QUICK SEARCH:   [advanced] Author: Keyword(s): Year:  Vol:  Page:

HOME  |   SEARCH  |   ARCHIVE  |   SUBSCRIBE  |   CONTACT  |   HELP

This Article Full Text Full Text (PDF) Submit an eLetter Alert me when this article is cited Alert me when eLetters are posted Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in Web of Science Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via Web of Science (59) Citing Articles via Google Scholar Google Scholar Articles by Svoboda, K. R. Articles by Lupica, C. R. Search for Related Content PubMed PubMed Citation Articles by Svoboda, K. R. Articles by Lupica, C. R.

 Previous Article  |  Next Article 

The Journal of Neuroscience, September 15, 1998, 18(18):7084-7098

Opioid Inhibition of Hippocampal Interneurons via Modulation of Potassium and Hyperpolarization-Activated Cation (I_h) Currents

Kurt R. Svoboda¹ and Carl R. Lupica^{1, 2}

¹ Department of Pharmacology and ² Program in Neuroscience, University of Colorado Health Sciences Center, Denver, Colorado 80262

The actions of mu- and delta-opioid agonists (DAMGO and DPDPE, respectively) on GABAergic interneurons in stratum oriens of area CA1 of the hippocampus were examined by using whole-cell voltage-clamp recordings in brain slices. Both agonists consistently generated outward currents of similar magnitude (15-20 pA) in the majority of cells. However, under control conditions, current-voltage (I/V) relationships revealed that only a small number of these cells (3 of 77) demonstrated clear increases in membrane conductance, associated with the activation of the potassium current known as G_irk. These interneurons also exhibited a slowly activating, inwardly rectifying current known as I_h on hyperpolarizing step commands. I_h was blocked by the extracellular application of cesium (3-9 mM) or ZD 7288 (10-100 µM) but was insensitive to barium (1-2 mM). In an effort to determine whether the holding current changes were attributable to the modulation of G_irk and/or I_h, we used known blockers of these ion channels (barium or cesium and ZD 7288, respectively). Extracellular application of cesium (3-9 mM) or ZD 7288 (25-100 µM) blocked I_h and significantly reduced the opioid-induced outward currents by 58%. Under these conditions the opioid agonists activated a potassium current with characteristics similar to G_irk. Similarly, during barium (1-2 mM) application the opioid-induced outward currents were reduced by 46%, and a clear reduction in I_h and the whole-cell conductance was revealed. These data suggest that the opioids can modulate both I_h and G_irk in the same population of stratum oriens interneurons and that the modulation of these ion channels can contribute to the inhibition of interneuron activity in the hippocampus.

Key words: delta-receptor; electrophysiology; enkephalin; GABA; hippocampus; opioid receptor; mu-receptor; nonselective cation current; oriens/alveus interneurons; queer current

---

Copyright © 1998 Society for Neuroscience  0270-6474/98/18187084-15$05.00/0

This article has been cited by other articles:

				L. J. Voss, J. W. Sleigh, J. P. M. Barnard, and H. E. Kirsch The Howling Cortex: Seizures and General Anesthetic Drugs Anesth. Analg., November 1, 2008; 107(5): 1689 - 1703. [Abstract] [Full Text] [PDF]

				M. Koehl, P. Meerlo, D. Gonzales, A. Rontal, F. W. Turek, and D. N. Abrous Exercise-induced promotion of hippocampal cell proliferation requires {beta}-endorphin FASEB J, July 1, 2008; 22(7): 2253 - 2262. [Abstract] [Full Text] [PDF]

				E. Calixto, E. J. Galvan, J. P. Card, and G. Barrionuevo Coincidence detection of convergent perforant path and mossy fibre inputs by CA3 interneurons J. Physiol., June 1, 2008; 586(11): 2695 - 2712. [Abstract] [Full Text] [PDF]

				W. J. Meilandt, G.-Q. Yu, J. Chin, E. D. Roberson, J. J. Palop, T. Wu, K. Scearce-Levie, and L. Mucke Enkephalin Elevations Contribute to Neuronal and Behavioral Impairments in a Transgenic Mouse Model of Alzheimer's Disease J. Neurosci., May 7, 2008; 28(19): 5007 - 5017. [Abstract] [Full Text] [PDF]

				L. L. Glickfeld, B. V. Atallah, and M. Scanziani Complementary Modulation of Somatic Inhibition by Opioids and Cannabinoids J. Neurosci., February 20, 2008; 28(8): 1824 - 1832. [Abstract] [Full Text] [PDF]

				S. Loacker, M. Sayyah, W. Wittmann, H. Herzog, and C. Schwarzer Endogenous dynorphin in epileptogenesis and epilepsy: anticonvulsant net effect via kappa opioid receptors Brain, April 1, 2007; 130(4): 1017 - 1028. [Abstract] [Full Text] [PDF]

