International Journal of Oral Biology

The Korean Academy of Oral Biology (대한구강생물학회)
권호 표지

Effect of Gamma-Aminobutyric Acid on the Gustatory Nucleus Tractus Solitarius in Rats

  • Kim, Mi-Won (Medical School, School of Dentistry Chonnam National University) ;
  • Park, Ha-Ok (Dental Science Research, School of Dentistry Chonnam National University) ;
  • Pahng, Mong-Sook (Dental Science Research, School of Dentistry Chonnam National University) ;
  • Park, Sang-Won (Dental Science Research, School of Dentistry Chonnam National University) ;
  • Kim, Sun-Hun (Dental Science Research, School of Dentistry Chonnam National University) ;
  • Jung, Ji-Yeon (Dental Science Research, School of Dentistry Chonnam National University) ;
  • Jeong, Yeon-Jin (Dental Science Research, School of Dentistry Chonnam National University) ;
  • Kim, Won-Jae (Dental Science Research, School of Dentistry Chonnam National University)
  • Published : 2005.09.30
Download PDF
⟨ Previous Next ⟩

Abstract

Gamma-aminobutyric acid (GABA) is known as an inhibitory neurotransmitter in the neurons of the central nervous system. However, its detailed action mechanisms in the rostral gustatory zone of the nucleus tractus solitarius (rNTS) have not been established. The present study was aimed to investigate the distribution, role and action mechanisms of GABA in rNTS. Membrane potentials were recorded by whole cell recordings in isolated brain slices of the rat medulla. Superfusion of GABA resulted in a concentration-dependent reduction in input resistance in the neurons in rNTS. The change in input resistance ws accompanied by response to a depolarizing pulse were diminished by GABA. Superfusion of the slices with either $GABA_A$ agonist, muscimol, $GABA_B$ agonist, baclofen or $GABA_C$ agonist, TACA, decreased input resistance and reduced the nerve activity in association with membrane hyperpolarization. It is suggested that inhibitory signals playa role in sensory processing by the rNTS, in that GABA actions occur through activation of $GABA_A,\;GABA_B\;and\;GABA_C$ receptor. These results suggest that GABA has an inhibitory effect on the rNTS through an activation of $GABA_A,\;GABA_B\;and\;GABA_C$ receptors and that the GABAergic inhibition probably plays an important role in sensory processing by the rNTS.

