Inhibitory and excitatory response areas of neurons in the central nucleus of the inferior colliculus in unanesthetized chinchillas

Experimental Brain Research

Volumn 174, Issue 1, 2006, Pages 124-143

  Alkhatib, Ala ^a   Biebel, Ulrich W ^a   Smolders, Jean W T ^a  

^a Physiologisches Institut II   (Germany)

Author keywords

Excitatory response regions; Inferior colliculus; Inhibitory response regions; Multiunits; Single units; Unanesthetized chinchilla

Indexed keywords

ANIMAL EXPERIMENT; ARTICLE; AUDIOMETRY; AUDITORY RESPONSE; CHINCHILLA; CONTROLLED STUDY; INFERIOR COLLICULUS; MALE; NERVE CELL; NERVE CELL EXCITABILITY; NERVE CELL INHIBITION; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL;

ACOUSTIC STIMULATION; ANIMALS; AUDITORY PATHWAYS; CHINCHILLA; INFERIOR COLLICULI; INFERIOR COLLICULUS; MALE; MICROELECTRODES; NEURONAL PLASTICITY; NEURONS; RABBITS;

EID: 33748344036     PISSN: 00144819     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00221-006-0424-8     Document Type: Article

References (86)

1. Abeles M, Goldstein MH Jr (1972) Responses of single units in the primary auditory cortex of the cat to tones and to tone pairs. Brain Res 42:337-352
2. Amin J (1999) A single hydrophobic residue confers barbiturate sensitivity to gamma-aminobutyric acid type C receptor. Mol Pharmacol 55:411-423
3. Antkowiak B (2001) How do general anaesthetics work? Naturwissenschaften 88:201-213
4. Astl J, Popelar J, Kvasnak E, Syka J (1996) Comparison of response properties of neurons in the inferior colliculus of guinea pigs under different anesthetics. Audiology 35:335-345
5. Belelli D, Lambert JJ, Peters JA, Wafford K, Whiting PJ (1997) The interaction of the general anesthetic etomidate with the gamma-aminobutyric acid type A receptor is influenced by a single amino acid. Proc Natl Acad Sci USA 94:11031-11036
6. Biebel UW, Langner G (2002) Evidence for interactions across frequency channels in the inferior colliculus of awake chinchilla. Hear Res 169:151-168
7. Bock GR, Webster WR, Aitkin LM (1972) Discharge patterns of single units in inferior colliculus of the alert cat. J Neurophysiol 35:265-277
8. Brown M, Webster WR, Martin RL (1997) The three-dimensional frequency organization of the inferior colliculus of the cat: a 2-deoxyglucose study. Hear Res 104:57-72
9. Caird DM, Klinke R (1983) Processing of binaural stimuli by cat superior olivary complex neurons. Exp Brain Res 52:385-399
10. Caspary DM, Palombi PS, Hughes LF (2002) GABAergic inputs shape responses to amplitude modulated stimuli in the inferior colliculus. Hear Res 168:163-173
11. Davis KA (2002) Evidence of a functionally segregated pathway from dorsal cochlear nucleus to inferior colliculus. J Neurophysiol 87:1824-1835
12. Davis KA, Young ED (2000) Pharmacological evidence of inhibitory and disinhibitory neuronal circuits in dorsal cochlear nucleus. J Neurophysiol 83:926-940
13. Davis KA, Ramachandran R, May BJ (1999) Single-unit responses in the inferior colliculus of decerebrate cats. II. Sensitivity to interaural level differences. J Neurophysiol 82:164-175
14. Egorova M, Ehret G, Vartanian I, Esser KH (2001) Frequency response areas of neurons in the mouse inferior colliculus. I. Threshold and tuning characteristics. Exp Brain Res 140:145-161
15. Ehret G (1997) The auditory midbrain, a "shunting yard" of acoustical information processing. In: Ehret G, Romand R (eds) The central auditory system. Oxford University Press, Oxford, pp 259-316
16. Ehret G, Merzenich MM (1988a) Complex sound analysis (frequency resolution, filtering and spectral integration) by single units of the inferior colliculus of the cat. Brain Res 472:139-163
17. Ehret G, Merzenich MM (1988b) Neuronal discharge rate is unsuitable for encoding sound intensity at the inferior-colliculus level. Hear Res 35:1-8
