Layer selective presynaptic modulation of excitatory inputs to hippocampal cornu Ammon 1 by μ-opioid receptor activation

Neuroscience

Volumn 151, Issue 1, 2008, Pages 209-221

  McQuiston, A R ^a  

^a VIRGINIA COMMONWEALTH UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

caged GABA; interneuron; photolysis; synaptic inhibition; voltage sensitive dye imaging

Indexed keywords

4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID A RECEPTOR BLOCKING AGENT; 4 AMINOBUTYRIC ACID B RECEPTOR BLOCKING AGENT; 4 AMINOBUTYRIC ACID RECEPTOR; ALPHA CARBOXY 2 NITROBENZYL ESTER; BENZYL DERIVATIVE; CARBOXYL GROUP; DYE; ENKEPHALIN[2 DEXTRO ALANINE 4 METHYLPHENYLALANINE 5 GLYCINE]; MU OPIATE RECEPTOR; OPIATE AGONIST; OPIATE RECEPTOR; TRIFLUOROACETIC ACID; UNCLASSIFIED DRUG; VOLTAGE SENSITIVE DYE;

4 AMINOBUTYRIC ACID RELEASE; ANATOMY; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ELECTROPHYSIOLOGY; EXCITATORY POSTSYNAPTIC POTENTIAL; HIPPOCAMPUS; HIPPOCAMPUS PYRAMIDAL CELL LAYER; HYPERPOLARIZATION; IMAGING; INTERNEURON; MALE; NEUROMODULATION; NONHUMAN; PATCH CLAMP; PHOTOLYSIS; POSTSYNAPTIC POTENTIAL; PRESYNAPTIC NERVE; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; STRATUM LACUNOSUM MOLECULARE; STRATUM ORIENS; STRATUM PYRAMIDALE; SYNAPTIC POTENTIAL; SYNAPTIC TRANSMISSION;

ANALGESICS, OPIOID; ANIMALS; COLORING AGENTS; DATA INTERPRETATION, STATISTICAL; ELECTROPHYSIOLOGY; ENKEPHALIN, ALA(2)-MEPHE(4)-GLY(5)-; EXCITATORY POSTSYNAPTIC POTENTIALS; HIPPOCAMPUS; IMAGE PROCESSING, COMPUTER-ASSISTED; MALE; PHOTOLYSIS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, GABA; RECEPTORS, OPIOID, MU; RECEPTORS, PRESYNAPTIC; SARCOPLASMIC RETICULUM;

EID: 37849004075     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2007.09.077     Document Type: Article

References (57)

