Differing roles of inhibition in hierarchical processing of species-specific calls in auditory brainstem nuclei

Journal of Neurophysiology

Volumn 94, Issue 6, 2005, Pages 4019-4037

  Xie, Ruili ^a   Meitzen, John ^a,b   Pollak, George D ^a  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUDITORY BRAIN STEM IMPLANT; AUDITORY SYSTEM FUNCTION; BAT; CELL POPULATION; CONTROLLED STUDY; EVOKED RESPONSE; GABAERGIC TRANSMISSION; INFERIOR COLLICULUS; INNERVATION; NERVE CELL; NERVE EXCITABILITY; NONHUMAN; PRIORITY JOURNAL; SPECIES DIFFERENCE; STIMULUS RESPONSE; SYNAPTIC INHIBITION;

ACOUSTIC STIMULATION; ACTION POTENTIALS; ANIMALS; AUDITORY PATHWAYS; BICUCULLINE; BRAIN STEM; CELL COUNT; CHIROPTERA; DOSE-RESPONSE RELATIONSHIP, RADIATION; DRUG INTERACTIONS; ECHOLOCATION; ELECTRODES; FUNCTIONAL LATERALITY; GABA ANTAGONISTS; GAMMA-AMINOBUTYRIC ACID; GLYCINE AGENTS; NEURAL INHIBITION; NEURONS; SOUND LOCALIZATION; SPECIES SPECIFICITY; STRYCHNINE;

EID: 28044432515     PISSN: 00223077     EISSN: None     Source Type: Journal    
DOI: 10.1152/jn.00688.2005     Document Type: Article

References (100)

1. Aitkin LM, Andersen DJ, and Brugge JF. Tonotopic organization and discharge characteristics of single neurons in nuclei of the lateral lemniscus of the cat. J Neurophysiol 33: 421-440, 1970.
2. Aitkin LM and Phillips SC. The interconnections of the inferior colliculi through their commissure. J Comp Neurol 228: 210-216, 1984.
3. Bartsch E and Schmidt S. Psychophysical frequency modulation thresholds in a FM-bat, Tadarida brasiliensis. Hear Res 67: 128-138, 1993.
4. Bauer EE, Klug A, and Pollak GD. Features of contralaterally evoked inhibition in the inferior colliculus. Hear Res 141: 80-96, 2000.
5. Bauer EE, Klug A, and Pollak GD. Spectral determination of responses to species-specific calls in the dorsal nucleus of the lateral lemniscus. J Neurophysiol 88: 1955-1967, 2002.
6. Bodenhamer RD and Pollak GD. Time and frequency domain processing in the inferior colliculus of echolocating bats. Hear Res 5: 317-335, 1981.
7. Boettiger CA and Doupe AJ. Intrinsic and thalamic excitatory inputs onto songbird LMAN neurons differ in their pharmacological and temporal properties. J Neurophysiol 79: 2615-2628, 1998.
8. Brand A, Urban R, and Grothe B. Duration tuning in the mouse auditory midbrain. J Neurophysiol 84: 1790-1799, 2000.
9. Brugge JF, Anderson DJ, and Aitkin LM. Responses of neurons in the dorsal nucleus of the lateral lemniscus of cat to binaural tonal stimulation. J Neurophysiol 33: 441-458, 1970.
10. Burger RM and Pollak GD. Analysis of the role of inhibition in shaping responses to sinusoidally amplitude-modulated signals in the inferior colliculus. J Neurophysiol 80: 1686-1701, 1998.
11. Burger RM and Pollak GD. Reversible inactivation of the dorsal nucleus of the lateral lemniscus reveals its role in the processing of multiple sound sources in the inferior colliculus of bats. J Neurosci 21: 4830-4843, 2001.
12. Casseday JH, Covey E, and Grothe B. Neural selectivity and tuning for sinusoidal frequency modulations in the inferior colliculus of the big brown bat, Eptesicus fuscus, J Neurophysiol 77: 1595-1605, 1997.
13. Casseday JH, Fremouw T, and Covey E. The inferior colliculus: a hub for the central auditory system. In: Integrative Functions in the Mammalian Auditory Pathway, edited by Oertel D, Popper AN, and Fay RR. New York: Springer-Verlag, 2002, p. 238-318.
14. Chen L, Kelly JB, and Wu SH. The commissure of Probst as a source of GABAergic inhibition. Hear Res 138: 106-114, 1999.
