Group I mGluRs increase locomotor network excitability in Xenopus tadpoles via presynaptic inhibition of glycinergic neurotransmission

European Journal of Neuroscience

Volumn 28, Issue 5, 2008, Pages 903-913

  Chapman, Rebecca J ^a,b   Issberner, Jonathan P ^a   Sillar, Keith T ^a  

^a UNIVERSITY OF ST ANDREWS   (United Kingdom)

^b UNIVERSITY OF LEEDS   (United Kingdom)

Author keywords

Glycine; Neuromodulation; Spinal cord; Vertebrate; Xenopus laevis

Indexed keywords

GLYCINE RECEPTOR ANTAGONIST; STRYCHNINE;

AMPLITUDE MODULATION; ANIMAL EXPERIMENT; ARTICLE; BRAIN NERVE CELL; CONTROLLED STUDY; EMBRYO; LOCOMOTION; MEMBRANE POTENTIAL; MOTONEURON; NERVE EXCITABILITY; NEUROTRANSMISSION; NONHUMAN; PRESYNAPTIC INHIBITION; PRIORITY JOURNAL; SWIMMING; SYNAPTIC TRANSMISSION; TADPOLE; TASK PERFORMANCE; XENOPUS;

ANIMALS; EXCITATORY POSTSYNAPTIC POTENTIALS; GLYCINE; GLYCINE AGENTS; INHIBITORY POSTSYNAPTIC POTENTIALS; LARVA; LOCOMOTION; NERVE NET; NEURAL INHIBITION; PRESYNAPTIC TERMINALS; RECEPTORS, GLYCINE; RECEPTORS, METABOTROPIC GLUTAMATE; SPINAL CORD; STRYCHNINE; SWIMMING; SYNAPTIC TRANSMISSION; UP-REGULATION; XENOPUS LAEVIS;

EID: 50449088385     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2008.06391.x     Document Type: Article

References (46)

