Leading inhibition to neural oscillation is important for time-domain processing in the auditory midbrain

Journal of Neurophysiology

Volumn 94, Issue 1, 2005, Pages 314-326

  Galazyuk, Alexander V ^a,b   Lin, Wenyu ^a   Llano, Daniel ^a   Feng, Albert S ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^b NORTHEAST OHIO MEDICAL UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR BLOCKING AGENT; BICUCULLINE;

ANIMAL EXPERIMENT; ARTICLE; AUDITORY NERVOUS SYSTEM; AUDITORY STIMULATION; BAT; FROG; INFORMATION PROCESSING; LATENT PERIOD; MESENCEPHALON; NERVE CELL; NONHUMAN; OSCILLATION; PRIORITY JOURNAL; SOUND DETECTION; TIME;

ACOUSTIC STIMULATION; ACTION POTENTIALS; ANIMALS; ANIMALS, NEWBORN; ANURA; AUDITORY PATHWAYS; BICUCULLINE; CHIROPTERA; DOSE-RESPONSE RELATIONSHIP, RADIATION; ECHOLOCATION; GABA ANTAGONISTS; MESENCEPHALON; NEURAL INHIBITION; NEURONS; PERIODICITY; REACTION TIME; SOUND; SPECIES SPECIFICITY; TIME FACTORS;

EID: 21544464774     PISSN: 00223077     EISSN: None     Source Type: Journal    
DOI: 10.1152/jn.00056.2005     Document Type: Article

References (63)