15. Clarey JC, Barone P, and Imig TJ. Physiology of thalamus and cortex. In: The Mammalian Auditory Pathway: Neurophysiology, edited by Webster DB, Popper AN, and Fay RR. New York: Springer-Verlag, 1992, p. 232-334.
16. Covey E. Response properties of single units in the dorsal nucleus of the lateral lemniscus and paralemniscal zone of an echolocating bat. J Neurophysiol 69: 842-859, 1993.
17. Covey E and Casseday JH. The monaural nuclei of the lateral lemniscus in an echolocating bat: parallel pathways for analyzing temporal features of sound. J Neurosci 11: 3456-3470, 1991.
18. Davis KA. Evidence of a functionally segregated pathway from dorsal cochlear nucleus to inferior colliculus. J Neurophysiol 87: 1824-1835, 2002.
19. Davis KA, Ramachandran R, and May BJ. Single-unit responses in the inferior colliculus of decerebrate cats. II. Sensitivity to interaural level differences. J Neurophysiol 82: 164-175, 1999.
20. Davis KA, Ramachandran R, and May BJ. Auditory processing of spectral cues for sound localization in the inferior colliculus. J Assoc Res Otolaryngol 4: 148-163, 2003.
21. Esser KH, Condon CJ, Suga N, and Kanwal JS. Syntax processing by auditory cortical neurons in the FM-FM area of the mustached bat, Pteronotus parnellii. Proc Natl Acad Sci USA 94: 14019-14024, 1997.
22. Faingold CL, Anderson CA, and Randall ME. Stimulation or blockade of the dorsal nucleus of the lateral lemniscus alters binaural and tonic inhibition in contralateral inferior colliculus neurons. Hear Res 69: 98-106, 1993.
23. Faingold CL, Boersma CA, Anderson CA, and Caspary DM. Involvement of GABA in acoustically-evoked inhibition in inferior colliculus neurons. Hear Res 52: 201-216, 1991.
24. Faingold CL, Gehlbach G, and Caspary DM. On the role of GABA as an inhibitory neurotransmitter in inferior colliculus neurons: iontophoretic studies. Brain Res 500: 302-312, 1989.
25. Faure PA, Fremouw T, Casseday JH, and Covey E. Temporal masking reveals properties of sound-evoked inhibition in duration-tuned neurons of the inferior colliculus. J Neurosci 23: 3052-3065, 2003.
26. Fuzessery ZM. Acute sensitivity to interaural time differences in the inferior colliculus of a bat that relies on passive sound localization. Hear Res 109: 46-62, 1997.
27. Fuzessery ZM. Monaural and binaural spectral cues created by the external ears of the pallid bat. Hear Res 95: 1-17, 1996.
28. Fuzessery ZM and Feng AS. Mating call selectivity in the thalamus and midbrain of the leopard frog (Rana pippens): single and multiunit analyses. J Comp Physiol [A] 150: 333-344, 1983.
29. Fuzessery ZM and Hall JC. Role of GABA in shaping frequency tuning and creating FM sweep selectivity in the inferior colliculus. J Neurophysiol 76: 1059-1073, 1996.
30. Fuzessery ZM and Hall JC. Sound duration selectivity in the pallid bat inferior colliculus. Hear Res 137: 137-154, 1999.
31. Glendenning KK, Brunso-Bechtold JK, Thompson GC, and Masterton RB. Ascending auditory afferents to the nuclei of the lateral lemniscus. J Comp Neurol 197: 673-703, 1981.
32. Grothe B. The evolution of temporal processing in the medial superior olive, an auditory brainstem structure. Prog Neurobiol 61: 581-610, 2000.
33. Grothe B, Schweizer H, Pollak GD, Schuller G, and Rosemann C. Anatomy and projection patterns of the superior olivary complex in the Mexican free-tailed bat, Tadarida brasiliensis mexicana. J Comp Neurol 343: 630-646, 1994.
34. Haplea S, Covey E, and Casseday JH. Frequency tuning and response latencies at three levels in the brainstem of the echolocating bat, Eptesicus fuscus. J Comp Physiol 174: 671-683, 1994.
35. Havey DC and Caspary DM. A simple technique for constructing 'piggy-back' multibarrel microelectrodes. Electroencephalogr Clin Neurophysiol 48: 249-251, 1980.
