Opioid systems in the dentate gyrus

Progress in Brain Research

Volumn 163, Issue , 2007, Pages

  Drake, Carrie T ^a   Chavkin, Charles ^b   Milner, Teresa A ^a  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

^b UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

Author keywords

disinhibition; dynorphin; enkephalin; GABA interneuron; long term potentiation; neurogenesis; opioid receptors; seizure

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR; DELTA OPIATE RECEPTOR; DELTA OPIATE RECEPTOR AGONIST; DYNORPHIN; ENKEPHALIN; KAPPA OPIATE RECEPTOR; KAPPA OPIATE RECEPTOR AGONIST; MOLECULAR LAYER; MORPHINE; MU OPIATE RECEPTOR; MU OPIATE RECEPTOR AGONIST; NALOXONE; OPIATE; OPIATE PEPTIDE; OPIATE RECEPTOR;

DELTA RHYTHM; DENDRITE; DENTATE GYRUS; GENE ACTIVATION; GRANULE CELL; HUMAN; INTERNEURON; LONG TERM POTENTIATION; MOSSY FIBER; NERVE CELL EXCITABILITY; NERVE CELL INHIBITION; NERVE ENDING; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PERFORANT NERVE TRACT; PHYSIOLOGY; PRIORITY JOURNAL; REVIEW; SEIZURE;

EID: 34548254437     PISSN: 00796123     EISSN: None     Source Type: Book Series    
DOI: 10.1016/S0079-6123(07)63015-5     Document Type: Review

References (166)

1. Abbadie C., Pan Y.X., Drake C.T., and Pasternak G.W. Comparative immunohistochemical distributions of carboxy terminus epitopes from the mu-opioid receptor splice variants MOR-1D, MOR-1 and MOR-1C in the mouse and rat CNS. Neuroscience 100 (2000) 141-153
2. Alreja M., Shanabrough M., Liu W.M., and Leranth C. Opioids suppress IPSCs in neurons of the rat medial septum/diagonal band of Broca: Involvement of μ-opioid receptors and septohippocampal GABAergic neurons. J. Neurosci. 20 (2000) 1179-1189
3. 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
4. Arvidsson U., Risling M., Frisén J., Piehl F., Fried K., Hökfelt T., and Cullheim S. trkC-like immunoreactivity in the primate descending serotoninergic system. Eur. J. Neurosci. 6 (1994) 230-236
5. Bausch S.B., and Chavkin C. Changes in hippocampal circuitry after pilocarpine-induced seizures as revealed by opioid receptor distribution and activation. J. Neurosci. 17 (1997) 477-492
6. Bausch S.B., Esteb T.M., Terman G.W., and Chavkin C. Administered and endogenously released kappa opioids decrease pilocarpine-induced seizures and seizure-induced histopathology. J. Pharmacol. Exp. Ther. 284 (1998) 1147-1155
7. Bausch S.B., Patterson T.A., Appleyard S.M., and Chavkin C. Immunocytochemical localization of delta opioid receptors in mouse brain. J. Chem. Neuroanat. 8 (1995) 175-189
8. Bausch S.B., Patterson T.A., Ehrengruber M., Lester H.A., Davidson N., and Chavkin C. Colocalization of mu opioid receptors with GIRK1 potassium channels in rat brain: an immunocytochemical study. Receptors Channels 3 (1995) 221-241
9. Bouvier M. Oligomerization of G-protein-coupled transmitter receptors. Nat. Rev. Neurosci. 2 (2001) 274-286
10. Bramham C.R. Opioid receptor dependent long-term potentiation: peptidergic regulation of synaptic plasticity in the hippocampus. Neurochem. Int. 20 (1992) 441-455
11. Bramham C.R., and Sarvey J.M. Endogenous activation of μ and δ-1 opioid receptors is required for long-term potentiation induction in the lateral perforant path: Dependence on GABAergic inhibition. J. Neurosci. 16 (1996) 8123-8131
12. Bunzow J.R., Saez C., Mortrud M., Bouvier C., Williams J.T., Low M., and Grandy D.K. Molecular cloning and tissue distribution of a putative member of the rat opioid receptor gene family that is not a mu, delta or kappa opioid receptor type. FEBS Lett. 347 (1994) 284-288
13. 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
14. Caudle R.M., Chavkin C., and Dubner R. Kappa2 opioid receptors inhibit NMDA receptor-mediated synaptic currents in guinea pig CA3 pyramidal cells. J. Neurosci. 14 (1994) 5580-5589
