Effects of μ-opioid receptor modulation on GABAB receptor synaptic function in hippocampal CA1

Journal of Neurophysiology

Volumn 97, Issue 3, 2007, Pages 2301-2311

  McQuiston, A Rory ^a,b  

^a VIRGINIA COMMONWEALTH UNIVERSITY MEDICAL CENTER   (United States)

^b VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; BICUCULLINE; DEXTRO PHENYLALANYLCYSTEINYLTYROSYL DEXTRO TRYPTOPHYLORNITHYLTHREONYLPENICILLAMINYLTHREONINAMIDE 2,7 DISULFIDE; ENKEPHALIN[2 DEXTRO ALANINE 4 METHYLPHENYLALANINE 5 GLYCINE]; MU OPIATE RECEPTOR;

ANIMAL TISSUE; ARTICLE; BRAIN FUNCTION; BRAIN REGION; CONTROLLED STUDY; HIPPOCAMPUS; IMAGING SYSTEM; MALE; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; RAT; SYNAPTIC TRANSMISSION;

ANALGESICS, OPIOID; ANIMALS; BICUCULLINE; DOSE-RESPONSE RELATIONSHIP, RADIATION; DRUG INTERACTIONS; ELECTRIC STIMULATION; ENKEPHALIN, ALA(2)-MEPHE(4)-GLY(5)-; EXCITATORY POSTSYNAPTIC POTENTIALS; GABA ANTAGONISTS; HIPPOCAMPUS; MALE; NEURONS; PATCH-CLAMP TECHNIQUES; PHOSPHINIC ACIDS; PROPANOLAMINES; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, GABA-B; RECEPTORS, OPIOID, MU; SYNAPSES;

EID: 33947174136     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.01179.2006     Document Type: Article

References (49)