36. Huffman RF and Covey E. Origin of ascending projections to the nuclei of the lateral lemniscus in the big brown bat, Eptesicus fuscus. J Comp Neurol 357: 532-545, 1995.
37. Huffman RF and Henson OW Jr. The descending auditory pathway and acousticomotor systems: connections with the inferior colliculus. Brain Res Brain Res Rev 15: 295-323, 1990.
38. Hurley LM and Pollak GD. Serotonin effects on frequency tuning of inferior colliculus neurons. J Neurophysiol 85: 828-842, 2001.
39. Joris PX, Schreiner CE, and Rees A. Neural processing of amplitude-modulated sounds. Physiol Rev 84: 541-577, 2004.
40. Kanwal JS. Processing species-specific calls combination-sensitive neurons in an echolocating bat. In: The Design of Animal Communication, edited by Hauser MD and Konishi M. Cambridge, MA: The MIT Press, 1999, p. 133-156.
41. Kelly JB, Buckthought AD, and Kidd SA. Monaural and binaural response properties of single neurons in the rat's dorsal nucleus of the lateral lemniscus. Hear Res 122: 25-40, 1998.
42. Klug A, Bauer EE, Hanson JT, Hurley L, Meitzen J, and Pollak GD. Response selectivity for species-specific calls in the inferior colliculus of Mexican free-tailed bats is generated by inhibition. J Neurophysiol 88: 1941-1954, 2002.
43. Klug A, Khan A, Burger RM, Bauer EE, Hurley LM, Yang L, Grothe B, Halvorsen MB, and Park TJ. Latency as a function of intensity in auditory neurons: influences of central processing. Hear Res 148: 107-123, 2000.
44. Klug A, Park TJ, and Pollak GD. Glycine and GABA influence binaural processing in the inferior colliculus of the mustache bat. J Neurophysiol 74: 1701-1713, 1995.
45. Koch U and Grothe B. GABAergic and glycinergic inhibition sharpens tuning for frequency modulations in the inferior colliculus of the big brown bat. J Neurophysiol 80: 71-82, 1998.
46. LeBeau FE, Malmierca MS, and Rees A. Iontophoresis in vivo demonstrates a key role for GABA(A) and glycinergic inhibition in shaping frequency response areas in the inferior colliculus of guinea pig. J Neurosci 21: 7303-7312,2001.
47. Leroy SA and Wenstrup JJ. Spectral integration in the inferior colliculus of the mustached bat. J Neurosci 20: 8533-8541, 2000.
48. Li L and Kelly JB. Inhibitory influence of the dorsal nucleus of the lateral lemniscus on binaural responses in the rat's inferior colliculus. J Neurosci 12: 4530-4539, 1992.
49. Malmierca MS, Hernandez O, Falconi A, Lopez-Poveda EA, Merchan M, and Rees A. The commissure of the inferior colliculus shapes frequency response areas in rat: an in vivo study using reversible blockade with microinjection of kynurenic acid. Exp Brain Res 153: 522-529, 2003.
50. Malmierca MS, Rees A, Le Beau FE, and Bjaalie JG. Laminar organization of frequency-defined local axons within and between the inferior colliculi of the guinea pig. J Comp Neurol 357: 124-144, 1995.
51. Markovitz NS and Pollak GD. Binaural processing in the dorsal nucleus of the lateral lemniscus. Hear Res 73: 121-140, 1994.
52. Markovitz NS and Pollak GD. The dorsal nucleus of the lateral lemniscus in the mustache bat: monaural properties. Hear Res 71: 51-63, 1993.
53. Mittmann DH and Wenstrup JJ. Combination-sensitive neurons in the inferior colliculus. Hear Res 90: 185-191, 1995.
54. Moore DR, Kotak VC, and Sanes DH. Commissural and lemniscal synaptic input to the gerbil inferior colliculus. J Neurophysiol 80: 2229-2236, 1998.
55. Nataraj K and Wenstrup J. Role of glycinergic and GABAergic inhibition in inhibitory combinatorial interactions in the nuclei of the lateral lemniscus. Assoc Res Otolaryngol Abstr 746, 2005.
56. Oliver DL and Shneiderman A. An EM study of the dorsal nucleus of the lateral lemniscus: inhibitory, commissural, synaptic connections between ascending auditory pathways. J Neurosci 9: 967-982, 1989.
57. Palombi PS and Caspary DM. GABA inputs control discharge rate primarily within frequency receptive fields of inferior colliculus neurons. J Neurophysiol 75: 2211-2219, 1996.
