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Retrograde endocannabinoid inhibition of goldfish retinal cones is mediated by 2-arachidonoyl glycerol

Published online by Cambridge University Press:  26 June 2007

SHIH-FANG FAN  and
STEPHEN YAZULLA
SHIH-FANG FAN
Affiliation:
Department of Neurobiology and Behavior, Stony Brook University, Stony Brook, New York
STEPHEN YAZULLA
Affiliation:
Department of Neurobiology and Behavior, Stony Brook University, Stony Brook, New York
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Abstract

A functional role for retinal endocannabinoids has not been determined. We characterized retrograde suppression of membrane currents of goldfish cones in a retinal slice. Whole-cell recordings were obtained from cone inner segments under voltage clamp. IK(V) was elicited by a depolarizing pulse to +54 mV from a holding potential of −70 mV. A fifty-millisecond puff of saline with 70 mM KCl or Group I mGluR agonist DHPG was applied through a pipette directly at a mixed rod/cone (Mb) bipolar cell body. The amplitude of IK(V) decreased 25% compared to the pre-puff control. Retrograde suppression of IK(V) was blocked by CB1 receptor antagonist, SR141716A. The FAAH inhibitor URB597 had no effect on the suppression of IK(V), whereas nimesulide, a COX-2 inhibitor, prolonged the effects of the K+ puff 10-fold. Orlistat, a blocker of 2-AG synthesis, blocked the effect of the K+ puff. Group I mGluR activation of Gq/11 was demonstrated in that a puff with DHPG decreased IK(V) of cones by 32%, an effect blocked by SR141716A. The effect of DHPG was not blocked by the mGluR5 antagonist MPEP, indicating involvement of mGluR1. The suppressive effect of the K+ puff vanished in a Ca2+-free, 2 mM Co2+ saline. TMB-8 or ryanodine, blocked the effect of DHPG, but not that of the K+ puff, showing that calcium influx or release from intracellular stores could mediate retrograde release. We suggest that retrograde suppression of cone IK(V) is mediated by Ca2+-dependent release of 2-AG from Mb bipolar cell dendrites by separate mechanisms: (1) voltage-dependent, mimicked by the K+ puff, that may be activated by the depolarizing ON response to light; (2) voltage-independent, occurring under ambient illumination, mediated by tonic mGluR1 activation. The negative feedback of this latter mechanism could regulate tonic glutamate release from cones within narrow limits, regardless of ambient illumination.

Keywords

RetinaCannabinoidRetrograde transmissionPhotoreceptorGoldfish
Type
Research Article
Information
Visual Neuroscience , Volume 24 , Issue 3 , May 2007 , pp. 257 - 267
Copyright
© 2007 Cambridge University Press

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References

REFERENCES

Akopian, A., Johnson, J., Gabriel, R., Brecha, N. & Witkovsky, P. (2000). Somatostatin modulates voltage-gated K+ and Ca2+ currents in rod and cone photoreceptors of the salamander retina. Journal of Neuroscience 20, 929–936.Google Scholar
Alger, B.E. (2002). Retrograde signaling in the regulation of synaptic transmission: Focus on endocannabinoids. Progress in Neurobiology 68, 247–286.CrossRefGoogle Scholar