1. Anwyl, R. (1999) Metabotropic glutamate receptors: electrophysiological properties and role in plasticity. Brain Res. Rev., 29, 83 120.
2. Boothby, K.M. Roberts, A. (1992a) The stopping response of Xenopus laevis embryos: pharmacology and intracellular physiology of rhythmic spinal neurons and hindbrain neurons. J. Exp. Biol., 169, 65 86.
3. Boothby, K.M. Roberts, A. (1992b) The stopping response of Xenopus laevis embryos: behaviour, development and physiology. J. Comp. Physiol. A., 170, 171 180.
4. Burke, J.P. Hablitz, J.J. (1994) Presynaptic depression of synaptic transmission mediated by activation of metabotropic glutamate receptors in rat neocortex. J. Neurosci., 14, 5120 5130.
5. Chapman, R.J. (2005) The role of metabotropic glutamate receptors in the control of swimming in hatchling Xenopus laevis tadpoles. PhD thesis. University of St Andrews.
6. Chapman, R.J. Sillar, K.T. (2003) Activation of group I metabotropic glutamate receptors contributes to the modulation of rhythmic motor activity in Xenopus laevis. SFN Abstracts 277.8.
7. Chapman, R.J. Sillar, K.T. (2007) Modulation of a spinal locomotor network by metabotropic glutamate receptors. Eur. J. Neurosci., 26, 2257 2268.
8. Cochilla, A.J. Alford, S. (1998) Metabotropic glutamate receptor-mediated control of neurotransmitter release. Neuron, 20, 1007 1016.
9. Dale, N. (1995) Experimentally derived model for the locomotor pattern generation in the Xenopus embryo. J. Physiol., 489, 489 510.
10. Dale, N. Kuenzi, F.M. (1997) Ion channels and the control of swimming in the Xenopus embryo. Prog. Neurobiol., 53, 729 756.
11. Dale, N. Roberts, A. (1984) Excitatory amino acid receptors in Xenopus embryo spinal cord and their role in the activation of swimming. J. Physiol., 348, 527 543.
12. Dale, N. Roberts, A. (1985) Dual-component amino-acid-mediated synaptic potentials: excitatory drive for swimming in Xenopus embryos. J. Physiol., 363, 35 59.
13. Dale, N., Ottersen, O.P., Roberts, A. Storm-Mathisen, J. (1986) Inhibitory neurones of a motor pattern generator in Xenopus revealed by antibodies to glycine. Nature, 324, 255 257.
14. Desai, M.A. Conn, P.J. (1991) Excitatory effects of ACPD receptor activation in the hippocampus are mediated by direct effects on pyramidal cells and blockade of synaptic inhibition. J. Neurophys., 66, 40 52.
15. Drew, G.M. Vaughan, C.W. (2004) Multiple metabotropic glutamate receptor subtypes modulate GABAergic neurotransmission in rat periaqueductal grey neurons in vitro. Neuropharm., 46, 927 934.
16. El Manira, A., Kyriakatos, A., Nanou, E. Mahmood, R. (2008) Endocannabinoid signalling in the spinal locomotor circuitry. Brain Res. Rev., 57, 29 36.
17. Glitsch, M., Llano, J. Marty, A. (1996) Glutamate as a candidate retrograde messenger at interneurone-purkinje synapses of rat cerebellum. J. Physiol., 497, 531 537.
18. A, glycine receptor, and mixed synaptic currents in Renshaw cells and ventral spinal interneurons. J. Neurosci., 25, 2010 2023.
19. Grillner, S., Deliagina, T., Ekeberg, O., El Manira, A., Hill, R.H., Lansner, A., Orlovsky, G.N. Wallen, P. (1995) Neural networks that co-ordinate locomotion and body orientation in lamprey. Trends Neurosci., 18, 270 279.
20. Hellgren, J., Grillner, S. Lansner, A. (1992) Computer simulation of the segmental neural network generating locomotion in lamprey by using populations of network interneurons. Biol. Cybern., 68, 1 13.
21. Holohean, A.M., Hackman, J.C. Davidoff, R.A. (1999) Mechanisms involved in the metabotropic glutamate receptor-enhancement of NMDA-mediated motoneurone responses in frog spinal cord. Br. J. Pharmacol., 126, 333 341.
22. Katsurabayashi, S., Kubota, H., Wang, Z.M., Rhee, J.S. Akaike, N. (2001) cAMP-dependent presynaptic regulation of spontaneous glycinergic IPSCs in mechanically dissociated rat spinal cord neurons. J. Neurophysiol., 85, 332 340.
23. 5, mediates depolarization of spinal cord neurons by blocking a leak current. J. Neurophysiol., 90, 2341 2348.
24. Kettunen, P., Kyriakatos, A., Hallen, K. El Manira, A. (2005) Neuromodulation via conditional release of endocannabinoids in the spinal locomotor network. Neuron, 45, 95 104.
