Opioid receptor subtype expression defines morphologically distinct classes of hippocampal interneurons

Journal of Neuroscience

Volumn 19, Issue 1, 1999, Pages 85-95

  Svoboda, Kurt R ^a   Adams, Cathy E ^a   Lupica, Carl R ^a,b  

^a UNIVERSITY OF COLORADO   (United States)

^b NATIONAL INSTITUTE ON DRUG ABUSE   (United States)

Author keywords

Delta receptor; Electrophysiology; Enkephalin; GABA; Hippocampus; Inhibition; Morphology; Mu receptor; Nonselective cation current; Opioid receptor; Oriens alveus interneurons; Potassium current

Indexed keywords

4 AMINOBUTYRIC ACID; DELTA OPIATE RECEPTOR; ENKEPHALIN; MU OPIATE RECEPTOR; OPIATE RECEPTOR; RECEPTOR SUBTYPE;

4 AMINOBUTYRIC ACID RELEASE; ANIMAL TISSUE; ARTICLE; BRAIN SLICE; DENDRITE; ELECTROPHYSIOLOGY; HIPPOCAMPUS; INTERNEURON; NERVE ENDING; NERVE PROJECTION; NONHUMAN; POTASSIUM CURRENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; PYRAMIDAL NERVE CELL; RAT; SYNAPSE;

EID: 0032906938     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.19-01-00085.1999     Document Type: Article

References (58)