Auclair, N., Otani, S., Soubrie, P. & Crepel, F. (2000). Cannabinoids modulate synaptic strength and plasticity at glutamatergic synapses of rat prefrontal cortex pyramidal neurons. Journal of Neurophysiology 83, 3287–3293.Google Scholar
Balse, E., Tessier, L.H., Forster, V., Roux, M., Sahel, J.A. & Picaud, S. (2006). Glycine receptors in a population of adult mammalian cones. Journal of Physiology 571, 391–403.CrossRefGoogle Scholar
Barnes, S. & Bui, Q. (1991). Modulation of calcium-activated chloride current via pH-induced changes of calcium channel properties in cone photoreceptors. Journal of Neuroscience 11, 4015–4023.Google Scholar
Barnett-Norris, J., Lynch, D. & Reggio, P.H. (2005). Lipids, lipid rafts and caveolae: Their importance for GPCR signaling and their centrality to the endocannabinoid system. Life Science 77, 1629–1639.CrossRefGoogle Scholar
Begg, M., Pacher, P., Batkai, S., Osei-Hyiaman, D., Offertaler, L., Mo, F.M., Liu, J. & Kunos, G. (2005). Evidence for novel cannabinoid receptors. Pharmacology and Therapeutics 106, 133–145.CrossRefGoogle Scholar
Bonhaus, D.W., Chang, L.K., Kwan, J. & Martin, G.R. (1998). Dual activation and inhibition of adenylyl cyclase by cannabinoid receptor agonists: Evidence for agonist-specific trafficking of intracellular responses. Journal of Pharmacology and Experimental Therapeutics 287, 884–888.Google Scholar
Bradshaw, H.B. & Walker, J.M. (2005). The expanding field of cannabimimetic and related lipid mediators. British Journal of Pharmacology 144, 459–465.CrossRefGoogle Scholar
Breivogel, C.S., Griffin, G., DiMarzo, V. & Martin, B.R. (2001). Evidence for a new G protein-coupled cannabinoid receptor in mouse brain. Molecular Pharmacology 60, 155–163.Google Scholar
Buckley, N.E., Hansson, S., Harta, G. & Mezey, É. (1998). Expression of the CB1 and CB2 receptor messenger RNAs during embryonic development in the rat. Neuroscience 82, 1131–1149.Google Scholar
Chaperon, F. & Thiébot, M.H. (1999). Behavioral effects of cannabinoid agents in animals. Critical Reviews in Neurobiology 13, 243–281.CrossRefGoogle Scholar
Chen, J., Matias, I., Dinh, T., Lu, T., Venezia, S., Nieves, A., Woodward, D.F. & Di, M.V. (2005). Finding of endocannabinoids in human eye tissues: Implications for glaucoma. Biochemical and Biophysical Research Communications 330, 1062–1067.CrossRefGoogle Scholar
Christie, M.J. & Vaughan, C.W. (2001). Cannabinoids act backwards. Nature 410, 527–530.CrossRefGoogle Scholar
Consroe, P., Musty, R., Rein, J., Tillery, W. & Pertwee, R.G. (1997). The perceived effects of smoked cannabis on patients with multiple sclerosis. European Neurology 38, 44–48.Google Scholar
Cravatt, B.F., Demarest, K., Patricelli, M.P., Bracey, M.H., Giang, D.K., Martin, B.R. & Lichtman, A.H. (2001). Supersensitivity to anandamide and enhanced cannabinoid signaling in mice lacking fatty acid amide hydrolase. Proceedings of the National Academy of Science of the U.S.A. 98, 9371–9376.CrossRefGoogle Scholar
Dawson, W.W., Jimenez-Antillon, C.F., Perez, J.M. & Zeskind, J.A. (1977). Marijuana and vision—after ten years' use in Costa Rica. Investigative Ophthalmology & Visual Science 16, 689–699.Google Scholar
Deutsch, D.G. & Chin, S.A. (1993). Enzymatic synthesis and degradation of anandamide, a cannabinoid receptor agonist. Biochemical Pharmacology 46, 791–796.CrossRefGoogle Scholar
