Adaptation in the auditory midbrain of the barn owl (Tyto alba) induced by tonal double stimulation

European Journal of Neuroscience

Volumn 35, Issue 3, 2012, Pages 445-456

  Singheiser, Martin ^a   Ferger, Roland ^a   von Campenhausen, Mark ^a   Wagner, Hermann ^a  

^a RWTH AACHEN UNIVERSITY   (Germany)

Author keywords

Audition; Inferior colliculus; Monaural; Sound localization

Indexed keywords

ACOUSTIC NERVE FIBER; ADAPTATION; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; AUDITORY MASKING; AUDITORY NERVOUS SYSTEM; AUDITORY RESPONSE; AUDITORY STIMULATION; CONTROLLED STUDY; EXTRACELLULAR SPACE; FEMALE; FREQUENCY MODULATION; HEARING TEST; INFERIOR COLLICULUS; MALE; MESENCEPHALON; NONHUMAN; OWL; PRIORITY JOURNAL; PURE TONE AUDIOMETRY; RESPONSE TIME; SIGNAL DETECTION;

ACOUSTIC STIMULATION; ADAPTATION, PHYSIOLOGICAL; ANIMALS; AUDITORY PATHWAYS; AUDITORY PERCEPTION; ELECTROPHYSIOLOGY; INFERIOR COLLICULI; MICE; NEURONS; SOUND LOCALIZATION; STRIGIFORMES;

EID: 84856463603     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2011.07967.x     Document Type: Article

References (78)