				A. R. McQuiston Effects of {micro}-Opioid Receptor Modulation on GABAB Receptor Synaptic Function in Hippocampal CA1 J Neurophysiol, March 1, 2007; 97(3): 2301 - 2311. [Abstract] [Full Text] [PDF]

				Y. Li and A. N. van den Pol Differential Target-Dependent Actions of Coexpressed Inhibitory Dynorphin and Excitatory Hypocretin/Orexin Neuropeptides J. Neurosci., December 13, 2006; 26(50): 13037 - 13047. [Abstract] [Full Text] [PDF]

				S. G. A. Frere and A. Luthi Pacemaker channels in mouse thalamocortical neurones are regulated by distinct pathways of cAMP synthesis J. Physiol., January 1, 2004; 554(1): 111 - 125. [Abstract] [Full Text] [PDF]

				A. R. McQuiston and P. Saggau Mu-opioid Receptors Facilitate the Propagation of Excitatory Activity in Rat Hippocampal Area CA1 by Disinhibition of all Anatomical Layers J Neurophysiol, September 1, 2003; 90(3): 1936 - 1948. [Abstract] [Full Text] [PDF]

				Z. Z Pan {kappa}-Opioid receptor-mediated enhancement of the hyperpolarization-activated current (Ih) through mobilization of intracellular calcium in rat nucleus raphe magnus J. Physiol., May 1, 2003; 548(3): 765 - 775. [Abstract] [Full Text] [PDF]

				Q.-Q. Sun, D. A. Prince, and J. R. Huguenard Vasoactive Intestinal Polypeptide and Pituitary Adenylate Cyclase-Activating Polypeptide Activate Hyperpolarization-Activated Cationic Current and Depolarize Thalamocortical Neurons In Vitro J. Neurosci., April 1, 2003; 23(7): 2751 - 2758. [Abstract] [Full Text] [PDF]

				J. M. Harrison, R. G. Allen, M. J. Pellegrino, J. T. Williams, and O. J. Manzoni Chronic Morphine Treatment Alters Endogenous Opioid Control of Hippocampal Mossy Fiber Synaptic Transmission J Neurophysiol, May 1, 2002; 87(5): 2464 - 2470. [Abstract] [Full Text] [PDF]

				X. Chen, H. G. Marrero, and J. E. Freedman Opioid Receptor Modulation of a Metabolically Sensitive Ion Channel in Rat Amygdala Neurons J. Neurosci., December 1, 2001; 21(23): 9092 - 9100. [Abstract] [Full Text] [PDF]

				K. S. Warren, K. Baker, and M. C. Fishman The slow mo mutation reduces pacemaker current and heart rate in adult zebrafish Am J Physiol Heart Circ Physiol, October 1, 2001; 281(4): H1711 - H1719. [Abstract] [Full Text] [PDF]

				J. T. Williams, M. J. Christie, and O. Manzoni Cellular and Synaptic Adaptations Mediating Opioid Dependence Physiol Rev, January 1, 2001; 81(1): 299 - 343. [Abstract] [Full Text] [PDF]

				X. Chen, H. G. Marrero, R. Murphy, Y.-J. Lin, and J. E. Freedman Altered gating of opiate receptor-modulated K+ channels on amygdala neurons of morphine-dependent rats PNAS, December 19, 2000; 97(26): 14692 - 14696. [Abstract] [Full Text] [PDF]

				A. P Southan, N. P Morris, G. J Stephens, and B. Robertson Hyperpolarization-activated currents in presynaptic terminals of mouse cerebellar basket cells J. Physiol., July 1, 2000; 526(1): 91 - 97. [Abstract] [Full Text] [PDF]

				Q.-S. Liu, S. Han, Y.-S. Jia, and G. Ju Selective Modulation of Excitatory Transmission by {micro}-Opioid Receptor Activation in Rat Supraoptic Neurons J Neurophysiol, December 1, 1999; 82(6): 3000 - 3005. [Abstract] [Full Text] [PDF]

				P. Jensen, D. J. Surmeier, and D. Goldowitz Rescue of Cerebellar Granule Cells from Death in weaver NR1 Double Mutants J. Neurosci., September 15, 1999; 19(18): 7991 - 7998. [Abstract] [Full Text] [PDF]

				P. J Emmerson and R. J Miller Pre- and postsynaptic actions of opioid and orphan opioid agonists in the rat arcuate nucleus and ventromedial hypothalamus in vitro J. Physiol., June 1, 1999; 517(2): 431 - 445. [Abstract] [Full Text] [PDF]

				K. R. Svoboda, C. E. Adams, and C. R. Lupica Opioid Receptor Subtype Expression Defines Morphologically Distinct Classes of Hippocampal Interneurons J. Neurosci., January 1, 1999; 19(1): 85 - 95. [Abstract] [Full Text] [PDF]

Home  |   Search  |   Archive  |   Subscribe  |   Contact  |   Help