18. Ehret G, Egorova M, Hage SR, Muller BA (2003) Spatial map of frequency tuning-curve shapes in the mouse inferior colliculus. Neuroreport 14:1365-1369
19. Evans EF, Zhao W (1993) Varieties of inhibition in the processing and control of processing in the mammalian cochlear nucleus. Prog Brain Res 97:117-126
20. Faingold CL, Anderson CA (1991) Loss of intensity-induced inhibition in inferior colliculus neurons leads to audiogenic seizure susceptibility in behaving genetically epilepsy-prone rats. Exp Neurol 113:354-363
21. Fubara BM, Casseday JH, Covey E, Schwartz-Bloom RD (1996) Distribution of GABA(A), GABA(B), and glycine receptors in the central auditory system of the big brown bat, Eptesicus fuscus. J Comp Neurol 369:83-92
22. Funkenstein HH, Winter P (1973) Responses to acoustic stimuli of units in the auditory cortex of awake squirrel monkeys. Exp Brain Res 18:464-488
23. Fuzessery ZM, Hall JC (1996) Role of GABA in shaping frequency tuning and creating FM sweep selectivity in the inferior colliculus. J Neurophysiol 76:1059-1073
24. Gaese BH, Ostwald J (2001) Anesthesia changes frequency tuning of neurons in the rat primary auditory cortex. J Neurophysiol 86:1062-1066
25. 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 32:613-636
26. Goldstein MH Jr, Abeles M (1975) Note on tonotopic organization of primary auditory cortex in the cat. Brain Res 100:188-191
27. Hage SR, Ehret G (2003) Mapping responses to frequency sweeps and tones in the inferior colliculus of house mice. Eur J Neurosci 18:2301-2312
28. Hernández O, Espinosa N, Pérez-González D, Malmierca MS (2005) The inferior colliculus of the rat: a quantitative analysis of monaural frequency response areas. Neuroscience 132:203-217
29. Hill KG, Geisler CD (1992) Two-tone suppression, excitation and the after effect in rate responses in auditory nerve fibres in the cat. Hear Res 64:52-60
30. Kiang NY (1968) A survey of recent developments in the study of auditory physiology. Ann Otol Rhinol Laryngol 77:656-675
31. Kiang NYS, Watanbe T, Thomas EC, Clark LF (1965) Discharge patterns of single fibers in the cat's auditory nerve. MIT Press, Cambridge
32. Koch U, Grothe B (1998) GABAergic and glycinergic inhibition sharpens tuning for frequency modulations in the inferior colliculus of the big brown bat. J Neurophysiol 80:71-82
33. Kopp-Scheinpflug C (1999) Interaktion von Exzitation und Inhibition bei der zentralnervösen Verarbeitung akustischer Information. Universität Leibzig
34. Kuwada S, Batra R, Yin TC, Oliver DL, Haberly LB, Stanford TR (1997) Intracellular recordings in response to monaural and binaural stimulation of neurons in the inferior colliculus of the cat. J Neurosci 17:7565-7581
35. Langner G, Schreiner CE (1988) Periodicity coding in the inferior colliculus of the cat. I. neuronal mechanisms. J Neurophysiol 60:1799-1822
36. Le Beau FE, Rees A, Malmierca MS (1996) Contribution of GABAand glycine-mediated inhibition to the monaural temporal response properties of neurons in the inferior colliculus. J Neurophysiol 75:902-919
37. Le Beau FEN, Malmierca MS, Rees A (2001) Iontophoresis in vivo demonstrates a key role for GABA(A) and glycinergic inhibition in shaping frequency response areas in the inferior colliculus of the guinea pig. J Neurosci 21:7303-7312
38. Liberman MC (1978) Auditory-nerve response from cats raised in a low-noise chamber. J Acoust Soc Am 63:442-455
39. Loftus WC, Bishop DC, Saint Marie RL, Oliver DL (2004) Organization of binaural excitatory and inhibitory inputs to the inferior colliculus from the superior olive. J Comp Neurol 472:330-344
40. Malmierca MS, Rees A, Le Beau FEN, Bjaalie JG (1995) Laminar organization of frequency-defined local axons within and between the inferior colliculi of the guinea pig. J Comp Neurol 357:124-144
