The Korean Journal of Physiology and Pharmacology

The Korean Society of Pharmacology (대한약리학회)
권호 표지
DOI QR코드

DOI QR Code

Nitric Oxide Modulation of GABAergic Synaptic Transmission in Mechanically Isolated Rat Auditory Cortical Neurons

  • Lee, Jong-Ju (Department of Pharmacology, School of Dentistry, Kyungpook National University)
  • Published : 2009.12.31
Download PDF
⟨ Previous Next ⟩

Abstract

The auditory cortex (A1) encodes the acquired significance of sound for the perception and interpretation of sound. Nitric oxide (NO) is a gas molecule with free radical properties that functions as a transmitter molecule and can alter neural activity without direct synaptic connections. We used whole-cell recordings under voltage clamp to investigate the effect of NO on spontaneous GABAergic synaptic transmission in mechanically isolated rat auditory cortical neurons preserving functional presynaptic nerve terminals. GABAergic spontaneous inhibitory postsynaptic currents (sIPSCs) in the A1 were completely blocked by bicuculline. The NO donor, S-nitroso-N-acetylpenicillamine (SNAP), reduced the GABAergic sIPSC frequency without affecting the mean current amplitude. The SNAP-induced inhibition of sIPSC frequency was mimicked by 8-bromoguanosine cyclic 3',5'-monophosphate, a membrane permeable cyclic-GMP analogue, and blocked by 2-(4-carboxyphenyl)-4,4,5,5-tetramethylimidazoline-1-oxyl-3-oxide, a specific NO scavenger. Blockade of presynaptic $K^+$ channels by 4-aminopyridine, a $K^+$ channel blocker, increased the frequencies of GABAergic sIPSCs, but did not affect the inhibitory effects of SNAP. However, blocking of presynaptic $Ca^{2+}$ channels by $Cd^{2+}$, a general voltage-dependent $Ca^{2+}$ channel blocker, decreased the frequencies of GABAergic sIPSCs, and blocked SNAP-induced reduction of sIPSC frequency. These findings suggest that NO inhibits spontaneous GABA release by activation of cGMP-dependent signaling and inhibition of presynaptic $Ca^{2+}$ channels in the presynaptic nerve terminals of A1 neurons.

