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Involvement of Group II Metabotropic Glutamate Receptors in Modulation of Evoked Activity in Frog Spinal Motoneurons

  • Comparative and Ontogenic Physiology
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Abstract

The effect of the agonist of group II mGluRs, including mGluR2 and mGluR3 (mGluR 2/3) receptor subtypes, on evoked activity and electric membrane properties of frog spinal (lumbar) motoneurons was studied electrophysiologically on sections of the isolated spinal cord. Extracellular recordings revealed a decrease in the amplitude of short-latency components of spinal reflexes and in the overall response area under the effect of DCG-IV [2S,2'R,3'R)-2-(2',3'-dicarboxycyclopropyl)glycine], a mGluR 2/3 agonist, within its concentration range of 0.05-5 μM. The half-maximal effective concentration (EC50) of the agonist for the suppression of short-latency response components was about 0.5 μM. Intracellular recordings of postsynaptic potentials from motoneurons upon DCG-IV application demonstrated a decrease in the number of spikes and the overall area of responses evoked by dorsal root stimulation. Most of motoneurons studied responded with hyperpolarization, increased amplitude of antidromic action potentials, altered afterpotential amplitude and increased excitability, indicative of the agonist effect on postsynaptic group II mGluRs in frog spinal motoneurons.

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References

  1. Karamyan, O.A., Chmykhova, N.M., and Veselkin, N.P., Second messengers in the presynaptic regulation of glycinergic synapse in frog moto-neurons, Neurosci. Behav. Physiol., 2018, vol. 48,no. 2, pp. 166–173.

    Article  CAS  Google Scholar 

  2. Conn, P.J. and Pin, J.P., Pharmacology and functions of metabotropic glutamate receptors, Annu. Rev. Pharmacol. Toxicol., 1997, vol. 37, pp. 205–237.

    Article  CAS  PubMed  Google Scholar 

  3. Marti, M., Paganini, F., Stocchi, S., Bianchi, C., Beani, L., and Morari, M., Presynaptic group I and II metabotropic glutamate receptors oppositely modulate striatal acetylcholine release, Eur. J. Neurosci., 2001, vol.14, pp. 1181–1184.

    Article  CAS  PubMed  Google Scholar 

  4. Chen, C.Y., Ling, E., Horowitz, J.M., and Bonham, A.C., Synaptic transmission in nucleus tractus solitarius is depressed by Group II and III but not Group I presynaptic metabotropic glutamate receptors in rats, J. Physiol., 2002, vol. 538, pp. 773–786.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Farazifard, R. and Wu, S.H., Metabotropic glutamate receptors modulate glutamatergic and GABAergic synaptic transmission in the central nucleus of the inferior colliculus, Brain Res., 2010, vol. 1325, pp. 28–40.

    Article  CAS  PubMed  Google Scholar 

  6. Ishida, M., Saitoh, T., Shimamoto, K., Ohfune, Y., and Shinozaki, H., A novel metabotropic glutamate receptor agonist: marked depression of monosynaptic excitation in the newborn rat isolated spinal cord, Brit. J. Pharmacol., 1993, vol. 109, pp. 1169–1177.

    Article  CAS  Google Scholar 

  7. Taccola, G., Marchetti, C., and Nistry, A., Role of group II and III metabotropic glutamate receptors in rhythmic patterns of the neonatal rat spinal cord in vitro, Exp. Brain Res., 2004, vol. 156, pp. 495–504.

    Article  CAS  PubMed  Google Scholar 

  8. Zhou, H.Y., Chen, S.R., Chen, H., and Pan, H.L., Functional plasticity of group II metabotropic glutamate receptors in regulating spinal excitatory and inhibitory synaptic input in neuropathic pain, J. Pharmacol. Exp. Ther., 2010. doi:10.1124/jpet.110.173112

    Google Scholar 

  9. Petralia, R.S., Wang, Y.-X., Niedzielski, A.S., and Wenthold, R.J., The metabotropic glutamate receptors, mGluR2 and mGluR3, show unique postsynaptic, presynaptic and glial localizations, Neu-rosci., 1996, vol. 71,no. 1, pp. 949–976.