25. Kiehn, O. Katz, P.S. (1999) Making circuits dance: neuromodulation of motor systems. In Katz, P.S. (Ed Beyond Neurotransmission: Neuromodulation and its importance for information processing. Oxford University Press, New York, pp. 1 28.
26. Kyriakatos, A. El Manira, A. (2007) Long-term plasticity of the spinal locomotor circuitry mediated by endocannabinoid and nitric oxide signalling. J. Neurosci., 27, 12664 12674.
27. Li, W.C., Perrins, R., Soffe, S.R., Yoshida, M., Walford, A. Roberts, A. (2001) Defining classes of spinal interneuron and their axonal projections in hatchling Xenopus laevis tadpoles. J. Comp. Neurol., 441, 248 265.
28. Marino, M.J., Wittman, M., Bradley, S.R., Hubert, G.W., Smith, Y. Conn, P.J. (2001) Activation of group I metabotropic glutamate receptors produces a direct excitation and disinhibition of GABAergic projection neurons in the substantia nigra pars reticulata. J. Neurosci., 21, 7001 7012.
29. McDearmid, J., Scrymgeour-Wedderburn, J.F.S. Sillar, K.T. (1997) Aminergic modulation of glycine release in a spinal network controlling swimming in Xenopus Laevis. J. Physiol., 503, 1473 1482.
30. McLean, D.L. Sillar, K.T. (2000) The distribution of NADPH-diaphorase- labelled interneurons and the role of nitric oxide in the swimming system of Xenopus laevis larvae. J. Exp. Biol., 203, 705 713.
31. McLean, D.L. Sillar, K.T. (2002) Nitric Oxide selectivity tunes inhibitory synapses during vertebrate locomotion. J. Neurosci., 22, 4175 4184.
32. McLean, D.L. Sillar, K.T. (2004) Metamodulation of a spinal locomotor network by Nitric Oxide. J. Neurosci., 24, 9561 9571.
33. McLean, D.L., McDearmid, J.R. Sillar, K.T. (2001) Induction of a non-rhythmic motor pattern by nitric oxide in hatchling Rana temporaria embryos. J. Exp. Bio., 204, 1307 1317.
34. Merrywest, S.D., Fischer, H. Sillar, K.T. (2002) Alpha-adrenoreceptor activation modulates swimming via glycinergic and GABAergic inhibitory pathways in Xenopus laevis tadpoles. Eur. J. Neurosci., 15, 375 383.
35. Nieuwkoop, P.D. Faber, J. (1956) Normal Tables of Xenopus laevis (Daudin). North Holland, Amsterdam.
36. de Novellis, V., Marabrese, I., Palazzo, E., Rossi, F., Berrino, L., Rodella, L. et al. (2003) Group I metabotropic glutamate receptors modulate glutamate and gamma-aminobutyric acid release in the periaqueductal grey of rats. Eur. J. Pharmacol., 462, 73 81.
37. Perrins, R. Roberts, A. (1995) Cholinergic and electrical motoneuron-to-motoneuron synapses contribute to on-cycle excitation during swimming in Xenopus embryos. J. Neurophys., 73, 1005 1012.
38. Poncer, J.C., Shinozaki, H. Miles, R. (1995) Dual modulation of synaptic inhibition by distinct metabotropic glutamate receptors in the rat hippocampus. J. Phys., 485, 121 134.
39. Reith, C.A. Sillar, K.T. (1997) Pre- and postsynaptic modulation of spinal GABAergic neurotransmission by the neurosteroid, 5beta-pregnan-3alpha-ol- 20-one. Brain Res., 770, 202 212.
40. Sillar, K.T. Roberts, A. (1988) Unmyelinated cutaneous afferent neurons activate two types of excitatory amino acid receptor in the spinal cord of Xenopus laevis embryos. J. Neurosci., 8, 1350 1360.
41. Sillar, K.T., Fischer, H., McLean, D.L. Merrywest, S.D. (2002) Fast inhibitory synapses: targets for neuromodulation and development of vertebrate motor behaviour. Brain Res. Rev., 40, 130 140.
42. Singer, J.H. Berger, A.J. (1999) Contribution of single-channel properties to the time course and amplitude variance of quantal glycine currents recorded in rat motorneurons. J. Neurophysiol., 81, 1608 1616.
43. Soffe, S.R. (1987) Ionic and pharmacological properties of reciprocal inhibition in Xenopus embryo motorneurons. J. Physiol., 382, 463 473.
44. Soffe, S.R. (1993) Two distinct rhythmic motor patterns are driven by common premotor and motorneurons in a simple vertebrate spinal cord. J. Neurosci., 13, 4456 4469.
45. B receptors modulate glycinergic inhibition and spike threshold in Xenopus embryo spinal neurons. J. Physiol., 469, 275 290.
46. Zhao, F.Y. Roberts, A. (1998) Assessing the roles of glutamatergic and cholinergic synaptic drive in the control of fictive swimming frequency in young Xenopus tadpoles. J. Comp. Physiol. A., 183, 753 758.