1. Ang C.W., Carlson G.C., and Coulter D.A. Hippocampal CA1 circuitry dynamically gates direct cortical inputs preferentially at theta frequencies. J Neurosci 25 (2005) 9567-9580
2. Arvidsson U., Riedl M., Chakrabarti S., Lee J.H., Nakano A.H., Dado R.J., Loh H.H., Law P.Y., Wessendorf M.W., and Elde R. Distribution and targeting of a mu-opioid receptor (MOR1) in brain and spinal cord. J Neurosci 15 (1995) 3328-3341
3. Atweh S.F., and Kuhar M.J. Autoradiographic localization of opiate receptors in rat brain. III. The telencephalon. Brain Res 134 (1977) 393-405
4. Bausch S.B., Patterson T.A., Ehrengruber M.U., Lester H.A., Davidson N., and Chavkin C. Colocalization of mu opioid receptors with GIRK1 potassium channels in the rat brain: an immunocytochemical study. Receptors Channels 3 (1995) 221-241
5. Capogna M., Gahwiler B.H., and Thompson S.M. Mechanism of mu-opioid receptor-mediated presynaptic inhibition in the rat hippocampus in vitro. J Physiol 470 (1993) 539-558
6. Capogna M., Gahwiler B.H., and Thompson S.M. Presynaptic inhibition of calcium-dependent and -independent release elicited with ionomycin, gadolinium, and alpha-latrotoxin in the hippocampus. J Neurophysiol 75 (1996) 2017-2028
7. Cohen G.A., Doze V.A., and Madison D.V. Opioid inhibition of GABA release from presynaptic terminals of rat hippocampal interneurons. Neuron 9 (1992) 325-335
8. Corrigall W.A., and Linseman M.A. Conditioned place preference produced by intra-hippocampal morphine. Pharmacol Biochem Behav 30 (1988) 787-789
9. Crain B.J., Chang K.J., and McNamara J.O. Quantitative autoradiographic analysis of mu and delta opioid binding sites in the rat hippocampal formation. J Comp Neurol 246 (1986) 170-180
10. Ding Y.Q., Kaneko T., Nomura S., and Mizuno N. Immunohistochemical localization of mu-opioid receptors in the central nervous system of the rat. J Comp Neurol 367 (1996) 375-402
11. Drake C.T., and Milner T.A. Mu opioid receptors are in somatodendritic and axonal compartments of GABAergic neurons in rat hippocampal formation. Brain Res 849 (1999) 203-215
12. Drake C.T., and Milner T.A. Mu opioid receptors are in discrete hippocampal interneuron subpopulations. Hippocampus 12 (2002) 119-136
13. Dvorak-Carbone H., and Schuman E.M. Patterned activity in stratum lacunosum moleculare inhibits CA1 pyramidal neuron firing. J Neurophysiol 82 (1999) 3213-3222
14. Faulkner H.J., Traub R.D., and Whittington M.A. Disruption of synchronous gamma oscillations in the rat hippocampal slice: a common mechanism of anaesthetic drug action. Br J Pharmacol 125 (1998) 483-492
15. Faulkner H.J., Traub R.D., and Whittington M.A. Anaesthetic/amnesic agents disrupt beta frequency oscillations associated with potentiation of excitatory synaptic potentials in the rat hippocampal slice. Br J Pharmacol 128 (1999) 1813-1825
16. Freund T.F., and Buzsaki G. Interneurons of the hippocampus. Hippocampus 6 (1996) 347-470
17. Gupta A., Wang Y., and Markram H. Organizing principles for a diversity of GABAergic interneurons and synapses in the neocortex. Science 287 (2000) 273-278
18. Herkenham M., and Pert C.B. In vitro autoradiography of opiate receptors in rat brain suggests loci of "opiatergic" pathways. Proc Natl Acad Sci U S A 77 (1980) 5532-5536
19. Jin W., Zhang R.J., and Wu J.Y. Voltage-sensitive dye imaging of population neuronal activity in cortical tissue. J Neurosci Methods 115 (2002) 13-27
20. Kalyuzhny A.E., and Wessendorf M.W. CNS GABA neurons express the mu-opioid receptor: immunocytochemical studies. Neuroreport 8 (1997) 3367-3372
21. Khazipov R., Congar P., and Ben-Ari Y. Hippocampal CA1 lacunosum-moleculare interneurons: modulation of monosynaptic GABAergic IPSCs by presynaptic GABAB receptors. J Neurophysiol 74 (1995) 2126-2137
22. Kreek M.J. Drug addictions. Molecular and cellular endpoints. Ann N Y Acad Sci 937 (2001) 27-49
23. Larkum M.E., Zhu J.J., and Sakmann B. A new cellular mechanism for coupling inputs arriving at different cortical layers. Nature 398 (1999) 338-341
24. Lupica C.R. Delta and mu enkephalins inhibit spontaneous GABA-mediated IPSCs via a cyclic AMP-independent mechanism in the rat hippocampus. J Neurosci 15 (1995) 737-749
25. Lupica C.R., and Dunwiddie T.V. Differential effects of mu- and delta-receptor selective opioid agonists on feedforward and feedback GABAergic inhibition in hippocampal brain slices. Synapse 8 (1991) 237-248
26. Lupica C.R., Proctor W.R., and Dunwiddie T.V. Dissociation of mu and delta opioid receptor-mediated reductions in evoked and spontaneous synaptic inhibition in the rat hippocampus in vitro. Brain Res 593 (1992) 226-238
27. Madison D.V., and Nicoll R.A. Enkephalin hyperpolarizes interneurones in the rat hippocampus. J Physiol 398 (1988) 123-130
28. Mansour A., Fox C.A., Burke S., Akil H., and Watson S.J. Immunohistochemical localization of the cloned mu opioid receptor in the rat CNS. J Chem Neuroanat 8 (1995) 283-305