1. Aitkin LM, Anderson 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 Dunlop CW. Interplay of excitation and inhibition in the cat medial geniculate body. J Neurophysiol 31: 44-61, 1968.
3. Berkowitz A and Suga N. Neural mechanisms of ranging are different in two species of bats. Hear Res 41: 255-264, 1989.
4. Bodenhamer RD and Pollak GD. Time and frequency domain processing in the inferior colliculus of echolocating bats. Hear Res 5: 317-335, 1981.
5. Brugge JF, Dubrovsky NA, Aitkin LM, and Anderson DJ. Sensitivity of single neurons in auditory cortex of cat to binaural tonal stimulation: effects of varying interaural time and intensity. J Neurophysiol 32: 1005-1024, 1969.
6. 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.
7. Chittajallu SK, Palakal MJ, and Wong D. Analysis and classification of delay-sensitive cortical neurons based on response to temporal parameters in echolocation signals. Hear Res 84: 157-166, 1995.
8. Condon CJ, White KR, and Feng AS. Processing of amplitude-modulated signals that mimic echoes from fluttering targets in the inferior colliculus of the little brown bat, Myotis lucifugus. J Neurophysiol 71: 768-784, 1994.
9. 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.
10. Covey E and Casseday JH. Timing in the auditory system of the bat. Annu Rev Physiol 61: 457-476, 1999.
11. Covey E, Kauer JA, and Casseday JH. Whole-cell patch-clamp recording reveals subthreshold sound-evoked postsynaptic currents in the inferior colliculus of awake bats. J Neurosci 16: 3009-3018, 1996.
12. Deatherage BH, Eldredge DH, and Davis H. Latency of action potentials in the cochlea of the guinea pig. J Acoust Soc Am 31: 479-486, 1959.
13. Denzinger A and Schnitzler HU. Echo SPL influences the ranging performance of the big brown bat, Eptesicus fuscus. J Comp Physiol A Sens Neural Behav Physiol 175: 563-571, 1994.
14. Endepols H, Walkowiak W, and Luksch H. Chemoarchitecture of the anuran auditory midbrain. Brain Res Rev 33: 179-198, 2000.
15. 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.
16. 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.
17. Feng AS and Lin WY. Differential innervation patterns of three divisions of frog auditory midbrain (torus semicircularis). J Comp Neurol 306: 613-630, 1991.
18. Feng AS, Simmons JA, and Kick SA. Echo detection and target-ranging neurons in the auditory system of the bat Eptesicus fuscus. Science 202: 645-648, 1978.
19. Fitzpatrick DC, Kanwal JS, Butman JA, and Suga N. Combination-sensitive neurons in the primary auditory cortex of the mustached bat. J Neurosci 13: 931-940, 1993.
20. Galazyuk AV and Feng AS. Oscillation may play a role in time domain central auditory processing. J Neurosci 21: RC147, 2001.
21. Galazyuk AV, Llano D, and Feng AS. Temporal dynamics of acoustic stimuli enhance amplitude tuning of inferior collicular neurons. J Neurophysiol 83: 128-138, 2000.
22. Goldberg JM and Brownell WE. Discharge characteristics of neurons in anteroventral and dorsal cochlear nuclei of cat. Brain Res 64: 35-54, 1973.
23. Griffin DR, Webster FA, and Michael CR. The echolocation of flying insects by bats. Anim Behav 8: 141-154, 1960.
24. 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 A Sens Neural Behav Physiol 174: 671-683, 1994.
25. Havey DC and Caspary DM. A simple technique for constructing "piggy-back" multibarrel microelectrodes. Electroencephalogr Clin Neurophysiol 48: 249-251, 1980.
26. He J. OFF responses in the auditory thalamus of the guinea pig. J Neurophysiol 88: 2377-2386, 2002.
27. Heil P. Auditory conical onset responses revisited. I. First spike timing. J Neurophysiol 77: 2616-2641, 1997a.
28. Heil P. Auditory cortical onset responses revisited. II. Response strength. J Neurophysiol 77: 2642-2660, 1997b.
29. Heil P. Further observations on the threshold model of latency for auditory neurons [comment]. Behav Brain Res 95: 233-236, 1998.
30. Heil P and Irvine DR. On determinants of first-spike latency in auditory cortex. Neuroreport 7: 3073-3076, 1996.
31. Heil P and Irvine DR. First-spike timing of auditory-nerve fibers and comparison with auditory cortex. J Neurophysiol 78: 2438-2454, 1997.
32. Heil P and Irvine DR. The posterior field P of cat auditory cortex: coding of envelope transients. Cereb Cortex 8: 125-141, 1998.
33. Hind JE, Goldberg JM, Greenwood DD, and Rose JE. Some discharge characteristics of single neurons in the inferior colliculus of the cat. II. Timing of the discharges and observations on binaural stimulation. J Neurophysiol 26: 321-341, 1963.
34. Irvine DR and Gago G. Binaural interaction in high-frequency neurons in inferior colliculus of the cat: effects of variations in sound pressure level on sensitivity to interaural intensity differences. J Neurophysiol 63: 570-591, 1990.
35. Kalko E. Insect pursuit, prey capture, and echolocation in pipistrelle bats. Anim Behav 50: 861-880, 1995.
36. Kalko EV and Schnitzler H-U. The echolocation and hunting behavior of Daubenton's bat, Myotis daubentoni. Behav Ecol Sociobiol 24: 225-238, 1989.
37. Kitzes LM, Gibson MM, Rose JE, and Hind JE. Initial discharge latency and threshold considerations for some neurons in cochlear nuclear complex of the cat. J Neurophysiol 41: 1165-1182, 1978.
38. 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.
39. Krahe R, Budinger E, and Ronacher B. Coding of a sexually dimorphic song feature by auditory interneurons of grasshoppers: the role of leading inhibition. J Comp Physiol A Sens Neural Behav Physiol 187: 977-985, 2002.
40. Lin WY and Feng AS. GABA is involved in spatial unmasking in the frog auditory midbrain. J Neurosci 23: 8143-8151, 2003.
41. Miller AR. Latency of unit responses in cochlear nucleus determined in two different ways. J Neurophysiol 38: 812-821, 1975.
42. Mittmann DH and Wenstrup JJ. Combination-sensitive neurons in the inferior colliculus. Hear Res 90: 185-191, 1995.
43. Oertel D. The role of timing in the brain stem auditory nuclei of vertebrates. Annu Rev Physiol 61: 497-519, 1999.
44. 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.
45. 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.
46. O'Neill WE. The bat auditory cortex. In: Hearing by Bats, edited by Popper AN and Fay RR. New York: Springer-Verlag, 1995, p. 416-498.
47. O'Neill WE and Suga N. Target range-sensitive neurons in the auditory cortex of the mustache bat. Science 203: 69-73, 1979.
48. O'Neill WE and Suga N. Encoding of target range and its representation in the auditory cortex of the mustached bat. J Neurosci 2: 17-31, 1982.
49. Park TJ and Pollak G. GABA shapes a topographic organization of response latency in the mustache bat's inferior colliculus. J Neurosci 13: 5172-5187, 1993.
50. Portfors CV and Wenstrup JJ. Topographical distribution of delay-tuned responses in the mustached bat inferior colliculus. Hear Res 151: 95-105, 2001.
51. Rhode WS and Greenberg S. Physiology of the cochlear nuclei. In: The Mammalian Auditory Pathway: Neurophysiology, edited by Popper AN and Fay RR. New York: Springer-Verlag, 1992, p. 94-152.
52. Rose JE, Galambos R, and Hughes JR. Microelectrode studies of the cochlear nuclei of the cat. Bull Johns Hopkins Hosp 104: 211-251, 1959.
53. Rose JE, Greenwood DD, Goldberg JM, and Hind JE. Some discharge characteristics of single neurons in the inferior colliculus of the cat. I. Tonotopical organization, relation of spike-counts to tone intensity, and firing patterns of single elements. J Neurophysiol 26: 294-320, 1963.
54. Sanes DH and Rubel EW. The ontogeny of inhibition and excitation in the gerbil lateral superior olive. J Neurosci 8: 682-700, 1988.
55. Schnitzler HU, Kalko E, Miller L, and Surlykke A. The echolocation and hunting behavior of the bat, Pipistrellus kuhli. J Comp Physiol A Sens Neural Behav Physiol 161: 267-274, 1987.
56. Simmons JA. The resolution of target range by echolocating bats. J Acoust Soc Am 54: 157-173, 1973.
57. Suga N. Echo-ranging neurons in the inferior colliculus of bats. Science 170: 449-452, 1970.
58. 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.
59. Sullivan WE. Neural representation of target distance in auditory cortex of the echolocating bat, Myotis lucifugus. J Neurophysiol 48: 1011-1032, 1982a.
60. Sullivan WE. Possible neural mechanisms of target distance coding in auditory system of the echolocating bat, Myotis lucifugus. J Neurophysiol 48: 1033-1047, 1982b.
61. Tanaka H, Wong D, and Taniguchi I. The influence of stimulus duration on the delay tuning of cortical neurons in the FM bat, Myotis lucifugus. J Comp Physiol A Sens Neural Behav Physiol 171: 29-40, 1992.
62. Volkov IO and Galazjuk AV. Formation of spike response to sound tones in cat auditory cortex neurons: interaction of excitatory and inhibitory effects. Neuroscience 43: 307-321, 1991.
63. Wong D, Maekawa M, and Tanaka H. The effect of pulse repetition rate on the delay sensitivity of neurons in the auditory cortex of the FM bat, Myotis lucifugus. J Comp Physiol A Sens Neural Behav Physiol 170: 393-402, 1992.