58. Park TJ and Pollak GD. GABA shapes a topographic organization of response latency in the mustache bat's inferior colliculus. J Neurosci 13: 5172-5187, 1993.
59. Pollak GD. Time is traded for intensity in the bat's auditory system. Hear Res 36: 107-124, 1988.
60. Pollak GD, Burger RM, and Klug A. Dissecting the circuitry of the auditory system. Trends Neurosci 26: 33-39, 2003a.
61. Pollak GD and Casseday JH. The Neural Basis of Echolocation In Bats. New York: Springer-Verlag, 1986.
62. Pollak GD, Klug A, and Bauer EE. Processing and representation of species-specific communication calls in the auditory system of bats, Int Rev Neurobiol 56: 83-121, 2003b.
63. Pollak GD, Marsh DS, Bodenhamer R, and Souther A. Characteristics of phasic on neurons in inferior colliculus of unanesthetized bats with observations relating to mechanisms for echo ranging. J Neurophysiol 40: 926-942, 1977.
64. Pollak GD and Park TJ. The effects of GABAergic inhibition on monaural response properties of neurons in the mustache bat's inferior colliculus. Hear Res 65: 99-117, 1993.
65. Pollak GD, Winer JA, and O'Neill WE. Perspectives on the functional organization of the mammalian auditory system:why bats are good models. In: Hearing by Bats, Springer Handbook of Auditory Research, edited by Popper AN and Fay RR. New York: Springer-Verlag, 1995, p. 481-498.
66. Pollak GK, Marsh DS, Bodenhamer R, and Souther A. A single-unit analysis of inferior colliculus in unanesthetized bats: response patterns and spike-count functions generated by constant- frequency and frequency-modulated sounds. J Neurophysiol 41: 677-691, 1978.
67. Portfors CV. Combination sensitivity and processing of communication calls in the inferior colliculus of the moustached bat Pteronotus parnellii. An Acad Bras Cienc 76: 253-257, 2004.
68. Portfors CV and Wenstrup JJ. Responses to combinations of tones in the nuclei of the lateral lemniscus. J Assoc Res Otolaryngol 2: 104-117, 2001a.
69. Portfors CV and Wenstrup JJ. Topographical distribution of delay-tuned responses in the mustached bat inferior colliculus. Hear Res 151: 95-105, 2001b.
70. Ramachandran R, Davis KA, and May BJ. Single-unit responses in the inferior colliculus of decerebrate cats. I. Classification based on frequency response maps. J Neurophysiol 82: 152-163, 1999.
71. Rauschecker JP and Tian B. Mechanisms and streams for processing of "what" and "where" in auditory cortex. Proc Natl Acad Sci USA 97: 11800-11806, 2000.
72. Roth GL, Aitkin LM, Andersen RA, and Merzenich MM. Some features of the spatial organization of the central nucleus of the inferior colliculus of the cat. J Comp Neurol 182: 661-680, 1978.
73. Schmidt U, Schlegel P, Schweitzer H, and Neuweiler G. Audition in vampire bats, Desmodus rotundas. J Comp Physiol 168: 45-51, 1991.
74. Schuller G. A cheap earphone for small animals with good frequency response in the ultrasonic frequency range. J Neurosci Methods 71: 187-190, 1997.
75. Schuller G, Radtke-Schuller S, and Betz M. A stereotaxic method for small animals using experimentally determined reference profiles. J Neurosci Methods 18: 339-350, 1986.
76. Shneiderman A, Oliver DL, and Henkel CK. Connections of the dorsal nucleus of the lateral lemniscus: an inhibitory parallel pathway in the ascending auditory system? J Comp Neurol 276: 188-208, 1988.
77. Sivaramakrishnan S, Sterbing-D'Angelo SJ, Filipovic B, D'Angelo WR, Oliver DL, and Kuwada S. GABA(A) synapses shape neuronal responses to sound intensity in the inferior colliculus. J Neurosci 24: 5031-5043,2004.
78. Suta D, Kvasnak E, Popelar J, and Syka J. Representation of species-specific vocalizations in the inferior colliculus of the guinea pig. J Neurophysiol 90: 3794-3808, 2003.
79. Syka J, Popelar J, Kvasnak E, and Astl J. Response properties of neurons in the central nucleus and external and dorsal cortices of the inferior colliculus in guinea pig. Exp Brain Res 133: 254-266, 2000.