Devane, W.A., Hanus, L., Breuer, A., Pertwee, R.G., Stevenson, L.S., Griffin, G., Gibson, D., Mandelbaum, A., Etinger, A. & Mechoulam, R. (1992). Isolation and structure of a brain constituent that binds to the cannabinoid receptor. Science 258, 1946–1949.CrossRefGoogle Scholar
Diana, M.A. & Marty, A. (2004). Endocannabinoid-mediated short-term synaptic plasticity: Depolarization-induced suppression of inhibition (DSI) and depolarization-induced suppression of excitation (DSE). British Journal of Pharmacology 142, 9–19.CrossRefGoogle Scholar
Diaz-Laviada, I. & Ruiz-Llorente, L. (2005). Signal transduction activated by cannabinoid receptors. Mini Review Medicinal Chemistry 5, 619–630.CrossRefGoogle Scholar
Dinh, T.P., Carpenter, D., Leslie, F.M., Freund, T.F., Katona, I., Sensi, S.L., Kathuria, S. & Piomelli, D. (2002). Brain monoglyceride lipase participating in endocannabinoid inactivation. Proceedings of the National Academy of Science of the U.S.A. 99, 10819–10824.CrossRefGoogle Scholar
Edwards, D.A., Kim, J. & Alger, B.E. (2006). Multiple mechanisms of endocannabinoid response initiation in hippocampus. Journal of Neurophysiology 95, 67–75.Google Scholar
Fan, S.F. & Yazulla, S. (1999a). Modulation of voltage-gated K+ currents (IK(v)) in retinal bipolar cells by ascorbate is mediated by dopamine D1 receptors. Visual Neuroscience 16, 928–931.Google Scholar
Fan, S.F. & Yazulla, S. (1999b). Suppression of voltage-dependent K+ currents in retinal bipolar cells by ascorbate. Visual Neuroscience 16, 141–148.Google Scholar
Fan, S.F. & Yazulla, S. (2001). Dopamine depletion with 6-OHDA enhances dopamine D1 receptor modulation of potassium currents in retinal bipolar cells. Visual Neuroscience 18, 327–337.CrossRefGoogle Scholar
Fan, S.F. & Yazulla, S. (2003). Biphasic modulation of voltage-dependent currents of retinal cones by cannabinoid CB1 agonist, WIN 55212-2. Visual Neuroscience 20, 177–188.CrossRefGoogle Scholar
Fan, S.F. & Yazulla, S. (2004). Inhibitory interaction of cannabinoid CB1 receptor and dopamine D2 receptor agonists on voltage-gated currents of goldfish cones. Visual Neuroscience 21, 69–79.CrossRefGoogle Scholar
Fan, S.F. & Yazulla, S. (2005). Reciprocal inhibition of voltage-gated potassium currents (I K(V)) by activation of cannabinoid CB1 and dopamine D1 receptors in ON bipolar cells of goldfish retina. Visual Neuroscience 22, 55–63.CrossRefGoogle Scholar
Fride, E. (2002). Endocannabinoids in the central nervous system—an overview. Prostaglandins Leukotrienes and Essential Fatty Acids 66, 221–233.CrossRefGoogle Scholar
Galante, M. & Diana, M.A. (2004). Group I metabotropic glutamate receptors inhibit GABA release at interneuron-Purkinje cell synapses through endocannabinoid production. Journal of Neuroscience 24, 4865–4874.Google Scholar
Gawienowski, A.M., Chatterjee, D., Anderson, P.J., Epstein, D.L. & Grant, W.M. (1982). Effect of delta 9-tetrahydrocannabinol on monoamine oxidase activity in bovine eye tissues, in vitro. Investigative Ophthalmology Visual Science 22, 482–485.Google Scholar
Glaser, S.T., Deutsch, D.D., Studholme, K.M., Zimov, S. & Yazulla, S. (2005). Endocannabinoids in the intact retina: 3H-anandamide uptake, fatty acid amide hydrolase immunoreactivity and hydrolysis of anandamide. Visual Neuroscience 22, 693–705.CrossRefGoogle Scholar