15. Caudle R.M., and Dubner R. Ifenprodil blocks the excitatory effects of the opioid peptide dynorphin 1-17 on NMDA receptor mediated currents in the CA3 region of the guinea pig hippocampus. Neuropeptides 32 (1998) 87-95
16. Chavkin C. Dynorphins are endogenous opioid peptides released from granule cells to act neurohumorly and inhibit excitatory neurotransmission in the hippocampus. Prog. Brain Res. 125 (2000) 363-367
17. Chavkin C., Henriksen S.J., Siggins G.R., and Bloom F.E. Selective inactivation of opioid receptors in rat hippocampus demonstrates that dynorphin-A and -B may act on mu-receptors in the CA1 region. Brain Res. 331 (1985) 366-370
18. Chavkin C., James I.F., and Goldstein A. Dynorphin is a specific endogenous ligand of the kappa opioid receptor. Science 215 (1982) 413-415
19. Chavkin C., Shoemaker W.J., McGinty J.F., Bayon A., and Bloom F.E. Characterization of the prodynorphin and proenkephalin neuropeptide systems in rat hippocampus. J. Neurosci. 5 (1985) 808-816
20. Chen Y., Mestek A., Liu J., Hurley J.A., and Yu L. Molecular cloning and functional expression of a mu-opioid receptor from rat brain. Mol. Pharmacol. 44 (1993) 8-12
21. Clark J.A., Liu L., Price M., Hersh B., Edelson M., and Pasternak G.W. Kappa opiate receptor multiplicity: evidence for two U50,488-sensitive kappa 1 subtypes and a novel kappa 3 subtype. J. Pharmacol. Exp. Ther. 251 (1989) 461-468
22. 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
23. Commons K.G., and Milner T.A. Ultrastructural heterogeneity of enkephalin-containing neurons in the rat hippocampal formation. J. Comp. Neurol. 358 (1995) 324-342
24. Commons K.G., and Milner T.A. Cellular and subcellular localization of delta opiate receptor immunoreactivity in the rat dentate gyrus. Brain Res. 738 (1996) 181-195
25. Commons K.G., and Milner T.A. The ultrastructural relationships between leu-enkephalin and GABA containing neurons differ within the hippocampal formation. Brain Res. 724 (1996) 1-15
26. Corbett A.D., Paterson S.J., and Kosterlitz H.W. Selectivity of ligands for opioid receptors. In: Herz A. (Ed). Opioids I (1993), Springer-Verlag, Berlin 645-680
27. Corbett A.D., Paterson S.J., McKnight A.T., Magnan J., and Kosterlitz H.W. Dynorphin and dynorphin are ligands for the kappa-subtype of opiate receptor. Nature 299 (1982) 79-81
28. 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
29. De Camilli P., and Jahn R. Pathways to regulated exocytosis in neurons. Annu. Rev. Physiol. 52 (1990) 625-645
30. Ding Y.Q., Kaneko T., Nomura S., and Mizuno N. Immunohistochemical localization of μ-opioid receptors in the central nervous system of the rat. J. Comp. Neurol. 367 (1996) 375-402
31. Drake C.T., Chang P.C., Harris J.A., and Milner T.A. Neurons with mu opioid receptors interact indirectly with enkephalin-containing neurons in the rat dentate gyrus. Exp. Neurol. 176 (2002) 254-261
32. Drake C.T., Chavkin C., and Milner T.A. Kappa opioid receptor-like immunoreactivity is present in substance P-containing subcortical afferents in guinea pig dentate gyrus. Hippocampus 7 (1997) 36-47
33. 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
34. Drake C.T., and Milner T.A. Mu opioid receptors are extensively co-localized with parvalbumin, but not somatostatin, in the dentate gyrus. Neurosci. Lett. 403 (2006) 176-180
35. Drake C.T., Patterson T.A., Simmons M.L., Chavkin C., and Milner T.A. Kappa opioid receptor-like immunoreactivity in guinea pig brain: ultrastructural localization in presynaptic terminals in hippocampal formation. J. Comp. Neurol. 370 (1996) 377-395
36. Drake C.T., Terman G.W., Simmons M.L., Milner T.A., Kunkel D.D., Schwartzkroin P.A., and Chavkin C. Dynorphin opioids present in dentate granule cells may function as retrograde inhibitory neurotransmitters. J. Neurosci. 14 (1994) 3736-3750
37. Eisch A.J., Barrot M., Schad C.A., Self D.W., and Nestler E.J. Opiates inhibit neurogenesis in the adult rat hippocampus. Proc. Natl. Acad. Sci. U.S.A. 97 (2000) 7579-7584