1. Ali AB, Thomson AM (1998) Facilitating pyramid to horizontal oriensalveus interneurone inputs- Dual intracellular recordings in slices of rat hippocampus. J Physiol (Lond) 507:185-199.
2. Ali AB, Deuchars J, Pawelzik H, Thomson AM (1998) CA1 pyramidal to basket and bistratified cell EPSPs: dual intracellular recordings in rat hippocampal slices. J Physiol (Lond) 507:201-217.
3. Bergles DE, Doze VA, Madison DV, Smith SJ (1996) Excitatory actions of norepinephrine on multiple classes of interneurons. J Neurosci 16:572-585.
4. Buhl EH, Halasy K, Somogyi P (1994a) Diverse sources of hippocampal unitary inhibitory postsynaptic potentials and the number of synaptic release site. Nature 368:823-828.
5. Buhl EH, Han Z, Lorinczi Z, Stezhka VV, Karnup SV, Somogyi P (1994b) Physiological properties of anatomically identified axo-axonic cells in the rat hippocampus. J Neurophysiol 71:1289-1307.
6. Buhl EH, Cobb SR, Halasy K, Somogyi P (1995) Properties of unitary IPSPs evoked by anatomically identified basket cells in the rat hippocampus. Eur J Neurosci 7:1989-2004.
7. Blasco-Ibanez JM, Freund TF (1995) Synaptic input of horizontal interneurons in stratum oriens of the hippocampal CA1 subfield: structural basis of feedback activation. Eur J Neurosci 7:2170-2180.
8. i increases in the dendrites of cerebellar Purkinje neurons. J Neurosci 15:2777-2788.
9. Ceranik K, Bender R, Geiger JRP, Monyer H, Jonas P, Frotscher M, Lubke J (1997) A novel type of GABAergic interneuron connecting the input and the output regions of the hippocampus. J Neurosci 17:5380-5394.
10. Chikwendu A, McBain CJ (1996) Two temporally overlapping "delayed-rectifiers" determine the voltage dependent potassium current phenotype in cultured hippocampal interneurons. J Neurophysiol 76:1477-1490.
11. Cobh SR, Buhl EH, Halasy K, Paulsen O, Somogyi P (1995) Synchronization of neuronal activity in hippocampus by individual GABAergic interneurons. Nature 378:75-78.
12. Cobb SR, Halasy K, Vida I, Nyiri G, Tamas G, Buhl EH, Somogyi P (1997) Synaptic effects of identified interneurons innervating both interneurons and pyramidal cells in the rat hippocampus. Neuroscience 79:629-648.
13. Cohen GA, Doze VA, Madison DV (1992) Opioid inhibition of GABA release from presynaptic terminals of rat hippocampal interneurons. Neuron 9:325-335.
14. Commons KG, Milner TA (1997) Localization of Delta opioid receptor immunoreactivity in interneurons and pyramidal cells in the rat hippocampus. J Comp Neurol 381:373-387.
15. Desmond NL, Scott CA, Jane Jr JA, Levy WB (1994) Ultrastructure identification of entorhinal cortical synapses in CA1 stratum lacunosum-moleculare of the rat. Hippocampus 4:594-600.
16. Dodt HU, Zieglgansberger W (1990) Visualizing unstained neurons in living brain slices by infrared DIC-videomicroscopy. Brain Res 537:333-336.
17. Frazier CJ, Rollins YD, Breese CR, Leonard S, Freedman R, Dunwiddie TV (1998) Acetylcholine activates an α-bungarotoxin sensitive nicotinic current in rat hippocampal interneurons, hut not pyramidal cells, J Neurosci 18:1187-1195.
18. Freund TF, Antal M (1988) GABA-containing neurons in the septum control inhibitory interneurons in the hippocampus. Nature 336:170-173.
19. Freund TF, Buzsáki G (1996) Interneurons of the hippocampus. Hippocampus 6:347-470.
20. Freund TF, Gulyas AI, Ascady L, Gores T, Toth K (1990) Serotonergic control of the hippocampus via local inhibitory interneurons. Proc Natl Acad Sci USA 87:8501-8505.
21. Fuzesi M, Racz B, Elias B, Halasy K (1997) Enkephalinergic nerve terminals target inhibitory interneurons in the rat hippocampus. NeuroReport 8:2471-2475.
22. Goldstein A, Naidu A (1989) Multiple opioid receptors: ligand selectivity profiles and binding site signatures. Mol Pharmacol 36:265-272.
23. Gulyas AI, Miles R, Hajos N, Freund TF (1993a) Precision and variability in post-synaptic target selection of inhibitory cells in the hippocampal CA3 region. Eur J Neurosci 5:1729-1751.
24. Gulyas AI, Miles R, Sik A, Toth K, Tamamaky N, Freund TF (1993b) Hippocampal pyramidal cells excite inhibitory neurons through a single release site. Nature 366:683-687.
25. + channel regulation of signal propagation in dendrites of hippocampal pyramidal neurons. Nature 368:869-875.
26. Lacaille JC, Mueller AL, Kunkel DD, Schwartzkroin PA (1987) Local circuit interactions between oriens/alveus interneurons and CA1 pyramidal cells in hippocampal slices: electrophysiology and morphology. J Neurosci 7:1979-1993.
27. Lee HK, Dunwiddie TV, Hoffer BJ (1980) Electrophysiological interactions of enkephalins with neuronal circuitry in the rat hippocampus II. Effects on interneuron excitability. Brain Res 184:331-342.
28. Li X, Somogyi P, Tepper JM, Buzsáki G (1992) Axonal and dendritic arborization of an intracellularly labeled chandelier cell in the CA1 region of the hippocampus. Exp Brain Res 90:519-525.
