Actions of endogenous opioids on NMDA receptor-independent long-term potentiation in area CA3 of the hippocampus

Journal of Neuroscience

Volumn 16, Issue 11, 1996, Pages 3652-3660

  Williams, Stephen H ^a,c   Johnston, Daniel ^a,b  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b Division of Neuroscience   (United States)

^c VANDERBILT UNIVERSITY   (United States)

Author keywords

CA3; hippocampus; LTP; mossy fiber; naloxone; NMDA independent; opioid; species differences

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; OPIATE PEPTIDE;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ELECTROPHYSIOLOGY; HIPPOCAMPUS; LONG TERM POTENTIATION; MALE; MOSSY FIBER; NONHUMAN; PRIORITY JOURNAL; RAT; SYNAPSE; SYNAPTIC TRANSMISSION;

EID: 0029933240     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.16-11-03652.1996     Document Type: Article

References (55)

1. Abraham WC, Goddard GV (1983) Asymmetric relationship between homosynaptic long-term potentiation and heterosynaptic long-term depression. Nature 305:717-719.
2. Amaral DG, Dent JA (1981) Development of the mossy fibers of the dentate gyrus. I. A light and electron microscopic study of the mossy fibers and their expansions. J Comp Neurol 195:51-86.
3. Amaral DG, Ishizuka N, Claiborne B (1990) Neurons, numbers and the hippocampal network. In: Understanding the brain through the hippocampus: the hippocampal region as a model for studying structure and function, Vol 83 (Storm-Mathisen J, Zimmer J, Ottersen OP, eds), pp 1-11. Amsterdam: Elsevier.
4. Bashir ZI, Bortolotto ZA, Davies CH, Berretta N, Irving AJ, Seal AJ, Henley JM, Jane DE, Watkins JC, Collingridge GL (1993) Induction of LTP in the hippocampus needs synaptic activation of glutamate metabotropic receptors. Nature 363:347-350.
5. Bear MF, Malenka RC (1994) Synaptic plasticity: LTP and LTD. Curr Opin Neurobiol 4:389-399.
6. Bradler JE, Barrionuevo G (1990) Heterosynaptic correlates of long-term potentiation induction in hippocampal CA3 neurons. Neuroscience 35:265-271.
7. Bramham CR (1992) Opioid receptor dependent long-term potentiation: peptidergic regulation of synaptic plasticity in the hippocampus. Neurochem Int 20: 441-471.
8. Bramham CR, Errington ML, Bliss TVP (1988) Naloxone blocks the induction of long-term potentiation in the lateral but not in the medial perforant pathway in the anesthetized rat. Brain Res 449:352-356.
9. Brown TH, Johnston D (1983) Voltage-clamp analysis of mossy fiber synaptic input to hippocampal neurons. J Neurophysiol 50:487-507.
10. Caudle RM, Chavkin C (1990) Mu opioid receptor activation reduces inhibitory postsynaptic potentials in hippocampal CA3 pyramidal cells of rat and guinea pig. J Pharmacol Exp Ther 252:1361-1369.
11. Caudle RM, Wagner JJ, Chavkin C (1991) Endogenous opioids released from perforant path modulate norepinephrine actions and inhibitory postsynaptic potentials in guinea pig CA3 pyramidal cells. J Pharmacol Exp Ther 258:18-26.
12. Claiborne BJ, Xiang Z, Brown TH (1993) Hippocampal circuitry complicates analysis of long-term potentiation in mossy fiber synapses. Hippocampus 3:115-121.
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. Crain BJ, Chang KJ, McNamara JO (1986) Quantitative autoradiographic analysis of mu and delta opioid binding sites in the rat hippocampal formation. J Comp Neurol 246:170-180.
15. Derrick BE, Martinez JL (1994a) Frequency-dependent associative long-term potentiation at the hippocampal mossy fiber-CA3 synapse. Proc Natl Acad Sci USA 91:10290-10294.
16. Derrick BE, Martinez JL (1994b) Opioid receptor activation is one factor underlying the frequency dependence of mossy fiber LTP induction. J Neurosci 14:4359-4367.
17. Derrick BE, Rodriguez SB, Lieberman DN, Martinez JL (1992) Mu opioid receptors are associated with the induction of hippocampal mossy fiber long-term potentiation. J Pharmacol Exp Ther 263:725-733.
18. Derrick BE, Weinberger SB, Martinez JL (1991) Opioid receptors are involved in an NMDA receptor-independent mechanism of LTP induction at hippocampal mossy fiber-CA3 synapses. Brain Res Bull 27:219-223.
19. Gall C, Brecha N, Karten HJ, Chang KJ (1981) Localization of enkephalin-like immunoreactivity to identified axonal and neuronal populations of the rat hippocampus. J Comp Neurol 198:335-350.
20. Hopkins WF, Johnston D (1984) Frequency-dependent noradrenergic modulation of long-term potentiation in the hippocampus. Science 226:350-352.
21. Hopkins WF, Johnston D (1988) Noradrenergic enhancement of long-term potentiation at mossy fiber synapses in the hippocampus. J Neurophysiol 59:667-687.
22. Huang Y-Y, Li X-C, Kandel ER (1994) cAMP contributes to mossy fiber LTP by initiating both a covalently mediated early phase and macromolecular synthesis-dependent late phase. Cell 79:69-79.
23. Ishihara K, Katsuki H, Sugimura M, Kaneko S, Satoh M (1990) Different drug-susceptibilities of long-term potentiation in three input systems to the CA3 region of the guinea pig hippocampus in vitro. Neuropharmacology 29:487-492.
