Ambient GABA-activated tonic inhibition sharpens auditory coincidence detection via a depolarizing shunting mechanism

Journal of Neuroscience

Volumn 31, Issue 16, 2011, Pages 6121-6131

  Tang, Zheng Quan ^a   Dinh, Emilie Hoang ^a   Shi, Wei ^a,b   Lu, Yong ^a,b  

^a NORTHEAST OHIO MEDICAL UNIVERSITY   (United States)

^b KENT STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID A RECEPTOR;

ANIMAL TISSUE; ARTICLE; AUDITORY SYSTEM FUNCTION; BRAIN NERVE CELL; BRAIN SLICE; CHICKEN; CONTROLLED STUDY; DEPOLARIZATION; EMBRYO; EXCITATORY POSTSYNAPTIC POTENTIAL; NERVOUS SYSTEM CONDUCTANCE; NONHUMAN; PRIORITY JOURNAL; SOUND DETECTION; SYNAPSE VESICLE; THALAMUS INTRALAMINAR NUCLEUS; TONIC INHIBITION;

ANIMALS; AUDITORY PATHWAYS; BLOTTING, WESTERN; CHICK EMBRYO; ELECTRIC STIMULATION; GAMMA-AMINOBUTYRIC ACID; INHIBITORY POSTSYNAPTIC POTENTIALS; MEMBRANE POTENTIALS; NEURAL INHIBITION; NEURONS; PATCH-CLAMP TECHNIQUES; RECEPTORS, GABA-A;

EID: 79955758939     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4733-10.2011     Document Type: Article

References (72)