29. Mansour A., Fox C.A., Thompson R.C., Akil H., and Watson S.J. mu-Opioid receptor mRNA expression in the rat CNS: comparison to mu-receptor binding. Brain Res 643 (1994) 245-265
30. Mansour A., Khachaturian H., Lewis M.E., Akil H., and Watson S.J. Autoradiographic differentiation of mu, delta, and kappa opioid receptors in the rat forebrain and midbrain. J Neurosci 7 (1987) 2445-2464
31. Mansouri F.A., Motamedi F., and 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 (1999) 419-423
32. Mansouri F.A., Motamedi F., Fathollahi Y., Atapour N., and Semnanian S. Augmentation of LTP induced by primed-bursts tetanic stimulation in hippocampal CA1 area of morphine dependent rats. Brain Res 769 (1997) 119-124
33. Masukawa L.M., and Prince D.A. Enkephalin inhibition of inhibitory input to CA1 and CA3 pyramidal neurons in the hippocampus. Brain Res 249 (1982) 271-280
34. McLean S., Rothman R.B., Jacobson A.E., Rice K.C., and 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 (1987) 497-510
35. McQuiston A.R. Effects of mu-opioid receptor modulation on GABAB receptor synaptic function in hippocampal CA1. J Neurophysiol 97 (2007) 2301-2311
36. McQuiston A.R., and 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 (2003) 1936-1948
37. Miles R., Toth K., Gulyas A.I., Hajos N., and Freund T.F. Differences between somatic and dendritic inhibition in the hippocampus. Neuron 16 (1996) 815-823
38. Nicoll R.A., Alger B.E., and Jahr C.E. Enkephalin blocks inhibitory pathways in the vertebrate CNS. Nature 287 (1980) 22-25
39. Olmstead M.C., and Franklin K.B. The development of a conditioned place preference to morphine: effects of lesions of various CNS sites. Behav Neurosci 111 (1997) 1313-1323
40. Olmstead M.C., and Franklin K.B. The development of a conditioned place preference to morphine: effects of microinjections into various CNS sites. Behav Neurosci 111 (1997) 1324-1334
41. Pourmotabbed A., Motamedi F., Fathollahi Y., Mansouri F.A., and 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 (1998) 125-134
42. Price C.J., Cauli B., Kovacs E.R., Kulik A., Lambolez B., Shigemoto R., and Capogna M. Neurogliaform neurons form a novel inhibitory network in the hippocampal CA1 area. J Neurosci 25 (2005) 6775-6786
43. Pu L., Bao G.B., Xu N.J., Ma L., and Pei G. Hippocampal long-term potentiation is reduced by chronic opiate treatment and can be restored by re-exposure to opiates. J Neurosci 22 (2002) 1914-1921
44. Rekling J.C. Effects of met-enkephalin on GABAergic spontaneous miniature IPSPs in organotypic slice cultures of the rat hippocampus. J Neurosci 13 (1993) 1954-1964
45. Reyes A., Lujan R., Rozov A., Burnashev N., Somogyi P., and Sakmann B. Target-cell-specific facilitation and depression in neocortical circuits. Nat Neurosci 1 (1998) 279-285
46. Self D.W., and Stein L. Pertussis toxin attenuates intracranial morphine self-administration. Pharmacol Biochem Behav 46 (1993) 689-695
47. Stevens K.E., Shiotsu G., and Stein L. Hippocampal mu-receptors mediate opioid reinforcement in the CA3 region. Brain Res 545 (1991) 8-16
48. Stumm R.K., Zhou C., Schulz S., and Hollt V. Neuronal types expressing mu- and delta-opioid receptor mRNA in the rat hippocampal formation. J Comp Neurol 469 (2004) 107-118
49. Svoboda K.R., Adams C.E., and Lupica C.R. Opioid receptor subtype expression defines morphologically distinct classes of hippocampal interneurons. J Neurosci 19 (1999) 85-95
50. Svoboda K.R., and Lupica C.R. Opioid inhibition of hippocampal interneurons via modulation of potassium and hyperpolarization-activated cation (Ih) currents. J Neurosci 18 (1998) 7084-7098
51. Swearengen E., and Chavkin C. Comparison of opioid and GABA receptor control of excitability and membrane conductance in hippocampal CA1 pyramidal cells in rat. Neuropharmacology 28 (1989) 689-697
52. Vida I., Halasy K., Szinyei C., Somogyi P., and Buhl E.H. Unitary IPSPs evoked by interneurons at the stratum radiatum-stratum lacunosum-moleculare border in the CA1 area of the rat hippocampus in vitro. J Physiol 506 Pt 3 (1998) 755-773
53. Wagner J.J., Etemad L.R., and Thompson A.M. Opioid-mediated facilitation of long-term depression in rat hippocampus. J Pharmacol Exp Ther 296 (2001) 776-781
54. White N.M. Addictive drugs as reinforcers: multiple partial actions on memory systems. Addiction 91 (1996) 921-949 1996)
55. Whittington M.A., Traub R.D., Faulkner H.J., Jefferys J.G., and Chettiar K. Morphine disrupts long-range synchrony of gamma oscillations in hippocampal slices. Proc Natl Acad Sci U S A 95 (1998) qj5807-qj5811
56. Wimpey T.L., Caudle R.M., and 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 (1990) 349-355
57. Wimpey T.L., and Chavkin C. Opioids activate both an inward rectifier and a novel voltage-gated potassium conductance in the hippocampal formation. Neuron 6 (1991) 281-289