1. Adolphs, R. (1993) Bilateral inhibition generates neuronal responses tuned to interaural level differences in the auditory brainstem of the barn owl. J. Neurosci., 13, 3647-3668.
2. Alves-Pinto, A., Baudoux, S., Palmer, A.R. & Summer, C.J. (2010) Forward masking estimated by signal detection theory analysis of neural responses in primary auditory cortex. JARO, 11, 477-494.
3. Anderson, L.A., Christianson, G.B. & Linden, J.F. (2009) Stimulus-specific adaptation occurs in the auditory thalamus. J. Neurosci., 29, 7359-7363.
4. Bee, M.A. & Klump, G.M. (2004) Primitive auditory stream segregation: a neurophysiological study in the songbird forebrain. J. Neurophysiol., 92, 1088-1104.
5. Bee, M.A. & Klump, G.M. (2005) Auditory stream segregation in the songbird forebrain: effects of time intervals on responses to interleaved tone sequences. Brain Behav. Evol., 66, 197-214.
6. Benda, J. & Herz, A.V.M. (2003) A universal model for spike-frequency adaptation. Neural Comput., 15, 2523-2564.
7. Benda, J., Longtin, A. & Maler, L. (2005) Spike-frequency adaptation separates transient communication signals from background oscillations. J. Neurosci., 25, 2312-2321.
8. Blauert, J. (1997) Spatial Hearing. MIT Press, Cambridge.
9. Bleeck, S., Sayles, M., Ingham, N. & Winter, I.M. (2006) The time course of recovery from suppression and facilitation from single units in the mammalian cochlear nucleus. Hear. Res., 212, 176-184.
10. Boettcher, F.A., Salvi, R.J. & Saunders, S.S. (1990) Recovery from short-term adaptation in single neurons in the cochlear nucleus. Hear. Res., 48, 125-144.
11. Brenner, N., Bialek, W. & de Ruyter van Steveninck, R. (2000) Information transmission. Neuron, 26, 695-702.
12. Brosch, M. & Schreiner, C. (1997) Time course of forward masking tuning curves in cat primary auditory cortex. J. Neurophysiol., 77, 923-943.
13. Chimento, T.C. & Schreiner, C.E. (1990) Time course of adaptation and recovery from adaptation in the cat auditory-nerve neurophonic. J. Acoust. Soc. Am, 88, 857-864.
14. Christianson, G.B. & Pena, J.L. (2006) Noise reduction of coincidence detector output by the inferior colliculus of the barn owl. J. Neurosci., 26, 5948-5954.
15. Cohen, Y.E. & Knudsen, E.I. (1998) Representation of binaural spatial cues in field L of the barn owl forebrain. J. Neurophysiol., 79, 879-890.
16. Crumling, M.A. & Saunders, J.A. (2007) Tonotopic distribution of short-term adaptation properties in the cochlear nerve of normal and acoustically overexposed chicks. J. Assoc. Res. Otolarnygol., 68, 4-68.
17. Dean, I., Harper, N.S. & McAlpine, D. (2005) Neural population coding of sound level adapts to stimulus statistics. Nat. Neurosci., 8, 1684-1689.
18. Dean, I., Robinson, B.L., Harper, N.S. & McAlpine, D. (2008) Rapid neural adaptation to sound level statistics. J. Neurosci., 28, 6430-6438.
19. Finlayson, P.G. (1999) Post-stimulatory suppression, facilitation and tuning for delays shape responses of inferior colliculus neurons to sequential pure tones. Hear. Res., 131, 177-194.
20. Finlayson, P.G. (2002) Paired-tone stimuli reveal reductions and alternations in temporal processing in inferior colliculus neurons of aged animals. J. Res. Assoc. Otolaryngol., 3, 321-331.
21. Finlayson, P.G. & Adam, T.J. (1997) Excitatory and inhibitory response adaptation in the superior olive complex affects binaural acoustic processing. Hear. Res., 103, 1-18.
22. Friedman, H.S. & Priebe, C.E. (1998) Estimating stimulus response latency. J. Neurosci. Meth., 83, 185-194.
23. Friedman, H.S. & Priebe, C.E. (1999) Smoothing bandwidth selection for response latency estimation. J. Neurosci. Meth., 87, 13-16.
24. Gutfreund, Y. & Knudsen, E.I. (2006) Adaptation in the auditory space map of the barn owl. J. Neurophysiol., 86, 813-825.
25. Ingham, N.J. & McAlpine, D. (2004) Spike-frequency adaptation in the inferior colliculus. J. Neurophysiol., 91, 632-645.
26. Ingham, N.J., Hart, H.C. & McAlpine, D. (2001) Spatial receptive fields of inferior colliculus neurons to auditory apparent motion in free field. J. Neurophysiol., 85, 23-33.
27. Keller, C.H. & Takahashi, T.T. (1996) Responses to stimulated echoes by neurons in the barn owl's auditory space map. J. Comp. Physiol. A., 178, 499-512.
28. Knudsen, E.I. (1983) Subdivisions of the inferior colliculus in the barn owl (Tyto alba). J. Comp. Neurol., 218, 174-186.
29. Knudsen, E.I. & Konishi, M. (1978) Space and frequency are represented separately in auditory midbrain of the owl. J. Neurophysiol., 41, 870-884.
30. Knudsen, E.I., Knudsen, P.F. & 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.
31. Kollmeier, B. & Gilkey, R.H. (1990) Binaural forward and backward masking: evidence for sluggishness in binaural detection. J. Acoust. Soc. Am., 87, 1709-1719.
32. Konishi, M. (1973a) How the owl tracks its prey. Am. Sci., 61, 414-424.
33. Konishi, M. (1973b) Locatable and nonlocatable acoustic signals for barn owls. Am. Nat., 107, 775-785.
34. Kuznetsova, M.S., Higgs, M.H. & Spain, W.J. (2008) Adaptation of firing rate and spike-timing precision in the avian cochlear nucleus. J. Neurosci., 28, 11906-11915.
35. Kvale, M.N. & Schreiner, C.E. (2008) Short-term adaptation of auditory receptive fields to dynamic stimuli. J. Neurophysiol., 91, 604-612.
36. Litovsky, R.Y. & Yin, T.C.T. (1998a) Physiological studies of the precedence effect in the inferior colliculus of the cat. I. Correlates of psychophysics. J. Neurophysiol., 80, 1285-1301.
37. Litovsky, R.Y. & Yin, T.C.T. (1998b) Physiological studies of the precedence effect in the inferior colliculus of the cat. II. Neural mechanisms. J. Neurophysiol., 80, 1302-1316.
38. Malmierca, M.S., Cristaudo, S., Perez-Gonzalez, D. & Covey, E. (2009) Stimulus-specific adaptation in the inferior colliculus of the anesthetized rat. J. Neurosci., 29, 5483-5493.