1. Ade KK, Janssen MJ, Ortinski PI, Vicini S (2008) Differential tonic GABA conductances in striatal medium spiny neurons. J Neurosci 28:1185-1197.
2. Agmon-Snir H, Carr CE, Rinzel J (1998) The role of dendrites in auditory coincidence detection. Nature 393:268-272.
3. Balakrishnan V, Trussell LO (2008) Synaptic inputs to granule cells of the dorsal cochlear nucleus. J Neurophysiol 99:208-219.
4. Belelli D, Harrison NL, Maguire J, Macdonald RL, Walker MC, Cope DW (2009) Extrasynaptic GABAA receptors: form, pharmacology, and function. J Neurosci 29:12757-12763.
5. Brickley SG, Revilla V, Cull-Candy SG, Wisden W, Farrant M (2001) Adaptive regulation of neuronal excitability by a voltage-independent potassium conductance. Nature 409:88-92.
6. Bright DP, Aller MI, Brickley SG (2007) Synaptic release generates a tonic GABAA receptor-mediated conductance that modulates burst precision in thalamic relay neurons. J Neurosci 27:2560-2569.
7. Brown N, Kerby J, Bonnert TP, Whiting PJ, Wafford KA (2002) Pharmacological characterization of a novel cell line expressing human o/.4fi38 GABAA receptors. Br J Pharmacol 136:965-974.
8. Bruckner S, Hyson RL (1998) Effect of GABA on the processing of interau-ral time differences in nucleus laminaris neurons in the chick. Eur J Neurosci 10:3438-3450.
9. Burger RM, Rubel EW (2007) Encoding of interaural timing for binaural hearing. In: The senses: a comprehensive reference, Vol 3, Audition (Dal-los P, Oertel D, eds), pp 613-630. San Diego: Academic.
10. Burger RM, Cramer KS, Pfeiffer JD, Rubel EW (2005) Avian superior olivary nucleus provides divergent inhibitory input to parallel auditory pathways. J Comp Neurol 481:6-18.
11. Campos ML, de Cabo C, Wisden W, Juiz JM, Merlo D (2001) Expression of GABAA receptor subunits in rat brainstem auditory pathways: cochlear nuclei, superior olivary complex and nucleus of the lateral lemniscus. Neuroscience 102:625-638.
12. Caraiscos VB, Elliott EM, You-Ten KE, Cheng VY, Belelli D, Newell JG, Jackson MF, Lambert JJ, Rosahl TW, Wafford KA, MacDonald JF, Orser BA (2004) Tonic inhibition in mouse hippocampal CA1 pyramidal neurons is mediated by a5 subunit-containing y-aminobutyric acid type A receptors. Proc Natl Acad Sci USA 101:3662-3667.
13. Carr CE, Fujita I, Konishi M (1989) Distribution of GABAergic neurons and terminals in auditory system of the barn owl. J Comp Neurol 286:190-207.
14. Cavelier P, Hamann M, Rossi D, Mobbs P, Attwell D (2005) Tonic excitation and inhibition of neurons: ambient transmitter sources and computational consequences. Prog Biophys Mol Biol 87:3-16.
15. Chadderton P, Margrie TW, Hausser M (2004) Integration of quanta in cerebellar granule cells during sensory processing. Nature 428:856-860.
16. Chance FS, Abbott LF, Reyes AD (2002) Gain modulation from background synaptic input. Neuron 35:773-782.
17. Code RA, Burd GD, Rubel EW (1989) Development of GABA immunore-activity in brainstem auditory nuclei of the chick: ontogeny of gradients in terminal staining. J Comp Neurol 284:504-518.
18. Cook DL, Schwindt PC, Grande LA, Spain WJ (2003) Synaptic depression in the localization of sound. Nature 421:66-70.
19. Cope DW, Hughes SW, Crunelli V (2005) GABAA receptor-mediated tonic inhibition in thalamic neurons. J Neurosci 25:11553-11563.
20. Debarbieux F, Brunton J, Charpak S (1998) Effect of bicuculline on tha-lamic activity: a direct blockade of IAHP in reticularis neurons. J Neuro-physiol 79:2911-2918.
21. Dröse S, Altendorf K (1997) Bafilomycins and concanamycins as inhibitors of V-ATPases and P-ATPases. J Exp Biol 200:1-8.
22. Farrant M, Nusser Z (2005) Variations on an inhibitory theme: phasic and tonic activation of GABAA receptors. Nat Rev Neurosci 6:215-229.
23. Funabiki K, Koyano K, Ohmori H (1998) The role of GABAergic inputs for coincidence detection in the neurones of nucleus laminaris of the chick. J Physiol 508:851-869.
24. Glykys J, Mody I (2007a) The main source ofambient GABA responsible for tonic inhibition in the mouse hippocampus. J Physiol 582:1163-1178.