41. Malmierca MS, Merchan MA, Henkel CK, Oliver DL (2002) Direct projections from cochlear nuclear complex to auditory thalamus in the rat. J Neurosci 22:10891-10897
42. McAlpine D, Palmer AR (2002) Blocking GABAergic inhibition increases sensitivity to sound motion cues in the inferior colliculus. J Neurosci 22:1443-1453
43. McAlpine D, Jiang D, Palmer AR (1996) Interaural delay sensitivity and the classification of low best-frequency binaural responses in the inferior colliculus of the guinea pig. Hear Res 97:136-152
44. Merzenich MM, Reid MD (1974) Representation of the cochlea within the inferior colliculus of the cat. Brain Res 77:397-415
45. Möller J (1978) Response characteristics of inferior colliculus neurons of awake cf-fm bat rhinolophus ferrumequinum-2. Two-tone stimulation. J Comp Physiol 125:227-236
46. Nagai T, Maeda T, Imai H, McGeer PL, McGeer EG (1985) Distribution of GABA-T-intensive neurons in the rat hindbrain. J Comp Neurol 231:260-269
47. Oliver DL, Huerta MF (1992) Inferior and superior colliculi. In: Webster DB, Popper AN, Fay RR (eds) The mammalian auditory pathway, vol 1. Springer, Berlin Heidelberg New York, pp 168-221
48. Oliver DL, Kuwada S, Yin TC, Haberly LB, Henkel CK (1991) Dendritic and axonal morphology of HRP-injected neurons in the inferior colliculus of the cat. J Comp Neurol 303:75-100
49. Oliver DL, Winer JA, Beckius GE, Saint Marie RL (1994) Morphology of GABAergic neurons in the inferior colliculus of the cat. J Comp Neurol 340:27-42
50. Palombi PS, Caspary DM (1996a) GABA inputs control discharge rate primarily within frequency receptive fields of inferior colliculus neurons. J Neurophysiol 75:2211-2219
51. Palombi PS, Caspary DM (1996b) Responses of young and aged Fischer 344 rat inferior colliculus neurons to binaural tonal stimuli. Hear Res 100:59-67
52. Park TJ, Pollak GD (1994) Azimuthal receptive fields are shaped by GABAergic inhibition in the inferior colliculus of the mustache bat. J Neurophysiol 72:1080-1102
53. Pedemonte M, Torterolo P, Velluti RA (1997) In vivo intracellular characteristics of inferior colliculus neurons in guinea pigs. Brain Res 759:24-31
54. Pelleg-Toiba R, Wollberg Z (1989) Tuning properties of auditory cortex cells in the awake squirrel monkey. Exp Brain Res 74:353-364
55. Pollak GD, Park TJ (1993) The effects of GABAergic inhibition on monaural response properties of neurons in the mustache bat's inferior colliculus. Hear Res 65:99-117
56. Ramachandran R, Davis KA, May BJ (1999) Single-unit responses in the inferior colliculus of decerebrate cats. I. Classification based on frequency response maps. J Neurophysiol 82:152-163
57. Reetz G, Ehret G (1999) Inputs from three brainstem sources to identified neurons of the mouse inferior colliculus. Brain Res 816:527-543
58. Roberts RC, Ribak CE (1987) GABAergic neurons and axon terminals in the brainstem auditory nuclei of the gerbil. J Comp Neurol 258:267-280
59. Romand R, Avan P (1997) Anatomical and functional aspects of the cochlear nucleus. In: Ehret G, Romand R (eds) The central auditory system. Oxford University Press, Oxford, pp 97-191
60. Sachs MB, Kiang NY (1968) Two-tone inhibition in auditory-nerve fibers. J Acoust Soc Am 43:1120-1128
61. Saint Marie RL, Morest DK, Brandon CJ (1989a) The form and distribution of GABAergic synapses on the principal cell types of the ventral cochlear nucleus of the cat. Hear Res 42:97-112
62. Saint Marie RL, Ostapoff EM, Morest DK, Wenthold RJ (1989b) Glycine-immunoreactive projection of the cat lateral superior olive: possible role in midbrain ear dominance. J Comp Neurol 279:382-396
63. Sanes DH, Malone BJ, Semple MN (1998) Role of synaptic inhibition in processing of dynamic binaural level stimuli. J Neurosci 18:794-803