38. Eisch A.J., and Harburg G.C. Opiates, psychostimulants, and adult hippocampal neurogenesis: Insights for addition and stem cell biology. Hippocampus 16 (2006) 271-286
39. Evans C.J., Keith D.E., Morrison H., Magendzo K., and Edwards R.H. Cloning of a delta opioid receptor by functional expression. Science 258 (1992) 1952-1955
40. Fredens K., Stengaard Pedersen K., and Larsson L.I. Localization of enkephalin and cholecystokinin immunoreactivities in the perforant path terminal fields of the rat hippocampal formation. Brain Res. 304 (1984) 255-263
41. French E.D., and Siggins G.R. An iontophoretic survey of opioid peptide actions in the rat limbic system: in search of opiate epileptogenic mechanisms. Regul. Pept. 1 (1980) 127-146
42. Freund T.F., and Buzsáki G. Interneurons of the hippocampus. Hippocampus 6 (1996) 347-470
43. Gall C. Seizures induce dramatic and distinctly different changes in enkephalin, dynorphin, and CCK immunoreactivities in mouse hippocampal mossy fibers. J. Neurosci. 8 (1988) 1852-1862
44. Gall C.M. Localization and seizure-induced alterations of opioid peptides and CCK in the hippocampus. Natl. Inst. Drug Abuse Res. Monogr. Ser. 82 (1988) 12-32
45. Gall C., Brecha N., Karten H.J., and Chang K.-J. Localization of enkephalin-like immunoreactivity to identified axonal and neuronal populations of the rat hippocampus. J. Comp. Neurol. 198 (1981) 335-350
46. George S.R., Fan T., Xie Z., Tse R., Tam V., Varghese G., and O'Dowd B.F. Oligomerization of mu- and delta-opioid receptors, generation of novel functional properties. J. Biol. Chem. 275 (2000) 26128-26135
47. Gomes I., Jordan B.A., Gupta A., Trapaidze N., Nagy V., and Devi L.A. Heterodimerization of μ and δ opioid receptors: a role in opiate synergy. J. Neurosci. 20 (2000) NIL22-NIL26
48. Goodman R.R., Snyder S.H., Kuhar M.J., and Young III W.S. Differentiation of delta and mu opiate receptor localizations by light microscopic autoradiography. Proc. Natl. Acad. Sci. U.S.A. 77 (1980) 6239-6243
49. Gould E., and Gross C.G. Neurogenesis in adult mammals: some progress and problems. J. Neurosci. 22 (2002) 619-623
50. Gubler U., Seeburg P., Hoffman B.J., Gage L.P., and Udenfriend S. Molecular cloning establishes proenkephalin as precursor of enkephalin-containing peptides. Nature 295 (1982) 206-208
51. Guerra D., Sole A., Cami J., and Tobena A. Neurophysiological performance in opiate addicts after rapid detoxification. Drug Alcohol Depend. 20 (1987) 261-270
52. Gulya K., Gehlert D.R., Wamsley J.K., Mosberg H., Hruby V.J., and Yamamura H.I. Light microscopic autoradiographic localization of delta opioid receptors in the rat brain using a highly selective bis-penicillamine cyclic enkephalin analog. J. Pharmacol. Exp. Ther. 238 (1986) 720-726
53. Heinricher M.M. Orphanin FQ/nociceptin: from neural circuitry to behavior. Life Sci. 73 (2003) 813-822
54. Herkenham M., and McLean S. The anatomical relationship of opioid peptides and opiate receptors in the hippocampi of four rodent species. Natl. Inst. Drug Abuse Res. Monogr. Ser. 82 (1988) 33-47
55. 2+ channels by G-protein beta gamma subunits. Nature 380 (1996) 258-262
56. Hong J.S., McGinty J.F., Grimes L., Kanamatsu T., Obie J., and Mitchell C.L. Seizure-induced alterations in the metabolism of hippocampal opioid peptides suggest opioid modulation of seizure-related behaviors. Natl. Inst. Drug Abuse Res. Monogr. Ser. 82 (1988) 48-66
57. Hong J.S., McGinty J.F., Lee P.H.K., Xie C.W., and Mitchell C.L. Relationship between hippocampal opioid peptides and seizures. Prog. Neurobiol. 40 (1993) 507-528
58. Hong J.S., Wood P.L., Gillin J.C., Yang H.Y., and Costa E. Changes of hippocampal Met-enkephalin content after recurrent motor seizures. Nature 285 (1980) 231-232
