin Neurophysiol Potentials Sect 77:214–224. doi:10.​1016/​0168-5597(90)90040-K CrossRef
go back to reference Joris PX, Yin TC (1995) Envelope coding in the lateral superior olive. I Sensitivity to interaural time differences J Neurophysiol 73:1043–1062PubMed Joris PX, Yin TC (1995) Envelope coding in the lateral superior olive. I Sensitivity to interaural time differences J Neurophysiol 73:1043–1062PubMed
go back to reference Karino S, Smith PH, Yin TC, et al. (2011) Axonal branching patterns as sources of delay in the mammalian auditory brainstem: a re-examination. J Neurosci 31:3016–3031CrossRefPubMedPubMedCentral Karino S, Smith PH, Yin TC, et al. (2011) Axonal branching patterns as sources of delay in the mammalian auditory brainstem: a re-examination. J Neurosci 31:3016–3031CrossRefPubMedPubMedCentral
go back to reference Köppl C (1997a) Phase locking to high frequencies in the auditory nerve and cochlear nucleus magnocellularis of the barn owl, Tyto alba. J Neurosci 17:3312–3321PubMed Köppl C (1997a) Phase locking to high frequencies in the auditory nerve and cochlear nucleus magnocellularis of the barn owl, Tyto alba. J Neurosci 17:3312–3321PubMed
go back to reference Köppl C (1997b) Frequency tuning and spontaneous activity in the auditory nerve and cochlear nucleus magnocellularis of the barn owl Tyto alba. J Neurophysiol 77:364–377PubMed Köppl C (1997b) Frequency tuning and spontaneous activity in the auditory nerve and cochlear nucleus magnocellularis of the barn owl Tyto alba. J Neurophysiol 77:364–377PubMed
go back to reference Larsen O, Dooling R, Ryals BM (1997) Roles of intracranial air pressure in bird audition. In: Lewis ER, Long GR, Lyon RF, Narins PM, Steele CR, Hecht-Poinar E (eds) Diversity in auditory mechanics. World Scientific, Singapore, pp. 11–17 Larsen O, Dooling R, Ryals BM (1997) Roles of intracranial air pressure in bird audition. In: Lewis ER, Long GR, Lyon RF, Narins PM, Steele CR, Hecht-Poinar E (eds) Diversity in auditory mechanics. World Scientific, Singapore, pp. 11–17
go back to reference Laumen G, Ferber AT, Klump GM, Tollin DJ (2016a) The physiological basis and clinical use of the binaural interaction component of the auditory brainstem response. Ear Hear doi. doi:10.1097/AUD.0000000000000301 Laumen G, Ferber AT, Klump GM, Tollin DJ (2016a) The physiological basis and clinical use of the binaural interaction component of the auditory brainstem response. Ear Hear doi. doi:10.​1097/​AUD.​0000000000000301​
go back to reference Manley GA, Köppl C, Konishi M (1988) A neural map of interaural intensity differences in the brain stem of the barn owl. J Neurosci 8:2665–2676PubMed Manley GA, Köppl C, Konishi M (1988) A neural map of interaural intensity differences in the brain stem of the barn owl. J Neurosci 8:2665–2676PubMed
go back to reference Moiseff A, Konishi M (1983) Binaural characteristics of units in the owl’s brainstem auditory pathway: precursors of restricted spatial receptive fields. J Neurosci 3:2553–2562PubMed Moiseff A, Konishi M (1983) Binaural characteristics of units in the owl’s brainstem auditory pathway: precursors of restricted spatial receptive fields. J Neurosci 3:2553–2562PubMed
go back to reference Myoga MH, Lehnert S, Leibold C, Felmy F, Grothe B (2014) Glycinergic inhibition tunes coincidence detection in the auditory brainstem. Nat Commun 5:3790CrossRefPubMedPubMedCentral Myoga MH, Lehnert S, Leibold C, Felmy F, Grothe B (2014) Glycinergic inhibition tunes coincidence detection in the auditory brainstem. Nat Commun 5:3790CrossRefPubMedPubMedCentral
go back to reference Overholt EM, Rubel EW, Hyson RL (1992) A circuit for coding interaural time differences in the chick brainstem. J Neurosci 12:1698–1708PubMed Overholt EM, Rubel EW, Hyson RL (1992) A circuit for coding interaural time differences in the chick brainstem. J Neurosci 12:1698–1708PubMed
go back to reference Peña 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 16:7046–7054PubMed Peña 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 16:7046–7054PubMed
go back to reference Pratt H, Polyakov A, Aharonson V, et al. (1998) Effects of localized pontine lesions on auditory brain-stem evoked potentials and binaural processing in humans. Electroencephalogr Clin Neurophysiol 108:511–520CrossRefPubMed Pratt H, Polyakov A, Aharonson V, et al. (1998) Effects of localized pontine lesions on auditory brain-stem evoked potentials and binaural processing in humans. Electroencephalogr Clin Neurophysiol 108:511–520CrossRefPubMed
go back to reference Riedel H, Granzow M, Kollmeier B (2001) Single-sweep-based methods to improve the quality of auditory brain stem responses part II: averaging methods. Zeitschrift für Audiol 40:62–85 Riedel H, Granzow M, Kollmeier B (2001) Single-sweep-based methods to improve the quality of auditory brain stem responses part II: averaging methods. Zeitschrift für Audiol 40:62–85