39. Marìn, G., Salas, C., Sentis, E., Rojas, X., Letelier, J.C. & Mpodozis, J. (2007) A cholinergic gating mechanism controlled by competitive interactions in the optic tectum of the pigeon. J. Neurosci., 27, 8112-8121.
40. Mazer, J.A. (1998) How the owl resolves auditory coding ambiguity. Proc. Natl. Acad. Sci. USA, 95, 10932-10937.
41. McAlpine, D. & Palmer, A.R. (2002) Blocking GABAergic inhibition increases sensitivity to sound motion cues in the inferior colliculus. J. Neurosci., 22, 1443-1453.
42. McAlpine, D., Jiang, D., Shackleton, T.M. & Palmer, A.R. (2000) Responses of neurons in the inferior colliculus to dynamic interaural phase cues: evidence for a mechanism of binaural adaptation. J. Neurophysiol., 83, 1356-1365.
43. Mysore, S.P., Asadollahi, A. & Knudsen, E.I. (2011) Signalling of the strongest stimulus in the owl optic tectum. J. Neurosci., 31, 5186-5196.
44. Nelson, B.S. & Takahashi, T.T. (2008) Independence of echo-threshold and echo-delay in the barn owl. PLoS One, 3, e3598.
45. Nelson, B.S. & Takahashi, T.T. (2010) Spatial hearing in echoic environments: the role of envelope in owls. Neuron, 67, 643-655.
46. Nelson, P.C. & Young, E.D. (2010) Neural correlates of context-dependent perceptual enhancement in the inferior colliculus. J. Neurosci., 30, 6577-6587.
47. Nelson, P.C., Smith, Z.M. & Young, E.D. (2009) Wide-dynamic range forward suppression in marmoset inferior colliculus neurons is generated centrally and accounts for perceptual masking. J. Neurosci., 29, 2553-2562.
48. Park, T.J., Brand, A., Koch, U., Ikebuchi, M. & Grothe, B. (2008) Dynamic ranges in level influence spatial coding in the lateral superior olive. Hear. Res., 238, 58-67.
49. Payne, R.S. (1962) How the barn owl locates prey by hearing. Living Bird, 1, 151-159.
50. Payne, R.S. (1971) Acoustic location of prey by barn owls (Tyto alba). J. Exp. Biol., 54, 535-573.
51. Pena, J.L. & deBello, W.M. (2010) Auditory processing, plasticity, and learning in the barn owl. ILAR J., 51, 338-352.
52. Pena, J.L., Viete, S., Funabiki, K., Saberi, K. & Konishi, M. (2001) Cochlear and neural delays for coincidence detection in owls. J. Neurosci., 21, 9455-9459.
53. Pérez, M.L. & Pena, J.L. (2006) Comparison of midbrain and thalamic space-specific neurons in barn owls. J. Neurophysiol., 95, 783-790.
54. Pérez, M.L., Shanbhag, S.J. & Pena, J.L. (2009) Auditory spatial tuning in the crossroads of the midbrain and the forebrain. J. Neurophysiol., 102, 1472-1482.
55. Peron, S.P. & Gabbiani, F. (2009) Role of spike-frequency adaptation in shaping neuronal response to dynamic stimuli. Biol. Cybern., 100, 505-520.
56. Reches, A. & Gutfreund, Y. (2008) Stimulus-specific adaptations in the gaze control system of the barn owl. J. Neurosci., 28, 1523-1533.
57. Reches, A., Netser, S. & Gutfreund, Y. (2010) Interactions between stimulus-specific adaptation and visual auditory integration in the forebrain of the barn owl. J. Neurosci., 30, 6991-6998.
58. Roche, B.E., Schult-Hostedde, A.I. & Brooks, R.J. (1999) Route choice by deer mice (Peromyscus maniculatus): reducing the risk of auditory detection by predators. Am. Midl. Nat., 142, 194-197.
59. Scholes, C., Palmer, A.R. & Summer, C.J. (2011) Forward suppression in the auditory cortex is frequency-specific. Eur. J. Neurosci., 33, 1240-1251.
60. Singheiser, M., Fischer, B.J. & Wagner, H. (2010) Estimated cochlear delays in low best-frequency neurons in the barn owl cannot explain coding of interaural time difference. J. Neurophysiol., 104, 1946-1954.
61. Spitzer, M.W. & Takahashi, T.T. (2006) Sound localization by barn owls in a simulated echoic environment. J. Neurophysiol., 95, 3571-3584.
62. Spitzer, M.W., Bala, A.D. & Takahashi, T.T. (2003) Auditory spatial discrimination by barn owls in simulated echoic conditions. J. Acoust. Soc. Am., 113, 1631-1645.
63. Spitzer, M.W., Bala, A.D. & Takahashi, T.T. (2004) A neuronal correlate of the precedence effect is associated with spatial selectivity in the barn owl's auditory midbrain. J. Neurophysiol., 92, 2051-2070.
64. Takahashi, T.T. (2010) How the owl tracks its prey - II. J. Exp. Biol., 213, 3399-3408.
65. Takahashi, T.T. & 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.
66. Takahashi, T.T., 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.
67. Tollin, D.J., Populin, L.C. & Yin, T.C.T. (2004) Neural correlates of the precedence effect in the inferior colliculus of behaving cats. J. Neurophysiol., 92, 3286-3297.
68. Ulanovsky, N., Las, L., Farkas, D. & Nelken, I. (2004) Multiple time scales of adaptation in auditory cortex neurons. J. Neurosci., 24, 10440-10453.
69. 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.
70. Wagner, H. (1990) Receptive fields of neurons in the owl's auditory brainstem change dynamically. Eur. J. Neurosci., 2, 949-959.
71. Wagner, H. (1992) On the ability of neurons in the barn owl's inferior colliculus to sense brief appearances of interaural time difference. J. comp. Physiol., A170, 3-11.
72. Wagner, H., Mazer, J.A. & 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, 343-1352.
73. 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.
74. 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.
75. Wen, B., Wang, G.I., Dean, I. & Delgutte, B. (2009) Dynamic range adaptation to sound level statistics in the auditory nerve. J. Neurosci., 29, 13797-13808.
76. Yates, G.K., Robertson, D. & Johnstone, B.M. (1985) Very rapid adaptation in the guinea pig auditory nerve. Hear. Res., 17, 1-12.
77. Yin, T.C.T. (1994) Physiological correlates of the precedence effect and summing localization in the inferior colliculus of the cat. J. Neurosci., 14, 5170-5186.
78. Zilany, M.S. & Carney, L.H. (2010) Power-law dynamics in an auditory nerve model can account for neural adaptation to sound-level statistics. J. Neurosci., 30, 10380-10390.