24. Jaffe D, Johnston D (1990) The induction of long-term potentiation at hippocampal mossy fibers follows a Hebbian rule. J Neurophysiol 64:948-960.
25. Jan LY, Jan YN (1982) Peptidergic transmission in sympathetic ganglia of the frog. J Physiol (Lond) 327:219-246.
26. Johnston D, Brown TH (1983) Interpretation of voltage-clamp measurements in hippocampal neurons. J Neurophysiol 50:464-486.
27. Jonas P, Major G, Sakmann B (1993) Quantal components of unitary EPSCs at the mossy fibre synapse on CA3 pyramidal cells of rat hippocampus. J Physiol (Lond) 472:615-663.
28. Levy WB, Steward O (1979) Synapses as associative memory elements in the hippocampal formation. Brain Res 175:233-245.
29. Lisman J (1989) A mechanism for the Hebb and the anti-Hebb processes underlying learning and memory. Proc Natl Acad Sci USA 86:9574-9578.
30. Lundberg JM, Hokfelt T (1983) Coexistence of peptides and classical neurotransmitters. Trends Neurosci 6:325-333.
31. Lundberg JM, Angaard A, Fahrenkrug J (1981) Complementary role of vasoactive intestinal polypeptide (VIP) and acetylcholine for cat submandibular gland blood flow and secretion. II. Effects of cholinergic antagonists and VIP antiserum. Acta Physiol Scand 113:329-336.
32. Mansour A, Fox CA, Akil H, Watson SJ (1995) Opioid-receptor mRNA expression in the rat CNS: anatomical and functional implications. Trends Neurosci 18:22-29.
33. Martin MR (1983) Naloxone and long term potentiation of hippocampal CA3 field potentials in vitro. Neuropeptides 4:45-50.
34. McGinty JF, Henriksen SJ, Goldstein A, Terenius L, Bloom FE (1983) Dynorphin is contained within hippocampal mossy fibers: immuno-chemical alterations after kainic acid administration and colchicine. Proc Natl Acad Sci USA 80:589-593.
35. McLean S, Rothman RB, Jacobson AE, Rice KC, Herkenham M (1987) 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.
36. Miles R, Wong RKS (1987) Latent synaptic pathways revealed after tetanic stimulation in the hippocampus. Nature 329:724-726.
37. Morris BJ, Johnston HM (1995) A role for hippocampal opioids in long-term functional plasticity. Trends Neurosci 18:350-355.
38. Provencher SW (1976) An eigenfunction expansion method for the analysis of exponential decay curves. J Chem Phys 64:2772-2777.
39. Salin PA, Weisskopf MG, Nicoll RA (1995) A comparison of the role of dynorphin in the hippocampal mossy fiber pathway in guinea pig and rat. J Neurosci 15:6939-6945.
40. Spruston N, Jaffe DB, Williams SH, Johnston D (1993) Voltage- and space-clamp errors associated with the measurement of electronically remote synaptic events. J Neurophysiol 70:781-802.
41. Stevens KE, Shiotsu G, Stein L (1991) Hippocampal μ receptors mediate opioid reinforcement in the CA3 region. Brain Res 545:8-16.
42. Terman GW, Wagner JJ, Chavkin C (1994) Kappa opioids inhibit induction of long-term potentiation in the dentate gyrus of the guinea pig hippocampus. J Neurosci 14:4740-4747.
43. Urban NN, Barrionuevo G (1995) Induction of Hebbian and non-Hebbian LTP at the hippocampal mossy fiber synapse by distinct patterns of high frequency stimulation. Soc Neurosci Abstr 21:2006.
44. Wagner JJ, Caudle RM, Chavkin C (1990) Stimulation of endogenous opioid release displaces mu receptor binding in rat hippocampus. Neuroscience 37:45-53.
45. Wagner JJ, Terman GW, Chavkin C (1993) Endogenous dynorphins inhibit excitatory neurotransmission and block LTP induction. Nature 363:451-454.
46. Weisskopf MG, Zalutsky RA, Nicoll RA (1993) The opioid peptide dynorphin mediates heterosynaptic depression of hippocampal mossy fibre synapses and modulates long-term potentiation. Nature 362:423-427.
47. Weisskopf MG, Castillo PE, Zalutsky RA, Nicoll RA (1994) Mediation of hippocampal mossy fiber long-term potentiation by cyclic AMP. Science 265:1878-1882.
48. Williams SH (1994) Comparison of mossy fiber LTP in the rat and guinea-pig hippocampus. Soc Neurosci Abstr 20:715.
49. Williams SH, Johnston D (1989) Long-term potentiation of hippocampal mossy fiber synapses is blocked by postsynaptic injection of calcium chelators. Neuron 3:583-588.
50. Williams SH, Johnston D (1991) Kinetic properties of two anatomically distinct excitatory synapses in hippocampal CA3 pyramidal neurons. J Neurophysiol 66:1010-1020.
51. Williams SH, Johnston D (1992) A novel action of endogenous opioids in the induction of hippocampal mossy fiber LTP. Soc Neurosci Abstr 18:403.
52. Xiang Z, Greenwood AC, Kairiss EW, Brown TH (1994) Quantal mechanism of long-term potentiation in hippocampal mossy-fiber synapses. J Neurophysiol 71:2552-2556.
53. 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.
54. Zalutsky RA, Nicoll RA (1990) Comparison of two forms of long-term potentiation in single hippocampal neurons. Science 248:1619-1624.
55. Zieglgansberger W, French ED, Siggins GR, Bloom FE (1979) Opioid peptides may excite hippocampal pyramidal neurons by inhibiting adjacent inhibitory interneurons. Science 205:415-417.