Roles of inhibition in creating complex auditory responses in the inferior colliculus: Facilitated combination-sensitive neurons

Journal of Neurophysiology

Volumn 93, Issue 6, 2005, Pages 3294-3312

  Nataraj, Kiran ^a,b   Wenstrup, Jeffrey J ^a  

^a NORTHEAST OHIO MEDICAL UNIVERSITY   (United States)

^b The University of Akron   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID; BICUCULLINE; GLYCINE; NEUROTRANSMITTER; STRYCHNINE;

ARTICLE; AUDITORY CORTEX; AUDITORY RESPONSE; BRAIN STEM; FACILITATION; INFERIOR COLLICULUS; IONTOPHORESIS; MESENCEPHALON; NERVE CELL INHIBITION; NERVE EXCITABILITY; NERVE POTENTIAL; NONHUMAN; PRIORITY JOURNAL;

ACOUSTIC STIMULATION; ACTION POTENTIALS; ANIMALS; AUDITORY PATHWAYS; BICUCULLINE; CELL COUNT; DRUG INTERACTIONS; GABA ANTAGONISTS; GLYCINE AGENTS; INFERIOR COLLICULUS; IONTOPHORESIS; MODELS, NEUROLOGICAL; NEURAL INHIBITION; NEURONS; OTTERS; REACTION TIME; REGRESSION ANALYSIS; STRYCHNINE; TIME FACTORS; WAKEFULNESS;

EID: 19344372243     PISSN: 00223077     EISSN: None     Source Type: Journal    
DOI: 10.1152/jn.01152.2004     Document Type: Article

References (60)

