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Localization and Functions of Kainate Receptors in the Basal Ganglia

  • Xiao-Tao Jin
  • Yoland Smith
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 717)

Abstract

Kainate receptors (KARs) are one of the three subtypes of ionotropic glutamate receptors in the CNS. These receptors are widely expressed pre- and postsynaptically throughout the brain. Thus, kainate receptor activation mediates a large variety of pre- and postsynaptic effects on either glutamatergic or GABAergic synaptic transmission. Although ionotropic functions for KAR have been described in multiple brain regions, there is considerable evidence from various CNS regions that KARs activation modulates GABA release through either G-protein dependent metabotropic pathway or secondary activation of G-protein coupled receptors. In the present chapter, we provide further evidence supporting that these two pathways are also involved in the modulation of GABA release in specific basal ganglia nuclei. Because of their more subtle effects on neurotransmisison regulation than other ionotropic glutamate receptors, KARs represent interesting targets for the future development of pharmacotherapy for basal ganglia diseases.

Keywords

Gaba Release Kainate Receptor Secondary Activation Striatal Interneuron GABAergic Synaptic Transmission 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. 1.
    Hollman M, Heinemann S. Cloned glutamate receptors. Annu Rev Neurosci 1994; 17:31–108.CrossRefGoogle Scholar
  2. 2.
    Bettler B, Mulle C. Neurotransmitter receptors IL AMPA and kainat ereceptors. Neuropharmacology 1995; 34:123–139.PubMedCrossRefGoogle Scholar
  3. 3.
    Charara A, Blankstein E, Smith Y. Presynaptic kainate receptors in the monkey striatum. Neuroscience 1999; 91(4):1195–1200.PubMedCrossRefGoogle Scholar
  4. 4.
    Lerma J, Paternain AV, Rodriguez-Moreno A et al. Molecular physiology of kainate receptors. Physiol Rev 2001; 81:971–998.PubMedGoogle Scholar
  5. 5.
    Kieval JZ, Hubert GW, Charara A et al. Subcellular and subsynaptic localization of presynaptic and postsynaptic kainate receptor subunits in the monkey striatum. J Neurosci 2001; 21:8746–8757.PubMedGoogle Scholar
  6. 6.
    Kullmann DM. Presynaptic kainate receptors in the hippocampus: slowly emerging from obscurity. Neuron 2001; 32:561–564.PubMedCrossRefGoogle Scholar
  7. 7.
    Huettner JE. Kainate receptors and synaptic transmission. Prog in Neurobiol 2003; 70(5):387–407.CrossRefGoogle Scholar
  8. 8.
    Lerma J. Roles and rules of kainate receptors in synaptic transmission. Nat Rev Neurosci 2003; 4(6):481–495.PubMedCrossRefGoogle Scholar
  9. 9.
    Jin X-T, Paré JF, Raju DV et al. Localization and function of pre and postsynaptic kainate receptors in the rat globus pallidus. Eur J Neurosci 2006; 23:374–386.PubMedCrossRefGoogle Scholar
  10. 10.
    Melyan Z, Lancaster B, Wheal HV. Metabotropic regulation of intrinsic excitability by synaptic activation of kainate receptors. J Neurosci 2004; 24:4530–4534.PubMedCrossRefGoogle Scholar
  11. 11.
    Braga MFM, Aroniadou-Anderjaska V, Xie J et al. Bidirectional modulation of GABA release by presynaptic glutamate receptor 5 kainate receptors in the basolateral amygdala. J Neurosci 2003; 23(2):442–452.PubMedGoogle Scholar
  12. 12.
    Cossart R, Tyzio R, Dinocourt C et al. Presynaptic kainate receptors that enhance the release of GABA on CA1 hippocampal interneurons. Neuron 2001; 29(2):497–508.PubMedCrossRefGoogle Scholar