59. Houser C.R., Miyashiro J.E., Swartz B.E., Walsh G.O., Rich J.R., and Delgado-Escueta A.V. Altered patterns of dynorphin immunoreactivity suggest mossy fiber reorganization in human hippocampal epilepsy. J. Neurosci. 10 (1990) 267-282
60. Ikeda S.R. Voltage-dependent modulation of N-type calcium channels by G-protein beta gamma subunits. Nature 380 (1996) 255-258
61. Jackisch R., Geppert M., Brenner A.S., and Illes P. Presynaptic opioid receptors modulating acetylcholine release in the hippocampus of the rabbit. Naunyn Schmiedebergs Arch. Pharmacol. 332 (1986) 156-162
62. Jackisch R., Werle E., and Hertting G. Identification of mechanisms involved in the modulation of release of noradrenaline in the hippocampus of the rabbit in vitro. Neuropharmacology 23 (1984) 1363-1371
63. Jiang Q., Takemori A.E., Sultana M., Portoghese P.S., Bowen W.D., Mosberg H.I., and Porreca F. Differential antagonism of opioid delta antinociception by [D-Ala2,Leu5,Cys6]enkephalin and naltrindole 5′-isothiocyanate: evidence for delta receptor subtypes. J. Pharmacol. Exp. Ther. 257 (1991) 1069-1075
64. Johnston H.M., and Morris B.J. Nitric oxide alters proenkephalin and prodynorphin gene expression in hippocampal granule cells. Neuroscience 61 (1994) 435-439
65. Kakidani H., Furutani Y., Takahashi H., Noda M., Morimoto Y., Hirose T., Asai M., Inayama S., Nakanishi S., and Numa S. Cloning and sequence analysis of cDNA for porcine beta-neo-endorphin/dynorphin precursor. Nature 298 (1982) 245-249
66. Kalyuzhny A.E., and Wessendorf M.W. CNS GABA neurons express the mu-opioid receptor: immunocytochemical studies. Neuroreport 20 8 (1997) 3367-3372
67. Kaplan T.J., Skyers P.R., Tabori N.E., Drake C.T., and Milner T.A. Ultrastructural evidence for mu-opioid modulation of cholinergic pathways in rat dentate gyrus. Brain Res. 1019 (2004) 28-38
68. Karhunen T., Vilim F.S., Alexeeva V., Weiss K.R., and Church P.J. Targeting of peptidergic vesicles in cotransmitting terminals. J. Neurosci. 21 (2001) RC127
69. Khachaturian H., Schaefer M.K.H., and Lewis M.E. Anatomy and function of the endogenous opioid system. In: Herz A. (Ed). Opiod I (1993), Springer-Verlag, Berlin 471-497
70. Kieffer B.L., Befort K., Gaveriaux-Ruff C., and Hirth C.G. The delta opioid receptor: isolation of a cDNA by expression cloning and pharmacological characterization. Proc. Natl. Acad. Sci. U.S.A. 89 (1992) 12048-12052
71. Lee P.H., Obie J., and Hong J.S. Opioids induce convulsions and wet dog shakes in rats: mediation by hippocampal mu, but not delta or kappa opioid receptors. J. Neurosci. 9 (1989) 692-697
72. Liu S., Wang J., Zhu D.Y., Fu Y., Lukowiak K., and Lu Y.M. Generation of functional inhibitory neurons in the adult rat hippocampus. J. Neurosci. 23 (2003) 732-736
73. Luscher C., Jan L.Y., Stoffel M., Malenka R.C., and Nicoll R.A. G protein-coupled inwardly rectifying K+ channels (GIRKs) mediate postsynaptic but not presynaptic transmitter actions in hippocampal neurons. Neuron 19 (1997) 687-695
74. Maderspach K., Nemeth K., Simon J., Benyhe S., Szucs M., and Wollemann M. A monoclonal antibody recognizing kappa-but not mu-and delta-opioid receptors. J. Neurochem. 56 (1991) 1897-1904
75. Maderspach K., Takacs J., Niewiadomska G., and Csillag A. Postsynaptic and extrasynaptic localization of kappa-opioid receptor in selected brain areas of young rat and chick using an anti-receptor monoclonal antibody. J. Neurocytol. 24 (1995) 478-486
76. Madison D.V., and Nicoll R.A. Enkephalin hyperpolarizes interneurons in the rat hippocampus. J. Physiol. 398 (1988) 123-130
77. Mansour A., Burke S., Pavlic R.J., Akil H., and Watson S.J. Immunohistochemical localization of the cloned kappa 1, receptor in the rat CNS and pituitary. Neuroscience 71 (1996) 671-690
78. 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
79. 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