80. Theunissen FE and Doupe AJ. Temporal and spectral sensitivity of complex auditory neurons in the nucleus HVc of male zebra finches. J Neurosci 18: 3786-3802, 1998.
81. Vater M, Habbicht H, Kossl M, and Grothe B. The functional role of GABA and glycine in monaural and binaural processing in the inferior colliculus of horseshoe bats. J Comp Physiol [A] 171: 541-553, 1992a.
82. Vater M, Kossl M, and Horn AK. GAD- and GABA-immunoreactivity in the ascending auditory pathway of horseshoe and mustached bats. J Comp Neural 325: 183-206, 1992b.
83. Vater M and Siefer W. The cochlea of Tadarida brasiliensis: specialized functional organization in a generalized bat. Hear Res 91: 178-195, 1995.
84. Wang X. On cortical coding of vocal communication sounds in primates. Proc Natl Acad Sci USA 97: 11843-11849, 2000.
85. Wenstrup JJ, Larue DT, and Winer JA. Projections of physiologically defined subdivisions of the inferior colliculus in the mustached bat: targets in the medial geniculate body and extrathalamic nuclei. J Comp Neurol 346: 207-236, 1994.
86. Winer JA. Functional architecture of the medial geniculate body and primary auditory cortex. In: The Mammalian Auditory Pathway: Neuroanatomy, edited by Webster DB, Popper AN, and Fay RR. New York: Springer-Verlag, 1992, p. 222-409.
87. Winer JA, Larue DT, Diehl JJ, and Hefti BJ. Auditory cortical projections to the cat inferior colliculus. J Comp Neurol 400: 147-174, 1998.
88. Winer JA, Larue DT, and Pollak GD. GABA and glycine in the central auditory system of the mustache bat: structural substrates for inhibitory neuronal organization. J Comp Neurol 355: 317-353, 1995.
89. Winter P and Funkenstein HH. The effect of species-specific vocalization on the discharge of auditory cortical cells in the awake squirrel monkey. Exp Brain Res 18: 489-504, 1973.
90. Yang L, Liu Q, and Pollak GD. Afferent connections to the dorsal nucleus of the lateral lemniscus of the mustache bat: evidence for two functional subdivisions. J Comp Neurol 373: 575-592, 1996.
91. Yang L and Pollak GD. Binaural inhibition in the dorsal nucleus of the lateral lemniscus of the mustache bat affects responses for multiple signals. Aud Neurosci 1: 1-17, 1994a.
92. Yang L and Pollak GD. Differential response properties to amplitude modulated signals in the dorsal nucleus of the lateral lemniscus of the mustache bat and the roles of GABAergic inhibition. J Neurophysiol 77: 324-340, 1997.
93. Yang L and Pollak GD. Features of ipsilaterally evoked inhibition in the dorsal nucleus of the lateral lemniscus. Hear Res 122: 125-141, 1998.
94. Yang L and Pollak GD. GABA and glycine have different effects on monaural response properties in the dorsal nucleus of the lateral lemniscus of the mustache bat. J Neurophysiol 71: 2014-2024, 1994b.
95. Yang L and Pollak GD. The roles of GABAergic and glycinergic inhibition on binaural processing in the dorsal nucleus of the lateral lemniscus of the mustache bat. J Neurophysiol 71: 1999-2013, 1994c.
96. Yang L, Pollak GD, and Resler C. GABAergic circuits sharpen tuning curves and modify response properties in the mustache bat inferior colliculus. J Neurophysiol 68: 1760-1774, 1992.
97. Yin TC, Hirsch JA, and Chan JC. Responses of neurons in the cat's superior colliculus to acoustic stimuli. II. A model of interaural intensity sensitivity. J Neurophysiol 53: 746-758, 1985.
98. Zahn T, Kollmar I, Baudoux S, Pecka M, and Grothe B. Persistent inhibition in high frequency neurons in the gerbil DNLL. Assoc Res Otolaryngol Abstr 1024, 2004.
99. Zhang DX, Li L, Kelly JB, and Wu SH. GABAergic projections from the lateral lemniscus to the inferior colliculus of the rat. Hear Res 117: 1-12, 1998.
100. Zhou X and Jen PH. Brief and short-term corticofugal modulation of subcortical auditory responses in the big brown bat, Eptesicus fuscus. J Neurophysiol 84: 3083-3087, 2000.