Goparaju, S.K., Ueda, N., Taniguchi, K. & Yamamoto, S. (1999). Enzymes of porcine brain hydrolyzing 2-arachidonoylglycerol, an endogenous ligand of cannabinoid receptors. Biochemical Pharmacology 57, 417–423.CrossRefGoogle Scholar
Goparaju, S.K., Ueda, N., Yamaguchi, H. & Yamamoto, S. (1998). Anandamide amidohydrolase reacting with 2-arachidonoylglycerol, another cannabinoid receptor ligand. FEBS Letters 422, 69–73.CrossRefGoogle Scholar
Grant, G.B. & Dowling, J.E. (1996). On bipolar cell responses in the teleost retina are generated by two distinct mechanisms. Journal of Neurophysiology 76, 3842–3849.Google Scholar
Grueter, B.A., Gosnell, H.B., Olsen, C.M., Schramm-Sapyta, N.L., Nedrasova, T., Landreth, G.E. & Winder, D.G. (2006). Extracellular-signal regulated kinase1-dependent metabotropic glutamate receptor 5-induced long-term depression in the bed nucleus of the stria terminalis is disrupted by cocaine administration. Journal of Neuroscience 26, 3210–3219.Google Scholar
Hamill, O.P., Marty, A., Neher, E., Sakmann, B. & Sigworth, F.J. (1981). Improved patch-clamp techniques of high resolution current recording from cells and cell-free membrane patches. Pflugers Archives 391, 85–100.CrossRefGoogle Scholar
Harsanyi, K. & Mangel, S.C. (1993). Modulation of cone to horizontal cell transmission by calcium and pH in the fish retina. Visual Neuroscience 10, 81–91.CrossRefGoogle Scholar
Heinbockel, T., Brager, D.H., Reich, C.G., Zhao, J., Muralidharan, S., Alger, B.E. & Kao, J.P.Y. (2005). Endocannabinoid signaling dynamics probed with optical tools. Journal of Neuroscience 25, 9449–9459.CrossRefGoogle Scholar
Hohmann, A.G., Suplita, R.L., Bolton, N.M., Neely, M.H., Fegley, D., Mangieri, R., Krey, J.F., Walker, J.M., Holmes, P.V., Crystal, J.D., Duranti, A., Tontini, A., Mor, M., Tarzia, G. & Piomelli, D. (2005). An endocannabinoid mechanism for stress-induced analgesia. Nature 435, 1108–1112.CrossRefGoogle Scholar
Howlett, A.C., Breivogel, C.S., Childers, S.R., Deadwyler, S.A., Hampson, R.E. & Porrino, L.J. (2004). Cannabinoid physiology and pharmacology: 30 years of progress. Neuropharmacology 47 Suppl 1, 345–358.CrossRefGoogle Scholar
Ishida, A.T., Stell, W.K. & Lightfoot, D.O. (1980). Rod and cone inputs to bipolar cells in goldfish retina. Journal of Comparative Neurology 191, 315–335.CrossRefGoogle Scholar
Isokawa, M. & Alger, B.E. (2006). The ryanodine receptor regulates endogenous cannabinoid mobilization in the hippocampus. Journal of Neurophysiology 95, 3001–3011.CrossRefGoogle Scholar
Jung, K.M., Mangieri, R., Stapleton, C., Kim, J., Fegley, D., Wallace, M., Mackie, K. & Piomelli, D. (2005). Stimulation of endocannabinoid formation in brain slice cultures through activation of group I metabotropic glutamate receptors. Molecular Pharmacology 68, 1196–1202.CrossRefGoogle Scholar
Kamermans, M., Fahrenfort, I., Schultz, K., Janssen-Bienhold, U., Sjoerdsma, T. & Weiler, R. (2001). Hemichannel-mediated inhibition in the outer retina. Science 292, 1178–1180.CrossRefGoogle Scholar
Kim, J. & Alger, B.E. (2004). Inhibition of cyclooxygenase-2 potentiates retrograde endocannabinoid effects in hippocampus. Nature Neuroscience 7, 697–698.CrossRefGoogle Scholar