80. Mansour A., Khachaturian H., Lewis M.E., Akil H., and Watson S.J. Anatomy of CNS opioid receptors. Trends Neurosci. 11 (1988) 308-314
81. Mansour A., Thompson R.C., Akil H., and Watson S.J. Delta opioid receptor mRNA distribution in the brain: comparison to delta receptor binding and proenkephalin mRNA. J. Chem. Neuroanat. 6 (1993) 351-362
82. Martin W.R. Pharmacology of opioids. Pharmacol. Rev. 35 (1983) 283-323
83. Matsumoto M., Yoshioka M., Togashi H., Hirokami M., Tochihara M., Ikeda T., Smith C.B., and Saito H. mu-Opioid receptors modulate noradrenaline release from the rat hippocampus as measured by brain microdialysis. Brain Res. 636 (1994) 1-8
84. Mattia A., Vanderah T., Mosberg H.I., and Porreca F. Lack of antinociceptive cross-tolerance between [D-Pen2, D-Pen5]enkephalin and [D-Ala2]deltorphin II in mice: evidence for delta receptor subtypes. J. Pharmacol. Exp. Ther. 258 (1991) 583-587
85. McDaniel K.L., Mundy W.R., and Tilsom H.A. Microinjection of dynorphin into the hippocampal formation impairs spatial learning in rats. Pharmacol. Biochem. Behav. 35 (1990) 429-435
86. McGinty J.F., Henriksen S.J., Goldstein A., Terenius L., and Bloom F.E. Dynorphin is contained within hippocampal mossy fibers: immunochemical alterations after Kainic acid administration and colchicines-induced neurotoxicity. Proc. Natl. Acad. Sci. U.S.A. 80 (1983) 589-593
87. McGinty J.F., Kanamatsu T., Obie J., and Hong J.S. Modulation of opioid peptide metabolism by seizures: differentiation of opioid subclasses. Natl. Inst. Drug Abuse Res. Monogr. Ser. 71 (1986) 89-101
88. 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
89. Merchenthaler I., Maderdrut J.L., Cianchetta P., Shughrue P.J., and Bronstein D. In situ hybridization histochemical localization of prodynorphin messenger RNA in the central nervous system of the rat. J. Comp. Neurol. 384 (1997) 211-232
90. Meunier J.-C., Mollereau C., Toll L., Suaudeau C., Moisand C., Alvinerie P., Butour J.-L., Guillemot J.-C., Ferrara P., Monsarrat B., Mazarguil H., Vassart G., Parmentier M., and Costentin J. Isolation and structure of the endogenous agonist of opioid receptor-like ORL1 receptor. Nature 377 (1995) 532-536
91. Milner T.A., and Drake C.T. Ultrastructural evidence for presynaptic μ opioid receptor modulation of synaptic plasticity in NMDA-receptor-containing dendrites in the dentate gyrus. Brain Res. Bull. 54 (2001) 131-140
92. Minami M., Hosoi Y., Toya T., Katao Y., Maekawa K., Katsumata S., Yabuuchi K., Onogi T., and Satoh M. In situ hybridization study of kappa-opioid receptor mRNA in the rat brain. Neurosci. Lett. 162 (1993) 161-164
93. Mogil J.S., and Pasternak G.W. The molecular and behavioral pharmacology of the orphanin FQ/nociceptin peptide and receptor family. Pharmacol. Rev. 53 (2001) 381-415
94. Moore S.D., Madamba S.G., Schweitzer P., and Siggins G.R. Voltage-dependent effects of opioid peptides on hippocampal CA3 pyramidal neurons in vitro. J. Neurosci. 14 (1994) 809-820
95. Morris B.J., and Johnston H.M. A role for hippocampal opioids in long-term functional plasticity. Trends Neurosci. 18 (1995) 350-355
96. Nestler E.J. Molecular basis of long-term plasticity underlying addiction. Nat. Rev. Neurosci. 2 (2001) 119-128
97. Neumaier J.F., Mailheau S., and Chavkin C. Opioid receptor-mediated responses in the dentate gyrus and CA1 region of the rat hippocampus. J. Pharmacol. Exp. Ther. 244 (1988) 564-570
98. Nock B., Rajpara A., O'Connor L.H., and Cicero T.J. Autoradiography of [3 H]U-69593 binding sites in rat brain: evidence for kappa opioid receptor subtypes. Eur. J. Pharmacol. 154 (1988) 27-34
99. Noda M., Furutani Y., Takahashi H., Toyosato M., Hirose T., Inayama S., Nakanishi S., and Numa S. Cloning and sequence analysis of cDNA for bovine adrenal preproenkephalin. Nature 295 (1982) 202-206