1. Adams JC and Mugnaini E. Dorsal nucleus of the lateral lemniscus: a nucleus of GABAergic projection neurons. Brain Res Bull 13: 585-590, 1984.
2. Adams JC and Mugnaini E. Immunocytochemical evidence for inhibitory and disinhibitory circuits in the superior olive. Hear Res 49: 281-298, 1990.
3. Andrasfalvy BK and Magee JC. Distance-dependent increase in AMPA receptor number in the dendrites of adult hippocampal CA1 pyramidal neurons. J Neurosci 21: 9151-9159, 2001.
4. Backoff PM, Palombi PS, and Caspary DM. Gamma-aminobutyric acidergic and glycinergic inputs shape coding of amplitude modulation in the chinchilla cochlear nucleus. Hear Res 134: 77-88, 1999.
5. Barrio LC, Araque A, and Buno W. Participation of voltage-gated conductances on the response succeeding inhibitory synaptic potentials in the crayfish slowly adapting stretch receptor neuron. J Neurophysiol 72: 1140-1151, 1994.
6. Bartlett EL, Stark JM, Guillery RW, and Smith PH. Comparison of the fine structure of cortical and collicular terminals in the rat medial geniculate body. Neurosci 100: 811-828, 2000.
7. Bertrand S and Cazalets JR. Postinhibitory rebound during locomotor-like activity in neonatal rat motoneurons in vitro. J Neurophysiol 79: 342-351, 1998.
8. Brand A, Behrend O, Marquardt T, McAlpine D, and Grothe B. Precise inhibition is essential for microsecond interaural time difference coding. Nature 417: 543-547, 2002.
9. 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.
10. Caspary DM, Havey DC, and Faingold CL. Effects of microiontophoretically applied glycine and GABA on neuronal response patterns in the cochlear nuclei. Brain Res 172: 179-185, 1979.
11. Casseday JH, Ehrlich D, and Covey E. Neural tuning for sound duration: role of inhibitory mechanisms in the inferior colliculus. Science 264: 847-850, 1994.
12. Casseday JH, Ehrlich D, and Covey E. Neural measurement of sound duration: control by excitatory-inhibitory interactions in the inferior colliculus. J Neurophysiol 84: 1475-1487, 2000.
13. Chandler SH, Hsaio CF, Inoue T, and Goldberg LJ. Electrophysiological properties of guinea pig trigeminal motoneurons recorded in vitro. J Neurophysiol 71: 129-145, 1994.
14. Chen QC and Jen PH. Bicuculline application affects discharge patterns, rate-intensity functions, and frequency tuning characteristics of bat auditory cortical neurons. Hear Res 150: 161-174, 2000.
15. Edamatsu H and Suga N. Differences in response properties of neurons between two delay-tuned areas in the auditory cortex of the mustached bat. J Neurophysiol 69: 1700-1712, 1993.
16. 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.
17. Faingold CL, Boersma Anderson CA, and Caspary DM. Involvement of GABA in acoustically-evoked inhibition in inferior colliculus neurons. Hear Res 52: 201-216, 1991.
18. Fitzpatrick DC, Suga N, and Olsen JF. Distribution of response types across entire hemispheres of the mustached bat's auditory cortex. J Comp Neurol 391: 353-365, 1998.
19. Foote SL, Freedman R, and Oliver AP. Effects of putative neurotransmitters on neuronal activity in monkey auditory cortex. Brain Res 86: 229-242, 1975.
20. Fujita I and Konishi M. The role of GABAergic inhibition in processing of interaural time difference in the owl's auditory system. J Neurosci 11: 722-739, 1991.
21. Fuzessery ZM and Feng AS. Mating call selectivity in the thalamus and midbrain of the leopard frog (Rana p. pipens): single- and multiunit analyses. J Comp Physiol [A] 150: 333-344, 1983.
22. 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.
23. Fuzessery ZM, Wenstrup JJ, Hall JC, and Leroy S. Inhibition has little effect on response latencies in the inferior colliculus. J Assoc Res Otolaryngol 4: 60-73, 2003.
24. Havey DC and Caspary DM. A simple technique for constructing "piggy-back" multibarrel microelectrodes. Electroencephalogr Clin Neurophysiol 48: 249-251, 1980.
25. Hodgkin AL and Huxley AF. A quantitative description of membrane current and its application to conduction and excitation in nerve. J Physiol 117: 500-544, 1952.
26. Kemmer M and Vater M. The distribution of GABA and glycine immunostaining in the cochlear nucleus of the mustached bat (Pteronotus parnellii). Cell Tissue Res 287: 487-506, 1997.
27. h) in the inferior colliculus: distribution and contribution to temporal processing. J Neurophysiol 90: 3679-3687, 2003.
28. 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.
29. LeBeau FE, Rees A, and Malmierca MS. Contribution of GABA- and glycine-mediated inhibition to the monaural temporal response properties of neurons in the inferior colliculus. J Neurophysiol 75: 902-919, 1996.