1. Ang CW, Carlson GC, Coulter DA. Hippocampal CA1 circuitry dynamically gates direct cortical inputs preferentially at theta frequencies. J Neurosci 25: 9567-9580, 2005.
2. Arvidsson U, Riedl M, Chakrabarti S, Lee JH, Nakano AH, Dado RJ, Loh HH, Law PY, Wessendorf MW, Elde R. Distribution and targeting of a mu-opioid receptor (MOR1) in brain and spinal cord. J Neurosci 15: 3328-3341, 1995.
3. Atweh SF, Kuhar MJ. Autoradiographic localization of opiate receptors in rat brain. III. The telencephalon. Brain Res 134: 393-405, 1977.
4. Bausch SB, Patterson TA, Ehrengruber MU, Lester HA, Davidson N, Chavkin C. Colocalization of mu opioid receptors with GIRK1 potassium channels in the rat brain: an immunocytochemical study. Receptors Channels 3: 221-241, 1995.
5. Buzsáki G. Theta oscillations in the hippocampus. Neuron 33: 325-340, 2002.
6. Capogna M, Gahwiler BH, Thompson SM. Mechanism of mu-opioid receptor-mediated presynaptic inhibition in the rat hippocampus in vitro. J Physiol 470: 539-558, 1993.
7. Cohen GA, Doze VA, Madison DV. Opioid inhibition of GABA release from presynaptic terminals of rat hippocampal interneurons. Neuron 9: 325-335, 1992.
8. Crain BJ, Chang KJ, McNamara JO. Quantitative autoradiographic analysis of mu and delta opioid binding sites in the rat hippocampal formation. J Comp Neurol 246: 170-180, 1986.
9. Ding YQ, Kaneko T, Nomura S, Mizuno N. Immunohistochemical localization of mu-opioid receptors in the central nervous system of the rat. J Comp Neurol 367: 375-402, 1996.
10. Drake CT, Milner TA. Mu opioid receptors are in somatodendritic and axonal compartments of GABAergic neurons in rat hippocampal formation. Brain Res 849: 203-215, 1999.
11. Drake CT, Milner TA. Mu opioid receptors are in discrete hippocampal interneuron subpopulations. Hippocampus 12: 119-136, 2002.
12. Dvorak-Carbone H, Schuman EM. Patterned activity in stratum lacunosum moleculare inhibits CA1 pyramidal neuron firing. J Neurophysiol 82: 3213-3222, 1999.
13. Faulkner HJ, Traub RD, Whittington MA. Disruption of synchronous gamma oscillations in the rat hippocampal slice: a common mechanism of anaesthetic drug action. Br J Pharmacol 125: 483-492, 1998.
14. Faulkner HJ, Traub RD, Whittington MA. Anaesthetic/amnesic agents disrupt beta frequency oscillations associated with potentiation of excitatory synaptic potentials in the rat hippocampal slice. Br J Pharmacol 128: 1813-1825, 1999.
15. Gupta A, Wang Y, Markram H. Organizing principles for a diversity of GABAergic interneurons and synapses in the neocortex. Science 287: 273-278, 2000.
16. Herkenham M, Pert CB. In vitro autoradiography of opiate receptors in rat brain suggests loci of "opiatergic" pathways. Proc Natl Acad Sci USA 77: 5532-5536, 1980.
17. Jarsky T, Roxin A, Kath WL, Spruston N. Conditional dendritic spike propagation following distal synaptic activation of hippocampal CA1 pyramidal neurons. Nat Neurosci 8: 1667-1676, 2005.
18. Jin W, Zhang RJ, Wu JY. Voltage-sensitive dye imaging of population neuronal activity in cortical tissue. J Neurosci Methods 115: 13-27, 2002.
19. Kalyuzhny AE, Wessendorf MW. CNS GABA neurons express the muopioid receptor: immunocytochemical studies. Neuroreport 8: 3367-3372, 1997.
20. Larkum ME, Zhu JJ, Sakmann B. A new cellular mechanism for coupling inputs arriving at different cortical layers. Nature 398: 338-341, 1999.
21. Lupica CR. Delta and mu enkephalins inhibit spontaneous GABA-mediated IPSCs via a cyclic AMP-independent mechanism in the rat hippocampus. J Neurosci 15: 737-749, 1995.
22. Lupica CR, Dunwiddie TV. Differential effects of mu- and delta-receptor selective opioid agonists on feedforward and feedback GABAergic inhibition in hippocampal brain slices. Synapse 8: 237-248, 1991.
23. Lupica CR, Proctor WR, Dunwiddie TV. Dissociation of mu and delta opioid receptor-mediated reductions in evoked and spontaneous synaptic inhibition in the rat hippocampus in vitro. Brain Res 593: 226-238, 1992.
24. Madison DV, Nicoll RA. Enkephalin hyperpolarizes interneurones in the rat hippocampus. J Physiol 398: 123-130, 1988.
25. Magee JC, Johnston D. A synaptically controlled, associative signal for Hebbian plasticity in hippocampal neurons. Science 275: 209-213, 1997.
26. Mansour A, Fox CA, Burke S, Akil H, Watson SJ. Immunohistochemical localization of the cloned mu opioid receptor in the rat CNS. J Chem Neuroanat 8: 283-305, 1995.