  13. 13.
    Jin X-T, Smith Y. Activation of presynaptic kainate receptors suppresses GABAergic synaptic transmission in the globus pallidus. Neuroscience 2007; 149:338–349.PubMedCrossRefGoogle Scholar
  14. 14.
    Smith Y, Charara A, Paquet M et al. Ionotropic and metabotropic GABA and glutamate receptors in primate basal ganglia. J Chem Neuroanat 2001; 22:13–42.PubMedCrossRefGoogle Scholar
  15. 15.
    Bahn S, Volk B, Wisden W. Kainate receptor gene expression in the developing rat brain. J Neurosci 1994; l4(9):5525–5547.Google Scholar
  16. 16.
    Bischoff S, Barhanin J, Bettler B et al. Spatial distribution of kainate receptor subunit mRNA in the mouse basal ganglia and ventral mesencephalon. J Comp Neurol 1997; 379:541–562.PubMedCrossRefGoogle Scholar
  17. 17.
    Chergui K, Bouron A, Normand E et al. Functional GluR6 kainate receptors in the striatum: indirect downregulation of synaptic transmission. J Neurosci 2000; 20(6):2175–2182.PubMedGoogle Scholar
  18. 18.
    Crowder TL, Ariwodola OJ, Weiner JL. Kainate receptor activation potentiates GABAergic synaptic transmission in the nucleus accumbens core. Brain Res 2006; 73–82.Google Scholar
  19. 19.
    Koos T, Tepper J. Inhibittory control of neurostriatal projection neurons by GABAergic interneurons. Nat Neurosci 1999; 2:467–472.PubMedCrossRefGoogle Scholar
  20. 20.
    Tepper JM, Bolam JR Functional diversity and specificity of neostriatal interneurons. Curr Opin Neurobio 2004; 14:685–692.CrossRefGoogle Scholar
  21. 21.
    Jaeger D, Kita H, Wilson CJ. Surround inhibition among projection neurons is week or nonexistent in the rat neostriatum. J Neurophysio 1994; 72:2555–2558.Google Scholar
  22. 22.
    Kita H, Kitai ST. Intracellular study of rat globus pallidus neurons: membrane properties and responses to neostriatal, subthalamic and nigral stimulation. Brain Res 1991; 564:296–305.PubMedCrossRefGoogle Scholar
  23. 23.
    Gerfen CR. The neostriatal mosaic: multiple levels of compartmental organization in the basal ganglia. Annu Rev Neurosci 1992; 15:285–320.PubMedCrossRefGoogle Scholar
  24. 24.
    Bevan MD, Booth PA, Eaton SA et al. Selective innervation of neostriatal interneurons by a subclass of neuron in the globus pallidus of the rat. J Neurosci 1998; 18:9438–9452.PubMedGoogle Scholar
  25. 25.
    Smith Y, Bevan MD, Shink E et al. Microcircuitry of the direct and indirect pathways of the basal ganglia. Neuroscience 1998; 86:353–387.PubMedCrossRefGoogle Scholar
  26. 26.
    Frerking M, Petersen CC, Nicoll RA. Mechanisms underlying kainate receptor-mediated disinhibition in the hippocampus. Proc Natl Acad Sci USA 1999; 96:12917–12922.PubMedCrossRefGoogle Scholar
  27. 27.
    Kerchner GA, Wilding TJ, Li P et al. Presynaptic kainate receptors regulate spinal sensory transmission. J Neurosci 2001; 21:59–66.PubMedGoogle Scholar
  28. 28.
    Hettinger BD, Lee A, Linden J et al. Ultrastructural localization of adenosine A2A receptors suggests multiple cellular sites for modulation of GABAergic neurons in rat striatum. J Comp Neurol 2001; 431:331–346.PubMedCrossRefGoogle Scholar
  29. 29.
    Bogenpohl JW, Pare JF, Smith Y. Subcellular localization of adenosine A2a receptors in the striatum and globus pallidus of monkey and rat. Soc Neurosci Abstr 2008; P–P056.Google Scholar
  30. 30.
    Kane-Jackson R, Smith Y Pre-synaptic kainate receptors in GABAergic and Glutamatergic axon terminals in the monkey globus pallidus. Neuroscience 2003; 120:285–289.CrossRefGoogle Scholar