30. Liu Y, Sakurai H, Kurokawa K, Yamada H, and Kudo M. Glycine- immunoreactive synapses in the central nucleus of the inferior colliculus. An electron microscopic study in the cat. Neurosci Lett 269: 183-185, 1999.
31. Margoliash D and Fortune ES. Temporal and harmonic combination-sensitive neurons in the zebra finch's HVc. J Neurosci 12: 4309-4326, 1992.
32. Marsh RA and Wenstrup JJ. Responses to combination of tones in the cochlear nucelus of awake mustached bats. Abstr Assoc Res Otolaryngol 37: 2002.
33. Mittmann DH and Wenstrup JJ. Combination-sensitive neurons in the inferior colliculus. Hear Res 90: 185-191, 1995.
34. Nataraj K. Neural Mechanisms in Analyzing Complex Sounds (PhD dissertation). Akron, OH: The University of Akron, 2003.
35. O'Neill WE and Suga N. Target range-sensitive neurons in the auditory cortex of the mustache bat. Science 203: 69-73, 1979.
36. Ohlemiller KK, Kanwal JS, and Suga N. Facilitative responses to species-specific calls in cortical FM-FM neurons of the mustached bat. Neuroreport 7: 1749-1755, 1996.
37. Olsen JF and Suga N. Combination-sensitive neurons in the medial geniculate body of the mustached bat: encoding of relative velocity information. J Neurophysiol 65: 1254-1274, 1991a.
38. Olsen JF and Suga N. Combination-sensitive neurons in the medial geniculate body of the mustached bat: encoding of target range information. J Neurophysiol 65: 1275-1296, 1991b.
39. Owen DG, Segal M, and Barker JL. A Ca-dependent Cl- conductance in cultured mouse spinal neurones. Nature 311: 567-570, 1984.
40. Park TJ and Pollak GD. GABA shapes sensitivity to interaural intensity disparities in the mustache bat's inferior colliculus: implications for encoding sound location. J Neurosci 13: 2050-2067, 1993.
41. 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.
42. Portfors CV, Gans DP and Wenstrup JJ. Responses to communication calls in the inferior colliculus of the mustached bat. Abstr Assoc Res Otolaryngol 143: 2002.
43. Portfors CV and Wenstrup JJ. Delay-tuned neurons in the inferior colliculus of the mustached bat: implications for analyses of target distance. J Neurophysiol 82: 1326-1338, 1999.
44. Portfors CV and Wenstrup JJ. Responses to combinations of tones in the nuclei of the lateral lemniscus. J Assoc Res Otolaryngol 2: 104-117, 2001.
45. Rauschecker JP, Tian B, and Hauser M. Processing of complex sounds in the macaque nonprimary auditory cortex. Science 268: 111-114, 1995.
46. Saint Marie RL, Ostapoff EM, Morest DK, and Wenthold RJ. Glycine-immunoreactive projection of the cat lateral superior olive: possible role in midbrain ear dominance. J Comp Neurol 279: 382-396, 1989.
47. Suga N, O'Neill WE, Kujirai K, and Manabe T. Specificity of combination-sensitive neurons for processing of complex biosonar signals in auditory cortex of the mustached bat. J Neurophysiol 49: 1573-1626, 1983.
48. Suga N, O'Neill WE, and Manabe T. Cortical neurons sensitive to combinations of information-bearing elements of biosonar signals in the mustache bat. Science 200: 778-781, 1978.
49. Suga N, O'Neill WE, and Manabe T. Harmonic-sensitive neurons in the auditory cortex of the mustache bat. Science 203: 270-274, 1979.
50. Suga N, Olsen JF and Butman JA. Specialized subsystems for processing biologically important complex sounds: cross-correlation analysis for ranging in the bat's brain. Cold Spring Harbor Symp Quant Biol 55: 585-597, 1990.
51. Tell F and Bradley RM. Whole-cell analysis of ionic currents underlying the firing pattern of neurons in the gustatory zone of the nucleus tractus solitarii. J Neurophysiol 71: 479-492, 1994.
52. Turecek R and Trussell LO. Presynaptic glycine receptors enhance transmitter release at a mammalian central synapse. Nature 411: 587-590, 2001.
53. 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, 1992.
54. Wang J, Caspary D, and Salvi RJ. GABA-A antagonist causes dramatic expansion of tuning in primary auditory cortex. Neuroreport 11: 1137-1140, 2000.
55. Wenstrup JJ and Leroy SA. Spectral integration in the inferior colliculus: role of glycinergic inhibition in response facilitation. J Neurosci 21: RC124, 2001.
56. Wenstrup JJ, Mittmann DH, and Grose CD. Inputs to combination-sensitive neurons of the inferior colliculus. J Comp Neurol 409: 509-528, 1999.
57. 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.
58. Winer JA, Saint Marie RL, Larue DT, and Oliver DL. Gabaergic feedforward projections from the inferior colliculus to the medial geniculate body. Proc Natl Acad Sci USA 93: 8005-8010, 1996.
59. Yang L, Pollak GD, and Resler C. GAB Aergic circuits sharpen tuning curves and modify response properties in the mustache bat inferior colliculus. J Neurophysiol 68: 1760-1774, 1992.
60. A-mediated inhibition. Science 284: 962-965, 1999.