25. Glykys J, Mody I (2007b) Activation of GABAA receptors: views from outside the synaptic cleft. Neuron 56:763-770.
26. Glykys J, Peng Z, Chandra D, Homanics GE, Houser CR, Mody I (2007) A new naturally occurring GABAA receptor subunit partnership with high sensitivity to ethanol. Nat Neurosci 10:40-48.
27. Gray L, Rubel EW (1985) Development of absolute thresholds in chickens. J Acoust Soc Am 77:1162-1172.
28. Grothe B (2003) New roles for synaptic inhibitioninsound localization. Nat Rev Neurosci 4:540-550.
29. Hamann M, Rossi DJ, Attwell D (2002) Tonic and spillover inhibition of granule cells control information flow through cerebellar cortex. Neuron 33:625-633.
30. Häusser M, Clark BA (1997) Tonic synaptic inhibition modulates neuronal output pattern and spatiotemporal synaptic integration. Neuron 19: 665-678.
31. Hefft S, Jonas P (2005) Asynchronous GABA release generates long-lasting inhibition at a hippocampal interneuron-principal neuron synapse. Nat Neurosci 8:1319-1328.
32. Howard MA, Rubel EW (2010) Dynamic spike thresholds during synaptic integration preserve and enhance temporal response properties in the avian cochlear nucleus. J Neurosci 30:12063-12074.
33. Jackson H, Rubel EW (1978) Ontogeny of behavioral responsiveness to sound in the chick embryo as indicated by electrical recordings of motil-ity. J Comp Physiol Psychol 92:682-696.
34. Kandler K, Clause A, Noh J (2009) Tonotopic reorganization of developing auditory brainstem circuits. Nat Neurosci 12:711-717.
35. Kaneda M, Farrant M, Cull-Candy SG (1995) Whole-cell and single-channel currents activated by GABA and glycine in granule cells of the rat cerebellum. J Physiol 485:419-435.
36. Kirmse K, Kirischuk S (2006) Ambient GABA constrains the strength of GABAergic synapsesat Cajal-Retzius cells inthe developing visual cortex. J Neurosci 26:4216-4227.
37. Kirmse K, Dvorzhak A, Kirischuk S, Grantyn R (2008) GABA transporter 1 tunes GABAergic synaptic transmission at output neurons of the mouse neostriatum. J Physiol 586:5665-5678.
38. Kozlov AS, Angulo MC, Audinat E, Charpak S (2006) Target cell-specific modulation of neuronal activity by astrocytes. Proc Natl Acad Sci U S A 103:10058-10063.
39. Kuba H, Koyano K, Ohmori H (2002) Synaptic depression improves coincidence detection in the nucleus laminaris in brainstem slices of the chick embryo. Eur J Neurosci 15:984-990.
40. Kuba H, Yamada R, Ohmori H (2003) Evaluation of the limiting acuity of coincidence detection in nucleus laminaris of the chicken. J Physiol 552:611-620.
41. Kuba H, Ishii TM, Ohmori H (2006) Axonal siteofspike initiation enhances auditory coincidence detection. Nature 444:1069-1072.
42. Lachica EA, Rübsamen R, Rubel EW (1994) GABAergic terminals in nucleus magnocellularis and laminaris originate from the superior olivary nucleus. J Comp Neurol 348:403-418.
43. Lee S, Yoon BE, Berglund K, Oh SJ, Park H, Shin HS, Augustine GJ, Lee CJ (2010) Channel-mediated tonic GABA release from glia. Science 330:790-796.
44. Lu T, Trussell LO (2000) Inhibitory transmission mediated by asynchronous transmitter release. Neuron 26:683-694.
45. Lu Y (2009) Regulation of glutamatergic and GABAergic neurotransmis-sion in the chick nucleus laminaris: role of N-type calcium channels. Neuroscience 164:1009-1019.
46. Maguire J, Mody I (2008) GABAAR plasticity during pregnancy: relevance to postpartum depression. Neuron 59:207-213.
47. Maguire JL, Stell BM, Rafizadeh M, Mody I (2005) Ovarian cycle-linked changes in GABAA receptors mediating tonic inhibition alter seizure susceptibility and anxiety. Nat Neurosci 8:797-804.
48. Mann EO, Mody I (2010) Control of hippocampal gamma oscillation frequency by tonic inhibition and excitation of interneurons. Nat Neurosci 13:205-212.
49. Mathews PJ, Jercog PE, Rinzel J, Scott LL, Golding NL (2010) Control of submillisecond synaptic timing in binaural coincidence detectors by Kv1 channels. Nat Neurosci 13:601-609.