  31. 31.
    Rodríguez-Moreno A, Lerma J. Kainate receptor modulation of GABA release involves a metabotropic function. Neuron 1998; 20:1211–1218.PubMedCrossRefGoogle Scholar
  32. 32.
    Frerking M, Nicoll RA. Synaptic kainate receptors. Curr Opin Neurobiol 2000; 10:342–351.PubMedCrossRefGoogle Scholar
  33. 33.
    Rodríguez-Moreno A, Sihra TS. Metabotropic actions of kainate receptors in the CNS. J Neurochem 2007; 103:2121–2135.PubMedCrossRefGoogle Scholar
  34. 34.
    Rodríguez-Moreno A, Sihra TS. Kainate receptors with a metabotropic modus operandi. Trends Neurosci 2007; 30(12):630–637.PubMedCrossRefGoogle Scholar
  35. 35.
    Nakamura M, Jang IS, Ishibashi H et al. Possible roles of kainate receptors on GABAergic nerve terminals projecting to rat substantia nigra dopaminergic neurons. J Neurophysiol 2003; 90:1662–1670.PubMedCrossRefGoogle Scholar
  36. 36.
    Cunha RA, Malva JO, Ribeiro JA. Pertussis toxin prevents presynaptic inhibition by kainate receptors of rat hippocampal [2H] GABA release. FEBS Letters 2000; 469(2-3):159–162.PubMedCrossRefGoogle Scholar
  37. 37.
    Rodriguez-Moreno A, Lopez-Garcia JC, Lerma J. Two populations of kainate receptors with separate signaling mechanisms in hippocampal interneurons. Proc Natl Acad Sci USA 2000; 97:1293–1298.PubMedCrossRefGoogle Scholar
  38. 38.
    Melyan Z, Wheal HV, Lancaster B. Metabotropic-mediated kainate receptor regulation of IsAHP and excitability in pyramidal cells. Neuron 2002; 34(1):107–114.PubMedCrossRefGoogle Scholar
  39. 39.
    Melyan Z, Lancaster B, Wheal HV. Metabotropic regulation of intrinsic excitability by synaptic activation of kainate receptors. J Neurosci 2004; 24:4530–4534.PubMedCrossRefGoogle Scholar
  40. 40.
    Lauri SE, Segerstrale M, Vesikansa A et al. Endogenous activation of kainate receptors regulates glutamate release and network activity in the developing hippocampus. J Neurosci 2005; 25:4473–4484.PubMedCrossRefGoogle Scholar
  41. 41.
    Petralia RS, Wang YX, Wenthold RJ. Histological and ultrastructural localization of the kainat receptor subunits, KA2 and GluR6/7, in the rat nervous system using selective antipeptide antibodies. J Comp Neurol 1994; 349:85–110.PubMedCrossRefGoogle Scholar
  42. 42.
    Rodriguez-Moreno A, Herreras O, Lerma J. Kainate receptors presynaptic ally downregulate GABAergic inhibition in the rat hippocampus. Neuron 1997; 19:893–901.PubMedCrossRefGoogle Scholar
  43. 43.
    Maingret F, Lauri SE, Taira T et al. Profound regulation of neonatal CA1 rat hippocampal GABAergic transmission by functionally distinct kainate receptor populations. J Physiol 2005; 567:131–142.PubMedCrossRefGoogle Scholar
  44. 44.
    Semyanov A, Kullmann DM. Kainate receptor-dependent axonal depolarization and action potential initiation in interneurons. Nature Neurosci 2001; 4:718–723.PubMedCrossRefGoogle Scholar
  45. 45.
    Kang N, Jiang L, He W et al. Presynaptic inactivation of action potentials and postsynaptic inhibition of GABAA currents contribute to KA-induced disinhibition in CA1 pyramidal neurons. J Neurophysiol 2004; 92:873–882.PubMedCrossRefGoogle Scholar

Copyright information

© Landes Bioscience and Springer Science+Business Media, LLC 2011

Authors and Affiliations

  1. 1.Division of Neuroscience, Yerkes National Primate Research Center and Department of NeurologyEmory UniversityAtlantaUSA

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