GABA-Mediated Modulation of the Discharge Pattern and Rate-Level Function of Two Simultaneously Recorded Neurons in the Inferior Colliculus of the Big Brown Bat, Eptesicus Fuscus

Fei-Jian Wu；Philip H.-S. Jen

bat ； bicuculline ； discharge pattern ； facilitation ； inferior colliculus ； masker ； probe ； rate-level function ； suppression

The Chinese Journal of Physiology

51卷1期（2008 / 02 / 01）

13 - 26

英文

Neurons in the central nucleus of the inferior colliculus (IC) receive excitatory and inhibitory inputs from both lower and higher auditory nuclei. Interaction of these two opposing inputs shapes response properties of IC neurons. In this study, we examine the interaction of excitation and inhibition on the responses of two simultaneously recorded IC neurons using a probe and a masker under forward masking paradigm. We specifically study whether a sound that serves as a probe to elicit responses of one neuron might serve as a masker to suppress or facilitate the responses of the other neuron. For each pair of IC neurons, we deliver the probe at the best frequency (BF) of one neuron and the masker at the BF of the other neuron and vice versa. Among 33 pairs of IC neurons recorded, this forward masking produces response suppression in 29 pairs of IC neurons and response facilitation in 4 pairs of IC neurons. The degree of suppression decreases with recording depth, sound level and BF difference between each pair of IC neurons. During bicuculline application, the degree of response suppression decreases in the bicuculline-applied neuron but increases in the paired neuron. Our data indicate that the forward masking of responses of IC neurons observed in this study is mostly mediated through GABA ergic inhibition which also shapes the discharge pattern of these neurons. These data suggest that interaction among individual IC neurons improves auditory sensitivity during auditory signal processing.