50. Mitchell SJ, Silver RA (2003) Shunting inhibition modulates neuronal gain during synaptic excitation. Neuron 38:433-445.
51. Monsivais P, Rubel EW (2001) Accommodation enhances depolarizing inhibition in central neurons. J Neurosci 21:7823-7830.
52. Nusser Z, Mody I (2002) Selective modulation of tonic and phasic inhibitions in dentate gyrus granule cells. J Neurophysiol 87:2624-2628.
53. Nusser Z, Sieghart W, Somogyi P (1998) Segregation of different GABAA receptors to synaptic and extrasynaptic membranes of cerebellar granule cells. J Neurosci 18:1693-1703.
54. Parks TN, Rubel EW (1975) Organization and development of brain stem auditory neclei of the chicken: organization of projections from n. mag-nocellularis to n. laminaris. J Comp Neurol 164:435-448.
55. Peng Z, Hauer B, Mihalek RM, Homanics GE, Sieghart W, Olsen RW, Houser CR (2002) GABAA receptor changes in 8 subunit-deficient mice: altered expression of a4 and y2 subunits in the forebrain. J Comp Neurol 446:179-197.
56. Reyes AD, Rubel EW, Spain WJ (1994) Membrane properties underlying the firing of neurons in the avian cochlear nucleus. J Neurosci 14:5352-5364.
57. Reyes AD, Rubel EW, Spain WJ (1996) In vitro analysis of optimal stimuli for phase-locking and time-delayed modulation of firing in avian nucleus laminaris neurons. J Neurosci 16:993-1007.
58. Richerson GB, Wu Y (2003) Dynamic equilibrium of neurotransmitter transporters: not just for reuptake anymore. J Neurophysiol 90:1363-1374.
59. Rossi DJ, Hamann M, Attwell D (2003) Multiple modes of GABAergic inhibition of rat cerebellar granule cells. J Physiol 548:97-110.
60. Rubel EW, Parks TN (1975) Organization and development of brain stem auditory nuclei of the chicken: tonotopic organization of n. magnocellu-laris and n. laminaris. J Comp Neurol 164:411-433.
61. Ruiz A, Campanac E, Scott RS, RusakovDA, KullmannDM (2010) Presynaptic GABAA receptors enhance transmission and LTP induction at hippocampal mossy fiber synapses. Nat Neurosci 13:431-438.
62. Salin PA, Prince DA (1996) Spontaneous GABAA receptor-mediated inhibitory currents in adult rat somatosensory cortex. J Neurophysiol 75:1573-1588.
63. Saxena NC, MacDonald RL (1996) Properties of putative cerebellar y-aminobutyric acid A receptor isoforms. Mol Pharmacol 49:567-579.
64. Seidl AH, Rubel EW, Harris DM (2010) Mechanisms for adjusting interaural time differences to achieve binaural coincidence detection. J Neurosci 30:70-80.
65. Semyanov A, Walker MC, Kullmann DM (2003) GABA uptake regulates cortical excitability via cell type-specific tonic inhibition. Nat Neurosci 6:484-490.
66. Shen H, Sabaliauskas N, Sherpa A, Fenton AA, Stelzer A, Aoki C, Smith SS (2010) A critical role for a4/36 GABAA receptors in shaping learning deficits at puberty in mice. Science 327:1515-1518.
67. Stell BM, Brickley SG, Tang CY, Farrant M, Mody I (2003) Neuroactive steroids reduce neuronal excitability by selectively enhancing tonic inhibition mediated by 8 subunit-containing GABAA receptors. Proc Natl Acad Sci USA 100:14439-14444.
68. Tang ZQ, Gao H, Lu Y (2009) Control of a depolarizing GABAergic input in an auditory coincidence detection circuit. J Neurophysiol 102:1672-1683.
69. von Bartheld CS, Code RA, Rubel EW (1989) GABAergic neurons in brainstem auditory nuclei of the chick: distribution, morphology, and connectivity. J Comp Neurol 287:470-483.
70. Wei W, Zhang N, Peng Z, Houser CR, Mody I (2003) Perisynaptic localization of 8 subunit-containing GABAA receptors and their activation by GABA spillover in the mouse dentate gyrus. J Neurosci 23:10650-10661.
71. Yang L, Monsivais P, Rubel EW (1999) The superior olivary nucleus and its influence on nucleus laminaris: a source of inhibitory feedback for coincidence detection in the avian auditory brainstem. J Neurosci 19: 2313-2325.
72. Zhou Q, Petersen CC, Nicoll RA (2000) Effects of reduced vesicular filling on synaptic transmission in rat hippocampal neurons. J Physiol 525:195-206.