Kiplinger, G.F., Manno, J.E., Rodda, B.E. & Forney, R.B. (1971). Dose-response analysis of the effects of tetrahydrocannabinol in man. Clinical Pharmacology and Therapeutics 12, 650–657.CrossRefGoogle Scholar
Klooster, J., Studholme, K.M. & Yazulla, S. (2001). Localization of the AMPA subunit GluR2 in the outer plexiform layer of goldfish retina. Journal of Comparative Neurology 441, 155–167.CrossRefGoogle Scholar
Kourennyi, D.E., Liu, X., Hart, J., Mahmud, F., Baldridge, W.H. & Barnes, S. (2004). Reciprocal modulation of calcium dynamics at rod and cone photoreceptor synapses by nitric oxide. Journal of Neurophysiology 92, 477–483.CrossRefGoogle Scholar
Kozak, K.R., Rowlinson, S.W. & Marnett, L.J. (2000). Oxygenation of the endocannabinoid, 2-Arachidonoylglycerol, to glyceryl prostaglandins by cyclooxygenase-2. Journal of Biological Chemistry 275, 33744–33749.CrossRefGoogle Scholar
Kreitzer, A.C. & Regehr, W.G. (2001). Retrograde inhibition of presynaptic calcium influx by endogenous cannabinoids at excitatory synapses onto Purkinje cells. Neuron 29, 717–727.CrossRefGoogle Scholar
Kurreny, D.E., Moroz, L.L., Turner, R.W., Sharkey, K.A. & Barnes, S. (1994). Modulation of ion channels in rod photoreceptors by nitric oxide. Neuron 13, 315–324.CrossRefGoogle Scholar
Lauckner, J.E., Hille, B. & Mackie, K. (2005). The cannabinoid agonist WIN55,212-2 increases intracellular calcium via CB1 receptor coupling to Gq/11 G proteins. Proceedings of the National Academy of Sciences USA 102, 19144–19149.CrossRefGoogle Scholar
Lichtman, A.H., Hawkins, E.G., Griffin, G. & Cravatt, B.F. (2002). Pharmacological activity of fatty acids is regulated, but not mediated, by fatty acid amide hydrolase in vivo. Journal of Pharmacology & Experimental Therapeutics 302, 73–79.CrossRefGoogle Scholar
Maejima, T., Hashimoto, K., Yoshida, T., Aiba, A. & Kano, M. (2001). Presynaptic inhibition caused by retrograde signal from metabotropic glutamate to cannabinoid receptors. Neuron 31, 463–475.CrossRefGoogle Scholar
Maejima, T., Oka, S., Hashimotodani, Y., Ohno-Shosaku, T., Aiba, A., Wu, D., Waku, K., Sugiura, T. & Kano, M. (2005). Synaptically driven endocannabinoid release requires Ca2+-assisted metabotropic glutamate receptor subtype 1 to phospholipase Cbeta4 signaling cascade in the cerebellum. Journal of Neuroscience 25, 6826–6835.Google Scholar
Makara, J.K., Mor, M., Fegley, D., Szabo, S.I., Kathuria, S., Astarita, G., Duranti, A., Tontini, A., Tarzia, G., Rivara, S., Freund, T.F. & Piomelli, D. (2005). Selective inhibition of 2-AG hydrolysis enhances endocannabinoid signaling in hippocampus. Nature Neuroscience 8, 1139–1141.CrossRefGoogle Scholar
Marc, R.E. & Sperling, H.G. (1976). The chromatic organization of the goldfish cone mosaic. Vision Research 16, 1211–1224.CrossRefGoogle Scholar
Matsuda, S., Kanemitsu, N., Nakamura, A., Mimura, Y., Ueda, N., Kurahashi, Y. & Yamamoto, S. (1997). Metabolism of anandamide, an endogenous cannabinoid receptor ligand, in porcine ocular tissues. Experimental Eye Research 64, 707–711.CrossRefGoogle Scholar