Keywords

References

  1. Akasu, T., Munakata, Y., Tsurusaki, M., Hasuo, H.J. : Role of $GABA_A$ and $GABA_C$ receptors in the biphasic GABA responses in neurons ofthe rat major pelvic ganglia. Neurophysiol. 82: 1489-1496,1999 https://doi.org/10.1152/jn.1999.82.3.1489
  2. Barraco, R., El-Ridi, M., Ergene, E., Parizon, M., and Bradley, D.: An atlas of the rat subpostremal nucleus tractus solitarius. Brain Res. 29: 703-765,1992
  3. Blanton, M, Turco, J., and Kriegstein, A.: Whole cell recording from neurons in slices of reptilian and mammalian cerebral cortex. J. Neuroscience Methods. 30: 203-210, 1989 https://doi.org/10.1016/0165-0270(89)90131-3
  4. Bormann, J and Feigenspan, A.: $GABA_C$ receptors. Trends Neurosci. 18:515-519,1995 https://doi.org/10.1016/0166-2236(95)98370-E
  5. Bradley, R.M., Mistretta, C.M., Bates, C.A., and Killackey, H.R.: Transganglionic transport of HRP from the circum-vallate papilla of the rat. Brain Res. 361: 154-161,1985 https://doi.org/10.1016/0006-8993(85)91285-5
  6. Bradley, R.M., and Sweazey, R.D.: In vitro intracellular recordings from gustatory neurons in the rat solitary nucleus. Brain Res. 508: 168-171,1990 https://doi.org/10.1016/0006-8993(90)91133-2
  7. Bradley, R.M., and Sweazey, R.D.: Separation of neuron types in the gustatory zone of the nucleus tractus solitarii on the basis of intrinsic firing properties. J. Neurophysiol. 67: 1659-1668,1992 https://doi.org/10.1152/jn.1992.67.6.1659
  8. Bradley, R.M.: Neurobiology of the gustatory zone of nucleus tractus solitarius. In Nucleus of the Solitary Tract, edited by Barraco, R., Boca Raton: CRC, 51-62, 1994
  9. Bradley, R.M.: Essentials of Oral Physiology, St. Louis: Mosby. 86-123,1995
  10. Cherubini, E., Rovira, C, Gaiarsa, L., Corradetti, R. and Ben Ari, Y.: GABA mediated excitation in immature rat CA3 hippocampal neurons. J Developmental Neuroscience. 4: 481-490, 1990 https://doi.org/10.1016/0736-5748(90)90080-L
  11. Cherubini, E., Gaiarsa, J., and Ben-Ari, Y.: GABA an excitatory transmitter in early postnatal life. TINS. 12: 515-519,1991 https://doi.org/10.1016/0166-2236(91)90003-D
  12. Del Rio, J., Soriano, E. and Ferrer, I.: Development of GABA-Immunoreactivity in the Neocortex of the Mouse. J Comparative Neurology. 326: 501-526,1992 https://doi.org/10.1002/cne.903260403
  13. Doetsch, G.S., Ganchrow, J.J., Nelson, L.M., and Erickson, R.P.: Information processing in the taste system of the rat, in Olfaction and Taste III, Pfaffmann, C, Ed., Rockefeller University Press, New York. 492: 1969
  14. Doetsch, GS. and Erickson, R.P.: Synaptic processing of taste-quality information in the nucleus tractus solitarius of the rat. J. Neurophysiol. 33:490-507,1970 https://doi.org/10.1152/jn.1970.33.4.490
  15. Du, J. and Bradley, R.M.: Electrophysiological and morphological properties of neurons acutely isolated from the rostral gustatory zone of the rat nucleus of the solitary tract. Chem. Senses. 21: 729-737,1996 https://doi.org/10.1093/chemse/21.6.729
  16. Fitzgerald, M., and Fulton, B.P.: The physiological properties of developing sensory neurons. In: Sensory Neurons, Diversity, Development and Plasticity, edited by S.A. Scott. New York: Oxford. 287-306,1992
  17. Grabauskas, G. and Bradley, R.M.: Tetanic stimulation induces short-term potentiation of inhibitory synaptic activity in the rostral nucleus of the solitary tract. J. Neurophysiol. 79: 595-604,1998 https://doi.org/10.1152/jn.1998.79.2.595
  18. Hamilton, R.B. and Norgren, R.: Central projections of gustatory nerves in the rat. J. Comp. Neurol. 222: 560-577, 1984 https://doi.org/10.1002/cne.902220408
  19. Hill, D.L. and Mistretta, C.M.: Developmental neurobiology of salt taste sensation. Trends in Neurosci. 13: 188-195, 1990 https://doi.org/10.1016/0166-2236(90)90046-D
  20. Johnston, G.A.: $GABA_C$ receptors: relatively simple transmitter-gated ion channels? Trends Pharmaco Sci. 17: 319-323,1996 https://doi.org/10.1016/0165-6147(96)10038-9