29. Lupica CR (1995) μ and δ enkephalins inhibit spontaneous GABA-mediated IPSCs via a cyclic AMP-independent mechanism in the rat hippocampus. J Neurosci 15:737-749.
30. Lupica CR, Dunwiddie TV (1991) Differential effects of mu- and delta-receptor selective opioid agonists on feedforward and feedback GABAergic inhibition in hippocampal brain slices. Synapse 8:237-248.
31. Lupica CR, Proctor WR, Dunwiddie TV (1992) Dissociation of μ and δ opioid receptor-mediated reductions in evoked and spontaneous synaptic inhibition in the rat hippocampus in vitro. Brain Res 593:226-238.
32. Maccaferri G, McBain CJ (1995) Passive propagation of LTD to stratum oriens-alveus inhibitory neurons modulates the temperoammonic input to the hippocampal CA1 region. Neuron 15:137-145.
33. Maccaferri G, McBain CJ (1996) The hyperpolarization-activated current Ih and its contribution to pacemaker activity in rat CA1 hippocampal stratum oriens-alveus interneurons. J Physiol (Lond) 497:119-130.
34. Madison DV, Nicoll RA (1988) Enkephalin hyperpolarizes interneurones in the rat hippocampus. J Physiol (Lond) 398:123-130.
35. Mansour A, Fox CA, Burke S, Akil H, Watson SJ (1995) Immunohistochemical localization of the cloned μ opioid receptor in the rat CNS. J Chem Neuroanat 8:283-305.
36. Masukawa LM, Prince DA (1984) Synaptic control of excitability in isolated dendrites of hippocampal neurons. J Neurosci 4:217-227.
37. McBain CJ, Dingledine R (1993) Heterogeneity of synaptic glutamate receptors on CA3 stratum radiatum interneurones of rat hippocampus. J Physiol (Lond) 462:373-392.
38. McBain CJ, DiChiara TJ, Kauer JA (1994) Activation of metahotropic glutamate receptors differentially affects two classes of hippocampal interneurons and potentiates excitatory synaptic transmission. J Neurosci 14:4433-4445.
39. McMahon LL, Kauer JA (1997) Hippocampal interneurons are excited via serotonin-gated ion channels. J Neurophysiol 78:2493-2502.
40. Miles R, Toth K, Gulyas AI, Hajos N, Freund TF (1996) Differences between somatic and dendritic inhibition in the hippocampus. Neuron 16:815-823.
41. + conductance in hippocampal interneurons. J Neurosci 17:4994-5003.
42. 3 receptor is present in different subpopulations of GABAergic neurons in the rat telencephalon. J Neurosci 17:3157-3167.
43. Mosbcrg HI, Hurst R, Hruby VJ, Gee K, Yamamura HI, Galligan JJ, Burks TF (1983) Bis-penicillamine enkephalins possess highly improved specificity toward delta opioid receptors. Proc Natl Acad Sci USA 80:5871-5874.
44. Nicoll RA, Alger BE, Jahr CE (1980) Enkephalin blocks inhibitory pathways in the vertebrate CNS. Nature 287:22-25.
45. Parra P, Gulyas AI, Miles R (1998) How many subtypes of inhibitory cells in the hippocampus? Neuron 20: 983-993.
46. Siggins GR, Zieglgansberger W (1981) Morphine and enkephalin peptides reduce inhibitory synaptic potentials in hippocampal pyramidal cells without alteration of membrane potential. Proc Natl Acad Sci USA 78:5235-5239.
47. Sik A, Penttonen M, Ylinen A, Buzsáki G (1995) Hippocampal CA1 interneurons: an in vivo intracellular labeling study. J Neurosci 15:6651-6665.
48. h) currents. J Neurosci 18:7084-7089, 1998.
49. i changes in the dendrites of hippocampal CA1 pyramidal neurons. J Neurophysiol 76:2896-2906.
50. Watson GB, Lanthorn TH (1993) Electrophysiological actions of delta opioids in CA1 of the rat hippocampal slice are mediated by one delta receptor subtype. Brain Res 601:129-135.
51. Whittington MA, Traub RD, Faulkner HJ, Jefferys JGR, Chettiar K (1998) Morphine disrupts long range synchrony of gamma oscillations in hippocampal slices. Proc Natl Acad Sci USA 95:5807-5811.
52. Whittington MA, Traub RD, Jefferys JG (1995) Synchronized oscillations in interneuron networks driven by metabotropic glutamate receptor activation. Nature 373:612-615.
53. Wimpey TL, Chavkin C (1991) Opioids activate both an inward rectifier and a novel voltage-gated potassium conductance in the hippocampal formation. Neuron 6:281-289.
54. Wimpey TL, Opheim KE, Chavkin C (1989) Effects of chronic morphine administration on the mu and delta opioid responses in the CA1 region of the rat hippocampus. J Pharmacol Exp Ther 251:405-411.
55. Xie C-W, Lewis DV (1991) Opioid-mediated facilitation of long-term potentiation at the lateral perforant path-dentate granule cell synapse. J Pharmacol Exp Ther 256:289-296.
56. Yanovsky Y, Sergceva OA, Freund TF, Haas HL (1997) Activation of interneurons at the stratum oriens/alveus border suppress excitatory transmission to apical dendrites in the CA1 area of the mouse hippocampus. Neuroscience 77:87-96.
57. Zhang L, McBain CJ (1995) Voltage-gated potassium currents in stratum oriens-alveus inhibitory neurones of the rat CA1 hippocampus. J Physiol (Lond) 488:647-660.
58. Zieglgansberger W, French ED, Siggins GR, Bloom FE (1979) Opioid peptides may excite hippocampal pyramidal neurons inhibiting adjacent inhibitory interneurons. Science 205:415-417.