27. Mansour A, Fox CA, Thompson RC, Akil H, Watson SJ. mu-Opioid receptor mRNA expression in the rat CNS: comparison to mu-receptor binding. Brain Res 643: 245-265, 1994.
28. Mansour A, Khachaturian H, Lewis ME, Akil H, Watson SJ. Autoradiographic differentiation of mu, delta, and kappa opioid receptors in the rat forebrain and midbrain. J Neurosci 7: 2445-2464, 1987.
29. Mansouri FA, Motamedi F, Fathollahi Y. Chronic in vivo morphine administration facilitates primed-bursts-induced long-term potentiation of Schaffer collateral-CA1 synapses in hippocampal slices in vitro. Brain Res 815: 419-423, 1999.
30. Mansouri FA, Motamedi F, Fathollahi Y, Atapour N, Semnanian S. Augmentation of LTP induced by primed-bursts tetanic stimulation in hippocampal CA1 area of morphine dependent rats. Brain Res 769: 119-124, 1997.
31. Markram H, Wang Y, Tsodyks M. Differential signaling via the same axon of neocortical pyramidal neurons. Proc Natl Acad Sci USA 95: 5323-5328, 1998.
32. Masukawa LM, Prince DA. Enkephalin inhibition of inhibitory input to CA1 and CA3 pyramidal neurons in the hippocampus. Brain Res 249: 271-280, 1982.
33. McLean S, Rothman RB, Jacobson AE, Rice KC, Herkenham M. Distribution of opiate receptor subtypes and enkephalin and dynorphin immunoreactivity in the hippocampus of squirrel, guinea pig, rat, and hamster. J Comp Neurol 255: 497-510, 1987.
34. McQuiston AR, Saggau P. Mu-opioid receptors facilitate the propagation of excitatory activity in rat hippocampal area CA1 by disinhibition of all anatomical layers. J Neurophysiol 90: 1936-1948, 2003.
35. Miles R, Toth K, Gulyas AI, Hajos N, Freund TF. Differences between somatic and dendritic inhibition in the hippocampus. Neuron 16: 815-823, 1996.
36. Nicoll RA, Alger BE, Jahr CE. Enkephalin blocks inhibitory pathways in the vertebrate CNS. Nature 287: 22-25, 1980.
37. Pourmotabbed A, Motamedi F, Fathollahi Y, Mansouri FA, Semnanian S. Involvement of NMDA receptors and voltage-dependent calcium channels on augmentation of long-term potentiation in hippocampal CA1 area of morphine dependent rats. Brain Res 804: 125-134, 1998.
38. Pu L, Bao GB, Xu NJ, Ma L, Pei G. Hippocampal long-term potentiation is reduced by chronic opiate treatment and can be restored by re-exposure to opiates. J Neurosci 22: 1914-1921, 2002.
39. Rekling JC. Effects of met-enkephalin on GABAergic spontaneous miniature IPSPs in organotypic slice cultures of the rat hippocampus. J Neurosci 13: 1954-1964, 1993.
40. Remondes M, Schuman EM. Direct cortical input modulates plasticity and spiking in CA1 pyramidal neurons. Nature 416: 736-740, 2002.
41. Reyes A, Lujan R, Rozov A, Burnashev N, Somogyi P, Sakmann B. Target-cell-specific facilitation and depression in neocortical circuits. Nat Neurosci 1: 279-285, 1998.
42. Svoboda KR, Adams CE, Lupica CR. Opioid receptor subtype expression defines morphologically distinct classes of hippocampal interneurons. J Neurosci 19: 85-95, 1999.
43. Svoboda KR, Lupica CR. Opioid inhibition of hippocampal interneurons via modulation of potassium and hyperpolarization-activated cation (Ih) currents. J Neurosci 18: 7084-7098, 1998.
44. Swearengen E, Chavkin C. Comparison of opioid and GABA receptor control of excitability and membrane conductance in hippocampal CA1 pyramidal cells in rat. Neuropharmacology 28: 689-697, 1989.
45. Thomson AM. Activity-dependent properties of synaptic transmission at two classes of connections made by rat neocortical pyramidal axons in vitro. J Physiol 502: 131-147, 1997.
46. Wagner JJ, Etemad LR, Thompson AM. Opioid-mediated facilitation of long-term depression in rat hippocampus. J Pharmacol Exp Ther 296: 776-781, 2001.
47. Whittington MA, Traub RD, Faulkner HJ, Jefferys JG, Chettiar K. Morphine disrupts long-range synchrony of gamma oscillations in hippocampal slices. Proc Natl Acad Sci USA 95: 5807-5811, 1998.
48. Wimpey TL, Caudle RM, Chavkin C. Chronic morphine exposure blocks opioid effects on both the early and late inhibitory postsynaptic potentials in hippocampal CA1 pyramidal cells. Neurosci Lett 110: 349-355, 1990.
49. Wimpey TL, Chavkin C. Opioids activate both an inward rectifier and a novel voltage-gated potassium conductance in the hippocampal formation. Neuron 6: 281-289, 1991.