Journal of Neurophysiology, Vol 76, Issue 3 1545-1558, Copyright © 1996 by APS

ARTICLES

Suppression of K+ conductance by metabotropic glutamate receptor in acutely dissociated large cholinergic neurons of rat caudate putamen

Y. Takeshita, N. Harata and N. Akaike
Department of Physiology, Kyushu University Faculty of Medicine, Fukuoka, Japan.

1. Responses to metabotropic glutamate receptor (mGluR) activation were investigated in acutely dissociated rat neostriatal (caudate putamen, CP) large cholinergic neurons, with the use of a nystatin-perforated patch-clamp technique. 2. Application of L-glutamate (Glu) in the presence of 6-cyano-7-nitroquinoxaline-2,3-dione (CNQX) induced a slow inward current accompanied by a decrease in membrane conductance at a holding potential (VH) of -44 mV. 3. The ratio of the maximal amplitude of the slow inward metabotropic glutamate (mGlu) response to that of the ionotropic glutamate response for large cholinergic CP neurons was larger than that for the hoppocampal CA1, CA3, and dentate gyrus neurons the nucleus tractus solitarii neuron, cerebellar Purkinje neuron, and granule cell of the main olfactory bulb. The threshold and half-maximal effective concentration values of these mGlu responses were 10- to 30-fold lower than those of the respective ionotropic responses. 4. Specific agonists of the mGluR, quisqualate (QA), (+/-)-1-aminocyclopentane-trans-1,3-dicarboxylic acid (tACPD), (1S,3R)-1-aminocyclopentane-1,3-dicarboxylic acid [(1S,3R)-ACPD], and (2S,3S,4S)-alpha-carboxycyclopropyl-glycine [L-CCG-1), similarly induced slow inward currents at the same VH. The relative affinities of the mGlu agonists were QA > Glu > L-CCG-1 > (1S,3R)-ACPD. L-CCG-1 did not induce any current at concentrations < 10(-6) M. 5. DL-2-amino-3-phosphonopropionic acid or DL-2-amino-4-phosphonobutyric acid did not block the mGlu response, whereas (RS)-alpha-methyl-4-carboxyphenyl-glycine, a selective mGluR antagonist, partially reduced the mGlu response. 6. The reversal potential of the mGlu response was close to the K+ equilibrium potential, and it shifted by 56.4 mV for a 10-fold change in extracellular K+ concentration. In 90.6% of the neurons tested, the instantaneous current induced by hyperpolarizing voltage steps was markedly suppressed during the mGlu response. In 9.4% of the neurons, the currents elicited by step pulses showed a voltage-dependent slow relaxation that was not affected by mGluR activation. 7. Under the current-clamp mode, the slow afterhyperpolarization (AHP) following a spontaneous discharge was not affected by tACPD. The AHP current was not blocked under the voltage-clamp mode, either. 8. (1S,3R)-ACPD or Glu in the presence of CNQX elicited membrane depolarization accompanied by increased rate of action potentials under the current-clamp mode. Tetrodotoxin had no effect on the membrane depolarization. 9. These results indicate that the mGluR on large cholinergic CP neurons is mainly of the mGluR1 and/or mGluR5 type, and it plays a significant role in controlling the membrane potential by way of suppressing the leak K+ conductance.

This article has been cited by other articles:

				P. Deng, Z.-P. Pang, Z. Lei, and Z. C. Xu Excitatory Roles of Protein Kinase C in Striatal Cholinergic Interneurons J Neurophysiol, October 1, 2009; 102(4): 2453 - 2461. [Abstract] [Full Text] [PDF]

				F. Ferraguti, L. Crepaldi, and F. Nicoletti Metabotropic Glutamate 1 Receptor: Current Concepts and Perspectives Pharmacol. Rev., December 1, 2008; 60(4): 536 - 581. [Abstract] [Full Text] [PDF]