    CAS  Google Scholar 

  10. Tang, F.R. and Sim, M.K., Pre- and/or post-syn-aptic localisation of metabotropic glutamate receptor 1α (mGluR1α) and 2/3 (mGluR 2/3) in the rat spinal cord, Neurosci. Res., 1999, vol. 34,iss. 2, pp. 73–78.

    Article  CAS  PubMed  Google Scholar 

  11. Cox, C.L. and Sherman, S.M., Glutamate inhibits thalamic reticular neurons, J. Neurosci., 1999, vol. 19, pp. 6694–6699.

    Article  CAS  PubMed  Google Scholar 

  12. Donato, R., Lape, R., and Nistry, A., Pre- and postsynaptic effects of metabotropic glutamate receptor activation on neonatal rat hypoglossal moto-neurons, Neurosci. Lett., 2003, vol. 338, pp. 9–12.

    Article  CAS  PubMed  Google Scholar 

  13. Muly, E.C., Mania, I., Guo JiDong, and Rainnie, D.J., Group II metabotropic glutamate receptors in anxiety circuitry: correspondence of physiological response and subcellular distribution, J. Comp. Neurol., 2007, vol. 505, pp. 682–700.

    Article  CAS  PubMed  Google Scholar 

  14. Lee, C.C. and Sherman, S.M., Glutamatergic inhibition in sensory neocortex, Cereb. Cortex, 2009, vol. 19, pp. 2281–2289.

    Article  PubMed  PubMed Central  Google Scholar 

  15. Lee, C.C. and Sherman, S.M., Intrinsic modulators of auditory thalamocortical transmission, Hearing Res., 2012, vol. 287, pp. 43–50.

    Article  Google Scholar 

  16. Lee, C.C., Inhibition of mamillary body neurons by direct activation of Group II metabotropic glutamate receptors, Neurotransmitter, 2016, vol. 3, pp. 1–10. e1357.doi: 10.14800/nt1357.

    CAS  Google Scholar 

  17. Bongianni, F., Mutolo, D., Carfi, M., and Pantaleo, T., Group I and II metabotropic glutamate receptors modulate respiratory activity in the lamprey, Eur. J. Neurosci., 2002, vol. 16, pp. 454–460.

    Article  PubMed  Google Scholar 

  18. Karamyan, O.A., Kozhanov, V.M., Masalov, I.S., Chmykhova, N.M., and Veselkin, N.P., The role of group II and II metabotropic glutamate receptors in modulation of miniature synaptic activity in frog spinal cord motoneurons, Cell Tiss. Biol., 2008, vol. 2,no. 5, pp. 493–503.

    Article  Google Scholar 

  19. Lodge, D., Tidball, P., Mercier, M.S., Lucas, S., Hanna, L., Ceolin, L., Kriticos, M., Fitzjohn, S.M., Sherwood, J.L., Bannister, N., Volianskis, A., Jane, D.E., Bortolotto, Z.A., and Collingridge, G.L., Antagonists reversibly reverse chemical LTD induced by group I, group II and group III metabotropic glutamate receptors, Neu-ropharmacol., 2013, vol. 74, pp. 135–146.

    CAS  Google Scholar 

  20. Lucas, S.J., Bortolotto, Z.A., Collingridge, G.L., and Lodge, D., Selective activation of either mGluR2 or mGluR3 receptors can induce LTD in the amygdale, Neuropharmacol., 2013, vol. 66, pp. 196–201.

    Article  CAS  Google Scholar 

  21. Tyszkiewicz, J.P., Gu, Z., Wang, X., Cai, X., and Yan, Z., Group II metabotropic glutamate receptors enhance NMDA receptor currents via a protein kinase C-dependent mechanism in pyramidal neurones of rat prefrontal cortex, J. Physiol., 2003, vol. 554,no. 3, pp. 765–777.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Trepanier, С., Lei, G., Xie, Y.-F., and MacDonald, J., Group II metabotropic glutamate receptors modify N-metyl-D-aspartate receptors via Srcki-nase, Sci. Rep., 2013, vol. 3, pp. 926–934.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Gereau, R.W. and Conn, P.J., Roles of specific metabotropic glutamate receptor subtypes in regulation of hippocampal CA1 pyramidal cell excitability, J. Neurophysiol., 1995, vol. 74, pp. 122–129.