100. Pan Y.X., Xu J., Bolan E., Abbadie C., Chang A., Zuckerman A., Rossi G., and Pasternak G.W. Identification and characterization of three new alternatively spliced mu-opioid receptor isoforms. Mol. Pharmacol. 56 (1999) 396-403
101. Pierce J.P., Kurucz O., and Milner T.A. The morphometry of a peptidergic transmitter system before and after seizure. I. Dynorphin B-like immunoreactivity in the hippocampal mossy fiber system. Hippocampus 9 (1999) 255-276
102. Pierce J.P., and Milner T.A. Parallel increases in the synaptic and surface areas of mossy fiber terminals following seizure induction. Synapse 39 (2001) 249-256
103. Pierce T.L., and Wessendorf M.W. Immunocytochemical mapping of endomorphin-2-immunoreactivity in rat brain. J. Chem. Neuroanat. 18 (2000) 181-207
104. Piguet P., and North R.A. Opioid actions at mu and delta receptors in the rat dentate gyrus in vitro. J. Pharmacol. Exp. Ther. 266 (1993) 1139-1146
105. Piva F., Limonta P., Dondi D., Pimpinelli F., Martini L., and Maggi R. Effects of steroids on the brain opioid system. J. Steroid Biochem. Mol. Biol. 53 (1995) 343-348
106. 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
107. Quinones-Jenab V., Jenab S., Ogawa S., Inturrisi C., and Pfaff D.W. Estrogen regulation of mu-opioid receptor mRNA in the forebrain of female rats. Brain Res. 47 (1997) 1
108. Rees H., Ang L.C., Shul D.D., George D.H., Begley H., and McConnell T. Increase in enkephalin-like immunoreactivity in hippocampi of adults with generalized epilepsy. Brain Res. 652 (1994) 113-119
109. Reinscheid R.K., Nothacker H.P., Bourson A., Ardati A., Henningsen R.A., Bunzow J.R., Grandy D.K., Langen H., Monsma Jr. F.J., and Civelli O. Orphanin FQ: a neuropeptide that activates an opioid-like G protein-coupled receptor. Science 270 (1995) 792-794
110. Rios C.D., Jordan B.A., Gomes I., and Devi L.A. G-protein-coupled receptor dimerization: modulation of receptor function. Pharmacol. Ther. 92 (2001) 71-87
111. Robbins T.W., and Everitt B.J. Limbic-striatal memory systems and drug addiction. Neurobiol. Learn. Mem. 78 (2002) 625-636
112. Rocha L., Ackermann R.F., and Engel Jr. J. Effects of chronic morphine pretreatment on amygdaloid kindling development, postictal seizure and suppression and benzodiazepine receptor binding in rats. Epilepsy Res. 23 (1996) 225-233
113. Roman E., Ploj K., Gustafsson L., Meyerson B.J., and Nylander I. Variations in opioid peptide levels during the estrous cycle in Sprague-Dawley rats. Neuropeptides 40 (2006) 195-206
114. Rothman R.B., Bowen W.D., Schumacher U.K., and Pert C.B. Effect of beta-FNA on opiate receptor binding: preliminary evidence for two types of mu receptors. Eur. J. Pharmacol. 95 (1983) 147-148
115. Rothman R.B., Jacobson A.E., Rice K.C., and Herkenham M. Autoradiographic evidence for two classes of mu opioid binding sites in rat brain using [125I]FK33824. Peptides 8 (1987) 1015-1021
116. Sandin J., Nylander I., Georgieva J., Schött P.A., Ögren S.O., and Terenius L. Hippocampal dynorphin B injections impair spatial learning in rats: a kappa-opioid receptor-mediated effect. Neuroscience 85 (1998) 375-382
117. Schindler C.J., Slamberova R., Rimanoczy A., Hnactzuk O.C., Riley M.A., and Vathy I. Field-specific changes in hippocampal opioid mRNA, peptides, and receptors due to prenatal morphine exposure in adult male rats. Neuroscience 126 (2004) 355-364
118. Scholz K.P., and Miller R.J. Inhibition of quantal transmitter release in the absence of calcium influx by a G protein-linked adenosine receptor at hippocampal synapses. Neuron 8 (1992) 1139-1150
119. Seri B., Garcia-Verdugo J.M., McEwen B.S., and Alvarez-Buylla A. Astrocytes give rise to new neurons in the adult mammalian hippocampus. J. Neurosci. 21 (2001) 7153-7160
120. Seward E.P., Chernevskaya N.I., and Nowycky M.C. Exocytosis in peptidergic nerve terminals exhibits two calcium-sensitive phases during pulsatile calcium entry. J. Neurosci. 15 (1995) 3390-3399