64. Scheich H, Bonke BA, Bonke D, Langner G (1979) Functional organization of some auditory nuclei in the guinea fowl demonstrated by the 2-deoxyglucose technique. Cell Tissue Res 204:17-27
65. Schmiedt RA (1982) Boundaries of two-tone rate suppression of cochlear-nerve activity. Hear Res 7:335-351
66. Semple MN, Aitkin LM (1979) Representation of sound frequency and laterality by units in central nucleus of cat inferior colliculus. J Neurophysiol 42(6):1626-1639
67. Servière J, Webster WR, Calford MB (1984) Isofrequency labelling revealed by a combined [4c]-2-deoxyglucose, electrophysiological, and horseradish peroxidase study of the inferior colliculus of the cat. J Comp Neurol 228:463-477
68. Shneiderman A, Oliver DL (1989) EM autoradiographic study of the projections from the dorsal nucleus of the lateral lemniscus: a possible source of inhibitory inputs to the inferior colliculus. J Comp Neurol 286:28-47
69. Spirou GA, Young ED (1991) Organization of dorsal cochlear nucleus type-IV unit response maps and their relationship to activation by bandlimited noise. J Neurophysiol 66:1750-1768
70. Stiebler I (1986) Tone threshold mapping in the inferior colliculus of the house mouse. Neurosci Lett 65:336-340
71. Suga N (1969) Classification of inferior collicular neurones of bats in terms of responses to pure tones, FM sounds and noise bursts. J Physiol 200:555-574
72. Tan AY, Zhang LI, Merzenich MM, Schreiner CE (2004) Tone-evoked excitatory and inhibitory synaptic conductances of primary auditory cortex neurons. J Neurophysiol 92:630-643
73. Thompson AM (2005) Descending connections of the auditory midbrain. In: Winer JA, Schreiner CE (eds) The inferior colliculus. Springer, Berlin Heidelberg New York, pp 182-199
74. Thompson GC, Cortez AM, Lam M-K (1985) Localization of GABA immunoreactivity in the auditory brainstem of guinea pigs. Brain Res 339:119-122
75. Vaughn MD, Pozza MF, Lingenhohl K (1996) Excitatory acoustic responses in the inferior colliculus of the rat are increased by GABAB receptor blockade. Neuropharmacology 35:1761-1767
76. Wagner T (1994) Intrinsic properties of identified neurons in the central nucleus of mouse inferior colliculus. Neuroreport 6:89-93
77. Wehr M, Zador AM (2003) Balanced inhibition underlies tuning and sharpens spike timing in auditory cortex. Nature 426:442-446
78. Wilkinson L (2004) Classification and regression trees. SYSTAT11 Statistics I. SYSTAT software, Inc., Richmond, pp 35-56
79. Winer JA, Schreiner CE (2005) The central auditory system. In: Winer JA, Schreiner CE (eds) The inferior colliculus. Springer Berlin Heidelberg New York, pp 1-68
80. Winer JA, Larue DT, Pollak GD (1995) GABA and glycine in the central auditory system of the mustache bat: structural substrates for inhibitory neuronal organization. J Comp Neurol 355:317-353
81. Wu SH, Ma CL, Kelly JB (2004) Contribution of AMPA, NMDA, and GABA(A) receptors to temporal pattern of postsynaptic responses in the inferior colliculus of the rat. J Neurosci 24:4625-4634
82. Yamamura T, Harada K, Okamura A, Kemmotsu O (1990) Is the site of action of ketamine anesthesia the N-methyl-D-aspartate receptor? Anesthesiology 72:704-710
83. Yan J, Suga N (1996) The midbrain creates and the thalamus sharpens echo-delay tuning for the cortical representation of target-distance information in the mustached bat. Hear Res 93:102-110
84. Yan J, Zhang Y, Ehret G (2005) Corticofugal shaping of frequency tuning curves in the central nucleus of the inferior colliculus of mice. J Neurophysiol 93:71-83
85. Zhang Y, Wu SH (2000) Long-term potentiation in the inferior colliculus studied in rat brain slice. Hear Res 147:92-103
86. Zurita P, Villa AE, de Ribaupierre Y, de Ribaupierre F, Rouiller EM (1994) Changes of single unit activity in the cat's auditory thalamus and cortex associated to different anesthetic conditions. Neurosci Res 19:303-316