				C. M. Root, N. A. Velazquez-Ulloa, G. C. Monsalve, E. Minakova, and N. C. Spitzer Embryonically Expressed GABA and Glutamate Drive Electrical Activity Regulating Neurotransmitter Specification J. Neurosci., April 30, 2008; 28(18): 4777 - 4784. [Abstract] [Full Text] [PDF]

				A. P. Berg, N. Sen, and D. A. Bayliss TrpC3/C7 and Slo2.1 Are Molecular Targets for Metabotropic Glutamate Receptor Signaling in Rat Striatal Cholinergic Interneurons J. Neurosci., August 15, 2007; 27(33): 8845 - 8856. [Abstract] [Full Text] [PDF]

				T. Heinbockel, K. A. Hamilton, and M. Ennis Group I Metabotropic Glutamate Receptors Are Differentially Expressed by Two Populations of Olfactory Bulb Granule Cells J Neurophysiol, April 1, 2007; 97(4): 3136 - 3141. [Abstract] [Full Text] [PDF]

				A. P. Berg and D. A. Bayliss Striatal Cholinergic Interneurons Express a Receptor-Insensitive Homomeric TASK-3-Like Background K+ Current J Neurophysiol, February 1, 2007; 97(2): 1546 - 1552. [Abstract] [Full Text] [PDF]

				K. Kaneda, T. Kita, and H. Kita Repetitive Activation of Glutamatergic Inputs Evokes a Long-Lasting Excitation in Rat Globus Pallidus Neurons In Vitro J Neurophysiol, January 1, 2007; 97(1): 121 - 133. [Abstract] [Full Text] [PDF]

				T. Heinbockel, N. Laaris, and M. Ennis Metabotropic Glutamate Receptors in the Main Olfactory Bulb Drive Granule Cell-Mediated Inhibition J Neurophysiol, January 1, 2007; 97(1): 858 - 870. [Abstract] [Full Text] [PDF]

				H. Zhang and D. Sulzer Glutamate Spillover in the Striatum Depresses Dopaminergic Transmission by Activating Group I Metabotropic Glutamate Receptors J. Neurosci., November 19, 2003; 23(33): 10585 - 10592. [Abstract] [Full Text] [PDF]

				A. Inanobe, A. Fujita, M. Ito, H. Tomoike, K. Inageda, and Y. Kurachi Inward rectifier K+ channel Kir2.3 is localized at the postsynaptic membrane of excitatory synapses Am J Physiol Cell Physiol, June 1, 2002; 282(6): C1396 - C1403. [Abstract] [Full Text] [PDF]

				D. Centonze, A. Pisani, P. Bonsi, P. Giacomini, G. Bernardi, and P. Calabresi Stimulation of Nitric Oxide-cGMP Pathway Excites Striatal Cholinergic Interneurons via Protein Kinase G Activation J. Neurosci., February 15, 2001; 21(4): 1393 - 1400. [Abstract] [Full Text] [PDF]

				G. Martin, Z. Nie, and G. R. Siggins Metabotropic Glutamate Receptors Regulate N-Methyl-D-Aspartate-Mediated Synaptic Transmission in Nucleus Accumbens J Neurophysiol, December 1, 1997; 78(6): 3028 - 3038. [Abstract] [Full Text] [PDF]

				F.-M. Zhou and J. J. Hablitz Metabotropic Glutamate Receptor Enhancement of Spontaneous IPSCs in Neocortical Interneurons J Neurophysiol, November 1, 1997; 78(5): 2287 - 2295. [Abstract] [Full Text] [PDF]

				J. A. F. Kearney, K. A. Frey, and R. L. Albin Metabotropic Glutamate Agonist-Induced Rotation: A Pharmacological, FOS Immunohistochemical, and [14C]-2-Deoxyglucose Autoradiographic Study J. Neurosci., June 1, 1997; 17(11): 4415 - 4425. [Abstract] [Full Text] [PDF]