1. Adams, J.C.(1979).Ascending projections to the inferior colliculus.J. Comp. Neurol.,183,519-538.
2. Aitkin, L.(1986).The Auditory Midbrain: Structure and Function in the Central Auditory Pathway.Clifton, NJ:Humana Press.
3. Bormann, J.(1988).Electrophysiology of GABAA and GABAB receptor subtypes.Trend Neurosci.,11,112-116.
4. Brosch, M.,Schreiner, C.E.(1997).Time course of forward masking tuning curves in cat primary auditory cortex.J. Neurophysiol.,77,923-943.
5. Calford, M.B.,Semple, M.N.(1995).Monaural inhibition in cat auditory cortex.J. Neurophysiol.,73,1876-1891.
6. Casseday, J.H.,Ehrlich, D.,Covey, E.(1994).Neural tuning for sound duration: role of inhibitory mechanisms in the inferior colliculus.Science,264,847-850.
7. Casseday, J.H.,Ehrlich, D.,Covey, E.(2000).Neural measurement of sound duration: control by excitatory-inhibitory interaction in the inferior colliculus.J. Neurophysiol.,84,1475-1487.
8. Cooper, J.R.,Bloom, F.E.,Roth, R.H.(1982).The biomedical basis of neuropharmacology.New York:Oxford University Press.
9. Covey, E.,Casseday, J.H.(1991).The monaural nuclei of the lateral lemniscus in an echolocating bat: parallel pathways for analyzing temporal features of sound.J. Neurosci.,11,3456-3470.
10. Ebert, U.,Ostwald, J.(1995).GABA alters the discharge pattern of chopper neurons in the ventral cochlear nucleus.Hear. Res.,91,160-166.
11. Ehret, G.,Merzenich, M.M.(1988).Complex sound analysis (frequency resolution, filtering and spectral integration) by single units of the inferior colliculus of the cat.Brain Res. Rev.,13,139-163.
12. Fubara, B.M.,Casseday, J.H.,Covey, E.,Schwartz-Bloom, R.D.(1996).Distribution of GABAA, GABAB and glycine receptors in the central auditory system of the big brown bat, Eptesicus fuscus.J. Comp. Neurol.,369,83-92.
13. Fuzessery, Z.M.,Feng, A.S.(1983).Frequency selectivity in the anuran medulla: excitatory and inhibitory tuning properties of single neurons in the dorsal medullary and superior olivary nuclei.J. Comp. Physiol. A,50,107-119.
14. Fuzessery, Z.M.,Hall, J.C.(1996).Role of GABA in shaping frequency tuning and creating FM sweep selectivity in the inferior colliculus.J. Neurophysiol.,76,1059-1073.
15. Herbert, H.,Aschoff, A.,Ostwald, J.(1991).Topography of projections from the auditory cortex to the inferior colliculus in the rat.J. Comp. Neurol.,304,103-122.
16. Huffman, R.F.,Henson, O.W.(1990).The descending auditory pathways and acoustico-motor systems: connections with the inferior colliculus.Brain Res. Rev.,15,295-323.
17. Jen, P.H.S.,Chen, Q.C.,Sun, X.D.(1998).Corticofugal regulation of auditory sensitivity in bat inferior colliculus.J. Comp. Physiol. A,183,683-697.
18. Jen, P.H.S.,Feng, R.B.(1999).Bicuculline application affects pulse duration tuning characteristics of bat inferior collicular neurons.J. Comp. Physiol. A,184,185-194.
19. Jen, P.H.S.,Schlegel, P. A.(1982).Auditory physiological properties of the neurons in the inferior colliculus of the big brown bat, Eptesicus fuscus.J. Comp. Physiol. A,147,351-363.
20. Jen, P.H.S.,Sun, X.D.,Chen, D.M.,Teng, H.B.(1987).Auditory space representation in the inferior colliculus of the FM bat, Eptesicus fuscus.Brain Res.,419,7-18.
21. Jen, P.H.S.,Wu, C.H.(2006).Duration organization selectivity in the inferior colliculus of the big brown bat, Eptesicus fuscus.Brain Res.,1108,76-87.
22. Jen, P.H.S.,Wu, C.H.(2005).The role of GABAergic inhibition in shaping the response size and duration selectivity of bat inferior collicular neurons to sound pulses in rapid sequences.Hear. Res.,202,222-234.
23. Jen, P.H.S.,Wu, C.H.,Luan, R.H.,Zhou, X.M.(2002).GABAergic inhibition contributes to pulse repetition rate-dependent frequency selectivity in inferior colliculus of the big brown bat, Eptesicus fuscus.Brain Res.,948,159-164.
24. Jen, P.H.S.,Wu, F.J.,Chen, Q.C.(2002).The effect of two-tone stimulation on responses of two simultaneously recorded neurons in the inferior colliculus of the big brown bat, Eptesicus fuscus.Hear. Res.,174,281-289.
25. Jen, P.H.S.,Zhang, J.P.(2000).The role of GABAergic inhibition on direction-dependent sharpening of frequency tuning in bat inferior collicular neurons.Brain Res.,862,127-137.
26. Jen, P.H.S.,Zhang, J.P.(1999).Corticofugal regulation of excitatory and inhibitory frequency tuning curves of bat inferior collicular neurons.Brain Res.,841,184-188.
27. Jen, P.H.S.,Zhou, X.M.(1999).Temporally patterned pulse trains affect duration tuning characteristics of bat inferior collicular neurons.J. Comp. Physiol. A,185,471-478.
28. Klug, A.,Park, T.J.,Pollak, G.D.(1995).Glycine and GABA influence binaural processing in the inferior colliculus of the mustache bat.J. Neurophysiol.,74,1701-1713.
29. 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.