121. Shors T.J., Miesegaes G., Beylin A., Zhao M., Rydel T., and Gould E. Neurogenesis in the adult is involved in the formation of trace memories. Nature 410 (2001) 372-376
122. Shors T.J., Townsend D.A., Zhao M., Kozorovitskiy Y., and Gould E. Neurogenesis may relate to some but not all types of hippocampal-dependent learning. Hippocampus 12 (2002) 578-584
123. Shuster S.J., Riedl M., Li X.R., Vulchanova L., and Elde R. Stimulus-dependent translocation of kappa opioid receptors to the plasma membrane. J. Neurosci. 19 (1999) 2658-2664
124. Simmons M.L., and Chavkin C. Endogenous opioid regulation of hippocampal function. Int. Rev. Neurobiol. 39 (1996) 145-196
125. Simmons M.L., Terman G.W., Drake C.T., and Chavkin C. Inhibition of glutamate release by presynaptic kappa 1-opioid receptors in the guinea pig dentate gyrus. J. Neurophysiol. 72 (1994) 1697-1705
126. Simmons M.L., Terman G.W., Gibbs S.M., and Chavkin C. L-type calcium channels mediate dynorphin neuropeptide release from dendrites but not axons of hippocampal granule cells. Neuron 14 (1995) 1265-1272
127. Simonato M., and Romualdi P. Dynorphin and epilepsy. Prog. Neurobiol. 50 (1996) 557-583
128. Skyers P.S., Einheber S., Pierce J.P., and Milner T.A. Increased mu-opioid receptor labeling is found on inner molecular layer terminals of the dentate gyrus following seizures. Exp. Neurol. 179 (2003) 200-209
129. Slamberová R., Rimanoczy A., Bar N., Schindler C.J., and Vathy I. Density of mu-opioid receptors in the hippocampus of adult male and female rats is altered by prenatal morphine exposure and gonadal hormone treatment. Hippocampus 13 (2003) 461-471
130. Slowe S.J., Simonin F., Kieffer B., and Kitchen I. Quantitative autoradiography of mu-, delta- and kappa 1 opioid receptors in kappa-opioid receptor knockout mice. Brain Res. 818 (1999) 335-345
131. 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
132. Svingos A.L., Colago E.E.O., and Pickel V.M. Cellular sites for dynorphin activation of kappa-opioid receptors in the rat nucleus accumbens shell. J. Neurosci. 19 (1999) 1804-1813
133. Tanapat P., Hastings N.B., Reeves A.J., and Gould E. Estrogen stimulates a transient increase in the number of new neurons in the dentate gyrus of the adult female rat. J. Neurosci. 19 (1999) 5792-5801
134. Tempel A., and Zukin R.S. Neuroanatomical patterns of the mu, delta, and kappa opioid receptors of rat brain as determined by quantitative in vitro autoradiography. Proc. Natl. Acad. Sci. U.S.A. 84 (1987) 4308-4312
135. Terman G.W., Drake C.T., Simmons M.L., Milner T.A., and Chavkin C. Opioid modulation of recurrent excitation in the hippocampal dentate gyrus. J. Neurosci. 20 (2000) 4379-4388
136. Terman G.W., Wagner J.J., and Chavkin C. Kappa opioids inhibit induction of long-term potentiation in the dentate gyrus of the guinea pig hippocampus. J. Neurosci. 14 (1994) 4740-4747
137. Thureson-Klein A.K., and Klein R.L. Exocytosis from neuronal large dense-core vesicles. Int. Rev. Cytol. 121 (1990) 67-126
138. Tielen A.M., van Leeuwen F.W., and Lopes da Silva F.H. The localization of leucine-enkephalin immunoreactivity within the guinea pig hippocampus. Exp. Brain Res. 48 (1982) 288-295
139. Torres-Reveron, A., Khalid, S., Drake, C.T. and Milner, T.A. (2006a) Enkephalin and dynorphin immunoreactivities increase in the dorsal hippocampus in response to estrogens and colocalize with estrogen receptor beta in mossy fiber terminals. Program No. 724.6 2006. Neuroscience Meeting Planner Atlanta GA: Society for Neuroscience, 2006. Online.
140. Torres-Reveron, A., Khalid, S., Drake, C.T. and Milner, T.A. (2006b). Enkephalin-immunoreactivity colocalizes with estrogen receptor immunoreactivity in terminals and increases in proestrus and estrogen replaced female rats in the dorsal hippocampus. Program No. Tn-26 2006. Poster Session Abstracts St. Paul Minnesota. International Narcotics Research Conference.