go back to reference Tollin DJ (2003) The lateral superior olive: a functional role in sound source localization. Neuroscientist 9:127–143CrossRefPubMed Tollin DJ (2003) The lateral superior olive: a functional role in sound source localization. Neuroscientist 9:127–143CrossRefPubMed
go back to reference Ungan P, Yagcioglu S (2002) Origin of the binaural interaction component in wave P4 of the short-latency auditory evoked potentials in the cat: evaluation of serial depth recordings from the brainstem. Hear Res 167:81–101. doi:10.1016/S0378-5955(02)00351-9 CrossRefPubMed Ungan P, Yagcioglu S (2002) Origin of the binaural interaction component in wave P4 of the short-latency auditory evoked potentials in the cat: evaluation of serial depth recordings from the brainstem. Hear Res 167:81–101. doi:10.​1016/​S0378-5955(02)00351-9 CrossRefPubMed
go back to reference Ungan P, Yagcioglu S, Özmen B (1997) Interaural delay-dependent changes in the binaural difference potential in cat auditory brainstem response: implications about the origin of the binaural interaction component. Hear Res 106:66–82. doi:10.1016/S0378-5955(97)00003-8 CrossRefPubMed Ungan P, Yagcioglu S, Özmen B (1997) Interaural delay-dependent changes in the binaural difference potential in cat auditory brainstem response: implications about the origin of the binaural interaction component. Hear Res 106:66–82. doi:10.​1016/​S0378-5955(97)00003-8 CrossRefPubMed
go back to reference Wada S, Starr A (1989) Anatomical bases of binaural interaction in auditory brainstem responses from guinea pig Wada S, Starr A (1989) Anatomical bases of binaural interaction in auditory brainstem responses from guinea pig
go back to reference Wada SI, Starr A (1983a) Generation of auditory brain stem responses (ABRs). I. Effects of injection of a local anesthetic (procaine HCI) into the trapezoid body of Guinea pigs and cat. Electroencephalogr Clin Neurophysiol 56:326–339CrossRefPubMed Wada SI, Starr A (1983a) Generation of auditory brain stem responses (ABRs). I. Effects of injection of a local anesthetic (procaine HCI) into the trapezoid body of Guinea pigs and cat. Electroencephalogr Clin Neurophysiol 56:326–339CrossRefPubMed
go back to reference Wada SI, Starr A (1983b) Generation of auditory brain stem responses (ABRs). III. Effects of lesions of the superior olive, lateral lemniscus and inferior colliculus on the ABR in Guinea pig. Electroencephalogr Clin Neurophysiol 56:352–366CrossRefPubMed Wada SI, Starr A (1983b) Generation of auditory brain stem responses (ABRs). III. Effects of lesions of the superior olive, lateral lemniscus and inferior colliculus on the ABR in Guinea pig. Electroencephalogr Clin Neurophysiol 56:352–366CrossRefPubMed
go back to reference Wada SI, Starr A (1983c) Generation of auditory brain stem responses (ABRs). II. Effects of surgical section of the trapezoid body on the ABR in Guinea pigs and cat. Electroencephalogr Clin Neurophysiol 56:340–351CrossRefPubMed Wada SI, Starr A (1983c) Generation of auditory brain stem responses (ABRs). II. Effects of surgical section of the trapezoid body on the ABR in Guinea pigs and cat. Electroencephalogr Clin Neurophysiol 56:340–351CrossRefPubMed
go back to reference Wernick JS, Starr A (1968) Binaural interaction in the superior olivary complex of the cat: an analysis of field potentials evoked by binaural-beat stimuli. J Neurophysiol 31:428–441PubMed Wernick JS, Starr A (1968) Binaural interaction in the superior olivary complex of the cat: an analysis of field potentials evoked by binaural-beat stimuli. J Neurophysiol 31:428–441PubMed
go back to reference Young SR, Rubel EW (1983) Frequency-specific projections of individual neurons in chick brainstem auditory nuclei. J Neurosci 3:1373–1378PubMed Young SR, Rubel EW (1983) Frequency-specific projections of individual neurons in chick brainstem auditory nuclei. J Neurosci 3:1373–1378PubMed
go back to reference Zaaroor M, Starr A (1991) Auditory brain-stem evoked potentials in cat after kainic acid induced neuronal loss. I. Superior olivary complex. Electroencephalogr Clin Neurophysiol 80:422–435CrossRefPubMed Zaaroor M, Starr A (1991) Auditory brain-stem evoked potentials in cat after kainic acid induced neuronal loss. I. Superior olivary complex. Electroencephalogr Clin Neurophysiol 80:422–435CrossRefPubMed
Metadata
Title
The Binaural Interaction Component in Barn Owl (Tyto alba) Presents few Differences to Mammalian Data
Authors
Nicolas Palanca-Castan
Geneviève Laumen
Darrin Reed
Christine Köppl
Publication date
01-12-2016
Publisher
Springer US
Published in
Journal of the Association for Research in Otolaryngology / Issue 6/2016
Print ISSN: 1525-3961
Electronic ISSN: 1438-7573
DOI
https://doi.org/10.1007/s10162-016-0583-7

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