Keywords

References

  1. Ahern GP, Klyachko VA, Jackson MB. cGMP and S-nitrosylation: two routes for modulation of neuronal excitability by NO. Trends Neurosci 25: 510-517, 2002 https://doi.org/10.1016/S0166-2236(02)02254-3
  2. Akaike N, Harata N. Nystatin perforated patch recording and its applications to analyses of intracellular mechanisms. Jpn J Physiol 44: 433-473, 1994 https://doi.org/10.2170/jjphysiol.44.433
  3. Arnold WP, Mittal CK, Katsuki S, Murad F. Nitric oxide activates guanylate cyclase and increases guanosine 3':5'-cyclic monophosphate levels in various tissue preparations. Proc Natl Acad Sci U S A 74: 3203-3207, 1977 https://doi.org/10.1073/pnas.74.8.3203
  4. Boulton CL, Irving AJ, Southam E, Potier B, Garthwaite J, Collingridge GL. The nitric oxide-cyclic GMP pathway and synaptic transmission in rat hippocampal slices. Eur J Neurosci 6: 1528-1535, 1994 https://doi.org/10.1111/j.1460-9568.1994.tb00543.x
  5. Bredt DS, Snyder SH. Nitric oxide mediates glutamate-linked enhancement of cGMP levels in the cerebellum. Proc Natl Acad Sci U S A 86: 9030-9033, 1989 https://doi.org/10.1073/pnas.86.22.9030
  6. Caspary DM, Ling L, Turner JG, Hughes LF. Inhibitory neurotransmission, plasticity and aging in the mammalian central auditory system. J Exp Biol 211: 1781-1791, 2008 https://doi.org/10.1242/jeb.013581
  7. Caspary DM, Raza A, Lawhorn Armour BA, Pippen J, Arneric SP. Immunocytochemical and neurochemical evidence for age-related loss of GABA in the inferior colliculus: implication for neural presbycusis. J Neurosci 10: 2363-2372, 1990
  8. Chik CL, Liu QY, Li B, Karspinski E, Ho AK. cGMP inhibits L-type $Ca^{2+}$ channel currents through protein phosphorylation in rat pinealocytes. J Neurosci 15: 3104-3109, 1995
  9. Grassi C, D'Ascenzo M, Valente A, Battista Azzena G. $Ca^{2+}$ channel inhibition induced by nitric oxide in rat insulinoma RINm5F cells. Pflügers Arch 437: 241-247, 1999 https://doi.org/10.1007/s004240050775
  10. Hendry SH, Schwark HD, Jones EG, Yan J. Numbers and proportions of GABA-immunoreactive neurons in different areas of monkey cerebral cortex. J Neurosci 7: 1503-1519, 1987
  11. Huh YB, Park DC, Yeo SG, Cha CI. Evidence for increased NADPH- diaphorase-positive neurons in the central auditory system of the aged rat. Acta Otolaryngol 128: 648-653, 2008 https://doi.org/10.1080/00016480701636868
  12. Hupfer K, Jurgens U, Ploog D. The effect of superior temporal lesions on the recognition of species-specific calls in the squirrel monkey. Exp Brain Res 30: 75-87, 1977
  13. Jaffrey SR, Snyder SH. Nitric oxide: a neural messenger. Annu Rev Cell Dev Biol 11: 417-440, 1995 https://doi.org/10.1146/annurev.cb.11.110195.002221
  14. Jang IS, Rhee JS, Watanabe T, Akaike N, Akaike N. Histaminergic modulation of GABAergic transmission in rat ventromedial hypothalamic neurones. J Physiol (Lond.) 534: 791-803, 2001 https://doi.org/10.1111/j.1469-7793.2001.00791.x
  15. Klyachko VA, Ahern GP, Jackson MB. cGMP-mediated facilitation in nerve terminals by enhancement of the spike afterhyperpolarization. Neuron 31: 1015-1025, 2001 https://doi.org/10.1016/S0896-6273(01)00449-4
  16. Knight JA. The process and theories of aging. Annu Clin Lab Sci 25: 1-12, 1995
  17. Ko GY, Kelly PT. Nitric oxide acts as a postsynaptic signaling molecule in calcium/calmodulin-induced synaptic potentiation in hippocampal CA1 pyramidal neurons. J Neurosci 19: 6784-6794, 1999
  18. Kraus MM, Prast H. Involvement of nitric oxide, cyclic GMP and phosphodiesterase 5 in excitatory amino acid and GABA release in the nucleus accumbens evoked by activation of the hippocampal fimbria. Neuroscience 112: 331-343, 2002 https://doi.org/10.1016/S0306-4522(02)00079-9
  19. Lee JJ, Cho YW, Huh YB, Cha CI, Yeo SG. Effect of nitric oxide on auditory cortical neurons of aged rats. Neurosci Lett 447: 37-41, 2008 https://doi.org/10.1016/j.neulet.2008.09.074
  20. Liang L, Lu T, Wang X. Neural representations of sinusoidal amplitude and frequency modulations in the primary auditory cortex of awake primates. J Neurophysiol 87: 2237-2261, 2002
  21. Li DP, Chen SR, Finnegan TF, Pan HL. Signalling pathway of nitric oxide in synaptic GABA release in the rat paraventricular nucleus. J Physiol 554: 100-110, 2004 https://doi.org/10.1113/jphysiol.2003.053371