141. Tortella F.C., Echevarria E., Robles L., Mosberg H.I., and Holaday J.W. Anticonvulsant effects of mu (DAGO) and delta (DPDPE) enkephalins in rats. Peptides 9 (1988) 1177-1181
142. Turlejski K., and Djavadian R. Life-long stability of neurons: a century of research on neurogenesis, neuronal death and neuron quantification in adult CNS. Prog. Brain Res. 136 (2002) 39-65
143. Unterwald E.M., Knapp C., and Zukin R.S. Neuroanatomical localization of kappa 1 and kappa 2 opioid receptors in rat and guinea pig brain. Brain Res. 562 (1991) 57-65
144. Velísek L., Stanton P.K., Moshé S.L., and Vathy I. Prenatal morphine exposure enhances seizure susceptibility but suppresses long-term potentiation in the limbic system of adult male rats. Brain Res. 869 (2000) 186-193
145. Verhage M., McMahon H.T., Ghijsen W.E.J.M., Boomsma F., Scholten G., Wiegant V.M., and Nicholls D.G. Differential release of amino acids, neuropeptides, and catecholamines from isolated nerve terminals. Neuron 6 (1991) 517-524
146. Vindrola O., Briones R., Asai M., and Fernandez Guardiola A. Amygdaloid kindling enhances the enkephalin content in rat brain. Neurosci. Lett. 21 (1981) 39-44
147. Wagner J.J., Caudle R.M., and Chavkin C. Kappa-opioids decrease excitatory transmission in the dentate gyrus of the guinea pig hippocampus. J. Neurosci. 12 (1992) 132-141
148. Wagner J.J., Caudle R.M., Neumaier J.F., and Chavkin C. Stimulation of endogenous opioid release displaces mu receptor binding in rat hippocampus. Neuroscience 37 (1990) 45-53
149. Wagner J.J., and Chavkin C. Endogenous opioids and LTP: another view. Neurochem. Int. 20 (1992) 457-460
150. Wagner J.J., Evans C.J., and Chavkin C. Focal stimulation of the mossy fibers releases endogenous dynorphins that bind kappa 1-opioid receptors in guinea pig hippocampus. J. Neurochem. 57 (1991) 333-343
151. Wagner J.J., Terman G.W., and Chavkin C. Endogenous dynorphins inhibit excitatory neurotransmission and block LTP induction in the hippocampus. Nature 363 (1993) 451-454
152. Weisskopf M.G., Zalutsky R.A., and Nicoll R.A. The opioid peptide dynorphin mediates heterosynaptic depression of hippocampal mossy fibre synapses and modulates long-term potentiation. Nature 362 (1993) 423-427
153. White J.D., Gall C.M., and McKelvy J.F. Proenkephalin is processed in a projection-specific manner in the rat central nervous system. Proc. Natl. Acad. Sci. U.S.A. 83 (1986) 7099-7103
154. 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
155. Wolozin B.L., and Pasternak G.W. Classification of multiple morphine and enkephalin binding sites in the central nervous system. Proc. Natl. Acad. Sci. U.S.A. 78 (1981) 6181-6185
156. Woolley C.S., and Schwartzkroin P.A. Hormonal effects on the brain. Epilepsia 39 Suppl 8 (1998) S2-S8
157. Xie C.W., Morrisett R.A., and Lewis D.V. Mu opioid receptor-mediated modulation of synaptic currents in dentate granule cells of rat hippocampus. J. Neurophysiol. 68 (1992) 1113-1120
158. Yasuda K., Raynor H., Kong C.D., Breder J., Takeda J., Reisine T., and Bell G.I. Cloning and functional comparison of kappa and delta opioid receptors from mouse brain. Proc. Natl. Acad. Sci. U.S.A. 90 (1993) 6736-6740
159. Yoshioka M., Matsumoto M., Togashi H., Smith C.B., and Saito H. Opioid receptor regulation of 5-hydroxytryptamine release from the rat hippocampus measured by in vivo microdialysis. Brain Res. 613 (1993) 74-79
160. Yuste R., and Tank D.W. Dendritic integration in mammalian neurons, a century after Cajal. Neuron 16 (1996) 701-716
161. Zadina J.E., Hackler L., Ge L.J., and Kastin A.J. A potent and selective endogenous agonist for the μ-opiate receptor. Nature 386 (1997) 499-502
162. Zakarian S., and Smyth D. Distribution of active and inactive forms of endorphins in rat pituitary and brain. Proc. Natl. Acad. Sci. U.S.A. 76 (1979) 5972-5976
163. Zakarian S., and Smyth D.G. Distribution of beta-endorphin-related peptides in rat pituitary and brain. Biochem. J. 202 (1982) 561-571
164. Zieglgänsberger W., French E.D., Siggins G.R., and Bloom F.E. Opioid peptides may excite hippocampal pyramidal neurons by inhibiting adjacent inhibitory interneurons. Science 205 (1979) 415-417
165. Zimprich A., Simon T., and Hollt V. Cloning and expression of an isoform of the rat mu opioid receptor (rMOR1B) which differs in agonist induced desensitization from rMOR1. FEBS Lett. 359 (1995) 142-146
166. Zukin R.S., Eghbali M., Olive D., Unterwald E.M., and Tempel A. Characterization and visualization of rat and guinea pig brain kappa opioid receptors: evidence for kappa 1 and kappa 2 opioid receptors. Proc. Natl. Acad. Sci. U.S.A. 85 (1988) 4061-4065