30. LeBeau, F.E.,Malmierca, M.S.,Rees, A.(2001).Iontophoresis in vivo demonstrates a key role for GABAA and glycinergic inhibition in shaping frequency response areas in the inferior colliculus of guinea pig.J. Neurosci.,21,7303-7312.
31. LeBeau, F.E.,Rees, A.,Malmierca, M.S.(1996).Contribution of GABA- and glycine-mediated inhibition to the monaural temporal response properties of neurons in the inferior colliculus.J. Neurophysiol.,75,902-919.
32. Lu, Y.,Jen, P.H.S.(2001).GABAergic and glycinergic neural inhibition in excitatory frequency tuning of bat inferior collicular neurons.Exp. Brain Res.,14,331-339.
33. Lu, Y.,Jen, P.H.S.(2003).Binaural interaction in the inferior colliculus of the big brown bat, Eptesicus fuscus.Hear. Res.,77,100-110.
34. Lu, Y.,Jen, P.H.S.(2002).Interaction of excitation and inhibition in inferior collicular neurons of the big brown bat, Eptesicus fuscus.Hear. Res.,169,140-150.
35. Lu, Y.,Jen, P.H.S.,Wu, M.(1998).GABAergic disinhibition affects the responses of bat inferior collicular neurons to temporally patterned sound pulses.J. Neurophysiol.,79,2303-2315.
36. Lu, Y.,Jen, P.H.S.,Zheng, Q.Y.(1997).GABAergic disinhibition changes the recovery cycle of bat inferior colliculus neurons.J. Comp. Physiol. A,181,331-341.
37. Moriyama, T.,Hou, T.Z.,Wu, M.,Jen, P.H.S.(1994).Responses of inferior collicular neurons of the FM bat, Eptesicus fuscus, to pulse trains with varied pulse amplitudes.Hear. Res.,79,105-114.
38. Nelson, P.G.,Erulkar, S.D.(1963).Synaptic mechanisms of excitation and inhibition in the central auditory pathway.J. Neurophysiol.,26,908-923.
39. Oliver, D.L.,Winer, J.A.,Beckius, G.E.,Saint Marie, R.L.(1994).Morphology of GABAergic neurons in the inferior colliculus of the cat.J. Comp. Neurol.,340,27-42.
40. Phillips, D.P.,Hall, S.E.,Hollett, J.L.(1989).Repetition rate and signal level effects on neuronal responses to brief tone pulses in cat auditory cortex.J. Acoust. Soc. Am.,85,2537-2549.
41. Pinheiro, A.D.,Wu, M.,Jen, P.H.S.(1991).Encoding repetition rate and duration in the inferior colliculus of the big brown bat, Eptesicus fuscus.J. Comp. Physiol. A,169,89-85.
42. Pollak, G.D.,Park, T.J.(1993).The effects of GABAergic inhibition on monaural response properties of neurons in the mustache bat`s inferior colliculus.Hear. Res.,65,99-117.
43. Roberts, R.C.,Ribak, C.E.(1987).An electron microscopic study of GABAergic neurons and terminals in the central nucleus of the inferior colliculus of the cat.J. Neurocytol.,16,333-345.
44. Saldana, E.,Feliciano, M.,Mugnaini, E.(1996).Distribution of descending projections from primary auditory neocortex to inferior colliculus mimics the topography of intracollicular projections.J. Comp. Neurol.,371,15-40.
45. Shneiderman, A.,Oliver, D.L.(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.
46. Suga, N.(1995).Sharpening of frequency tuning by inhibition in the central auditory system: tribute to Yasuji Katsuki.Neurosci. Res.,2,287-299.
47. Vater, M.,Habbicht, H.,Kossl, M.,Grothe, B.(1992).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.
48. Winer, J.A.(2006).Decoding the auditory corticofugal systems.Hear. Res.,211,1-8.
49. Wu, C.H.,Jen, P.H.S.(2006).The role of GABAergic inhibition in shaping duration selectivity of bat inferior collicular neurons determined with temporally patterned sound trains.Hear. Res.,215,55-65.
50. Wu, C.H.,Jen, P.H.S.(2006).GABA-mediated echo duration selectivity of inferior collicular neurons of Eptesicus fuscus, determined with single pulses and pulse-echo pairs.J. Comp. Physiol. A,192,985-1002.
51. Wu, M.,Jen, P.H.S.(1991).Encoding of acoustic stimulus intensity by inferior collicular neurons of the big brown bat, Eptesicus fuscus.Chinese J. Physiol.,34,145-155.
52. Yang, L.,Pollak, G.D.,Resler, C.(1992).GABAergic circuits sharpen tuning curves and modify response properties in the mustache bat inferior colliculus.J. Neurophysiol.,68,1760-1774.
53. Zhou, X.M.,Jen, P.H.S.(2000).Corticofugal inhibition compresses all types of rate intensity functions of inferior collicular neurons in the big brown bat.Brain Res.,881,62-68.
54. Zhou, X.M.,Jen, P.H.S.(2000).Neural inhibition sharpens auditory spatial selectivity of bat inferior collicular neurons.J. Comp. Physiol. A,186,389-398.
55. Zhou, X.M.,Jen, P.H.S.(2002).The role of GABAergic inhibition in shaping directional selectivity of bat inferior collicular neurons determined with temporally patterned sound trains.J. Comp. Physiol. A,188,815-826.

1. Wu, Fei-Jian,Jen, Philip H.-S.(2009).Involvement of GABA-Mediated Inhibition in Shaping the Frequency Selectivity of Neurons in the Inferior Colliculus of the Big Brown Bat, Eptesicus fuscus.Chinese Journal of Physiology,52(1),38-46.