  22. Ling LL, Hughes LF, Caspary DM. Age-related loss of the GABA synthetic enzyme glutamic acid decarboxylase in rat primary auditory cortex. Neuroscience 132: 1103-1113, 2005 https://doi.org/10.1016/j.neuroscience.2004.12.043
  23. Manzoni O, Prezeau L, Marin P, Deshager S, Bockaert J, Fagni L. Nitric oxide induced blockade of NMDA receptors. Neuron 8: 653-662, 1992 https://doi.org/10.1016/0896-6273(92)90087-T
  24. Neff WD. The brain and hearing: auditory discriminations affected by brain leisions. Ann Otol Rhinol Laryngol 86: 500-506, 1977
  25. Ozaki M, Shibuya I, Kabashima N, Isse T, Noguchi J, Ueta Y, Inoue Y, Shigematsu A, Yamashita H. Preferential potentiation by nitric oxide of spontaneous inhibitory postsynaptic currents in rat supraoptic neurons. J Neuroendocrinol 12: 273-281, 2000 https://doi.org/10.1046/j.1365-2826.2000.00448.x
  26. Peinado M. Histology and histochemistry of the aging cerebral cortex; an overview. Microsc Res Tech 43: 1-7, 1998 https://doi.org/10.1002/(SICI)1097-0029(19981001)43:1<1::AID-JEMT1>3.0.CO;2-E
  27. Pineda J, Kogan JH, Aghajanian GK. Nitric oxide and carbon monoxide activate locus coeruleus neurons through a cGMP- dependent protein kinase: involvement of a nonselective cationic channel. J Neurosci 16: 1389-1399, 1996
  28. Prieto JJ, Peterson BA, Winer JA. Morphology and spatial distribution of GABAergic neurons in cat primary auditory cortex. J Comp Neurol 344: 349-382, 1994 https://doi.org/10.1002/cne.903440304
  29. Raza A, Arneric SP, Milbrandt J, Caspary DM. Age-related changes in brainstem auditory neurotransmitters: measures of GABA and acetylcholine function. Hear Res 77: 221-230, 1994 https://doi.org/10.1016/0378-5955(94)90270-4
  30. Schreiner CE, Read HL, Sutter ML. Modular organization of frequency integration in primary auditory cortex. Annu Rev Neurosci 23: 501-529, 2000 https://doi.org/10.1146/annurev.neuro.23.1.501
  31. Stamler JS, Toone EJ, Lipton SA, Sucher NJ. (S)NO signals: translocation, regulation, and a consensus motif. Neuron 18: 691-696, 1997 https://doi.org/10.1016/S0896-6273(00)80310-4
  32. Tewari K, Simard JM. Sodium nitroprusside and cGMP decrease $Ca^{2+}$ availability in basilar artery smooth muscle cells. Pflügers Arch 433: 304-311, 1997 https://doi.org/10.1007/s004240050281
  33. Tohse N, Sperelakis N. cGMP inhibits the activity of single calcium channels in embryonic chick heart cells. Circ Res 69: 325-331, 1991 https://doi.org/10.1161/01.RES.69.2.325
  34. Wei JY, Ethan J, Cohen D, Daw NW, Barnstable CJ. cGMP-induced presynaptic depression and postsynaptic facilitation at glutamatergic synapses in visual cortex. Brain Res 927: 42-54, 2002 https://doi.org/10.1016/S0006-8993(01)03323-6
  35. Wu LG, Saggau P. Pharmacological identification of two types of presynaptic voltage-dependent calcium channels at CA3-CA1 synapses of the hippocampus. J Neurosci 14: 5613-5622, 1994
  36. Yang Q, Chen SR, Li DP, Pan HL. KV1.1/1.2 channels are downstream effectors of nitric oxide on synaptic GABA release to preautonomic neurons in the paraventricular nucleus. Neuroscience 149: 315-327, 2007 https://doi.org/10.1016/j.neuroscience.2007.08.007
  37. Zagotta WN, Siegelbaum SA. Structure and function of cyclic nucleotide-gated channels. Annu Rev Neurosci 19: 235-263, 1996 https://doi.org/10.1146/annurev.ne.19.030196.001315

Cited by

  1. Nitrergic Inhibition of Tachykininergic Neuro-Muscular Transmission via Cyclic GMP in the Hamster Ileum vol.73, pp.4, 2009, https://doi.org/10.1292/jvms.10-0425
  2. Nitric Oxide-Mediated Posttranslational Modifications: Impacts at the Synapse vol.2016, pp.None, 2009, https://doi.org/10.1155/2016/5681036
  3. Nitric oxide promotes GABA release by activating a voltage-independent Ca2+ influx pathway in retinal amacrine cells vol.117, pp.3, 2009, https://doi.org/10.1152/jn.00803.2016
  4. Pathology of nNOS-Expressing GABAergic Neurons in Mouse Model of Alzheimer’s Disease vol.384, pp.None, 2009, https://doi.org/10.1016/j.neuroscience.2018.05.013
  5. Nitric Oxide Signaling in the Auditory Pathway vol.15, pp.None, 2009, https://doi.org/10.3389/fncir.2021.759342