  21. Kim, K.H., Takeuchi, H. : Pharmacological characteristics of two different types of inhibitory GABAreceptors on Achatina fulica neurones. Eur J Pharmacol. 182: 49-62,1990 https://doi.org/10.1016/0014-2999(90)90492-O
  22. King, M., Wang, L., and Bradley, R.: Substance P excites neurones in the gustatory zone of the rat nucleus tractus solitarius. Brain Research. 619: 120-130,1993 https://doi.org/10.1016/0006-8993(93)91603-P
  23. King, M. and Bradley, R.: Relationship between structure and Function of Neurons in the rat rostral nucleus tractus solitarii. J Comparative Neurology. 344: 50-64,1994 https://doi.org/10.1002/cne.903440105
  24. Koller, H., Siebler, M., Schmalenbach, C. and Muller, H.: GABA and glutamate receptor development of cultured neurons from rat hippocampus, septal region, and neocortex. Synapse. 5: 59-64,1990 https://doi.org/10.1002/syn.890050105
  25. Kriegstein, A.R., Suppes, T., and Prince, D.A.: Cellular and synaptic physiology and epileptogenesis of developing rat neocortical neurons in vitro. Developmental Brain Research. 34:161-171,1987 https://doi.org/10.1016/0165-3806(87)90206-9
  26. Lasiter, P.S. and Kachele, D.L.: Organization of GABA and GABA-transaminas containing neurons in the gustatory zone of the nucleuos the solitary tract. Brain Res. Bull. 21: 623-636, 1988 https://doi.org/10.1016/0361-9230(88)90202-X
  27. Lasiter, P.S., Wong, D.M., and Kachele, D.L.: Postnatal development of the rostral solitary nucleus in rat: dendritic morphology and mitochondrial enzyme activity. Brain Research Bull. 21: 313-321,1989 https://doi.org/10.1016/0361-9230(89)90059-2
  28. MacDermott, A.B., and Westbrook, GL.: Early development of voltage-dependent sodium currents in cultured mouse spinal cord neurons. Devel. Biol. 113: 317-326,1986 https://doi.org/10.1016/0012-1606(86)90167-3
  29. McCormick, D.A., and Prince, D.A.: Postnatal development of electrophysiological properties of rat cerebral cortical pyramidal neurons. J. Physiology. 393: 743-762,1987 https://doi.org/10.1113/jphysiol.1987.sp016851
  30. Mistretta, C.M.: Developmental neurobiology of the taste system. In Smell and Taste in Health and Disease, edited by Getchell, T.V., Doty, R.L., Bartoshuk, L.M., and Snow, J.B.Jr, New York: Raven Press. 35-64,1991
  31. Pfaffmann, C, Erickson, R.P., Frommer, G.P., and Halpern, B.P.: Gustatory discharbes in the rat medulla and thalamus, in Sensory Communication, Rosenblith, W.A., Ed., MIT Press, Cambridge. 455: 1961
  32. Tell, F., and Bradley, R.M.: 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 https://doi.org/10.1152/jn.1994.71.2.479
  33. Travers, J.B., Travers, S.P., and Norgren, R.: Gustatory neural processing in the hindbrain. Annu. Rev. Neurosci. 10: 595-632, 1987 https://doi.org/10.1146/annurev.ne.10.030187.003115
  34. Vogt, M. and Mistretta, C.M.: Convergence in mammalian nucleus of solitary tract during development and functional differentiation of salt taste circuits. J. Neurosci. 10: 3148-3157,1990
  35. Walton, M., Schaffner, A. and Barker, J.: Sodium channels, $GABA_A$ receptors, and glutamate receptors develop sequentially on embryonic rat spinal cord cells. J Neuroscience. 13: 2068-2084,1993
  36. Whitehead, M.C.: Neuronal architecture of the nucleus of the solitary tract in the hamster. J. Comp. Neurol. 276: 547-572, 1988 https://doi.org/10.1002/cne.902760409
  37. Zhang, L.: Development of GABA-mediated, chloride-dependent inhibition in CA1 pyramidal neurones of immature rat hippocampal slices. J. Physiology. 444:25-49,1991 https://doi.org/10.1113/jphysiol.1991.sp018864
  38. Zhang, W., Han, X.Y., Wong, S.M., Takeuchi, H. : Pharmacologic characteristics of excitatory gamma-amino-butyric acid (GABA)receptors in a snail neuron. Gen Pharmacol, 28:45-53,1997 https://doi.org/10.1016/S0306-3623(96)00152-8