    Article  CAS  PubMed  Google Scholar 

  24. Rainnie, D.G., Holmes, K.H., and Shinnock-Gallagher, P., Activation of metabotropic glutamate receptors by trans-ACPD hyperpolarizes neurons of the basolateral amygdale, J. Neurosci., 1994, vol. 14, pp. 7208–7220.

    Article  CAS  PubMed  Google Scholar 

  25. Holmes, K.H., Keele, N.B., and Shinnick-Gallagher, P., Loss of mGluR- mediated hyperpolar-izations and increase in mGluR depolarizations in basolateral amygdala neurons in kindling-induced epilepsy, J. Neurophysiol., 1996, vol. 76, pp. 2808–2812.

    Article  CAS  PubMed  Google Scholar 

  26. Dutar, P., Petrozzino, J.J., Vu, H.M., Schmidt, M.F., and Perkel, D.J., Slow synaptic inhibition mediated by metabotropic glutamate receptor activation of GIRK channels, J. Neuro-physiol., 2000, vol. 84, pp. 2284–2290.

    CAS  Google Scholar 

  27. Watanabe, D. and Nakanishi, S., mGluR2 post-synaptically senses granule cell inputs at Golgi cell synapses, Neuron, 2003, vol. 39, pp. 821–829.

    Article  CAS  PubMed  Google Scholar 

  28. Sekizawa, S., Bechtold, A.G., Tham, R.C., and Bonham, A.C., A novel postsynaptic group II metabotropic glutamate receptor role in modulating baroreceptor signal transmission, J. Neurosci., 2009, vol. 29, pp. 11 807–11 816.

    Article  CAS  Google Scholar 

  29. Zhang, H., Cilz, N.I., Yang, C., Hu, B., Dong, H., and Lei, S., Depression of neuronal excitability and epileptic activities by group II metabotropic glutamate receptors in the medial entorhinal cortex, Hippocampus, 2015, vol. 25, pp. 1299–1313.

    Article  CAS  PubMed  Google Scholar 

  30. Lorinz, A. and Nusser, Z., Cell-type-dependent molecular composition of the axon initial segment, J. Neurosci., 2008, vol. 2008(28), pp. 53 14–329 14.

    Google Scholar 

  31. Anwyl, R., Metabotropic glutamate receptors: electrophysiological properties and role in plasticity, Brain. Res. Rev., 1999, vol. 29, pp. 83–120.

    Article  CAS  PubMed  Google Scholar 

  32. Stuart, D., The segmental motor system-advances, issues and possibilities, Progress in Brain Research, Binder, M., Ed., Elsevier Science B.V., 1999, vol. 123, pp. 3–28.

    Article  CAS  PubMed  Google Scholar 

  33. Cotel, F., Antri, M., Barthe, J.-Y., and Orsal, D., Identified ankle extensor and flexor motoneurons display different firing profiles in the neonatal rat, J. Neurosci., 2009, vol. 29, pp. 2748–2753.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Krutki, P., Hałuszka, A., Mrówczynski, W., Gardiner, P.F., and Celichowski, J., Adaptations of motoneuron properties to chronic compensatory muscle overload, J. Neurophysiol., 2015, vol. 113, pp. 2769–2777.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Authors and Affiliations

  1. Sechenov Institute of Evolutionary Physiology and Biochemistry, Russian Academy of Sciences, St. Petersburg, Russia

    N. M. Chmykhova, S. O. Gapanovich & N. P. Veselkin

  2. St. Petersburg State University, St. Petersburg, Russia

    E. N. Pariyskaya & N. P. Veselkin

Authors
  1. N. M. Chmykhova
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  2. S. O. Gapanovich
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  3. E. N. Pariyskaya
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  4. N. P. Veselkin
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Correspondence to N. M. Chmykhova.

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Russian Text © The Author(s), 2019, published in Zhurnal Evolyutsionnoi Biokhimii i Fiziologii, 2019, Vol. 55, No. 2, pp. 121–129.

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Chmykhova, N.M., Gapanovich, S.O., Pariyskaya, E.N. et al. Involvement of Group II Metabotropic Glutamate Receptors in Modulation of Evoked Activity in Frog Spinal Motoneurons. J Evol Biochem Phys 55, 131–139 (2019). https://doi.org/10.1134/S0022093019020066

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  • DOI: https://doi.org/10.1134/S0022093019020066

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