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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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.
Conn, P.J. and Pin, J.P., Pharmacology and functions of metabotropic glutamate receptors, Annu. Rev. Pharmacol. Toxicol., 1997, vol. 37, pp. 205–237.
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.
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.
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.
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.
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.
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
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.
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.
Cox, C.L. and Sherman, S.M., Glutamate inhibits thalamic reticular neurons, J. Neurosci., 1999, vol. 19, pp. 6694–6699.
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.
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.
Lee, C.C. and Sherman, S.M., Glutamatergic inhibition in sensory neocortex, Cereb. Cortex, 2009, vol. 19, pp. 2281–2289.
Lee, C.C. and Sherman, S.M., Intrinsic modulators of auditory thalamocortical transmission, Hearing Res., 2012, vol. 287, pp. 43–50.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
Watanabe, D. and Nakanishi, S., mGluR2 post-synaptically senses granule cell inputs at Golgi cell synapses, Neuron, 2003, vol. 39, pp. 821–829.
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.
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.
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.
Anwyl, R., Metabotropic glutamate receptors: electrophysiological properties and role in plasticity, Brain. Res. Rev., 1999, vol. 29, pp. 83–120.
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.
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.
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.
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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