McAllister, S.D. & Glass, M. (2002). CB1 and CB2 receptor-mediated signalling: A focus on endocannabinoids. Prostaglandins Leukotrienes and Essential Fatty Acids 66, 161–171.CrossRefGoogle Scholar
Mechoulam, R. (2002). Discovery of endocannabinoids and some random thoughts on their possible roles in neuroprotection and aggression. Prostaglandins Leukotrienes and Essential Fatty Acids 66, 93–99.CrossRefGoogle Scholar
Mechoulam, R., Ben-Shabat, S., Hanus, L., Ligumdky, M., Kaminski, N.E., Shatz, A.R., Gopher, A., Almog, S., Martin, B.R. & Compton, D.R. (1995). Identification of an endogenous 2-monoglyceride, present in canine gut, that binds to cannabinoid receptors. Biochemical Pharmacology 50, 83–90.CrossRefGoogle Scholar
Melis, M., Perra, S., Muntoni, A.L., Pillolla, G., Lutz, B., Marsicano, G., Di, M.V., Gessa, G.L. & Pistis, M. (2004). Prefrontal cortex stimulation induces 2-arachidonoyl-glycerol-mediated suppression of excitation in dopamine neurons. Journal of Neuroscience 24, 10707–10715.Google Scholar
Munro, S., Thomas, K.L. & Abu-Shaar, M. (1993). Molecular characterization of peripheral receptors for cannabinoids. Nature 365, 61–65.CrossRefGoogle Scholar
Narushima, M., Hashimoto, K. & Kano, M. (2006). Endocannabinoid-mediated short-term suppression of excitatory synaptic transmission to medium spiny neurons in the striatum. Neuroscience Research 54, 159–164.CrossRefGoogle Scholar
Ohno-Shosaku, T., Hashimotodani, Y., Maejima, T. & Kano, M. (2005). Calcium signaling and synaptic modulation: Regulation of endocannabinoid-mediated synaptic modulation by calcium. Cell Calcium 38, 369–374.CrossRefGoogle Scholar
Ohno-Shosaku, T., Maejima, T. & Kano, M. (2001). Endogenous cannabinoids mediate retrograde signals from depolarized postsynaptic neurons to presynaptic terminals. Neuron 29, 729–738.CrossRefGoogle Scholar
Ohno-Shosaku, T., Shosaku, J., Tsubokawa, H. & Kano, M. (2002). Cooperative endocannabinoid production by neuronal depolarization and group I metabotropic glutamate receptor activation. European Journal of Neuroscience 15, 953–961.CrossRefGoogle Scholar
Pertwee, R.G. & Ross, R.A. (2002). Cannabinoid receptors and their ligands. Prostaglandins Leukotrienes and Essential Fatty Acids 66, 101–121.CrossRefGoogle Scholar
Pertwee, R.G. (2005). Pharmacological actions of cannabinoids. Handbook of Experimental Pharmacology 168, 1–51.CrossRefGoogle Scholar
Picaud, S., Pattnaik, B., Hicks, D., Forster, V., Fontaine, V., Sahel, J. & Dreyfus, H. (1998). GABAA and GABAC receptors in adult porcine cones: Evidence from a photoreceptor-glia co-culture model. Journal of Physiology 513, 33–42.CrossRefGoogle Scholar
Piomelli, D., Giuffrida, A., Calignano, A. & deFonseca, F.R. (2000). The endocannabinoid system as a target for therapeutic drugs. Trends in Pharmacological Science 21, 218–224.CrossRefGoogle Scholar
Porcella, A., Casellas, P., Gessa, G.L. & Pani, L. (1998). Cannabinoid receptor CB1 mRNA is highly expressed in the rat ciliary body: Implications for the antiglaucoma properties of marihuana. Molecular Brain Research 58, 240–245.CrossRefGoogle Scholar
Russo, E.B., Merzouki, A., Mesa, J.M., Frey, K.A. & Bach, P.J. (2004). Cannabis improves night vision: A case study of dark adaptometry and scotopic sensitivity in kif smokers of the Rif mountains of northern Morocco. Journal of Ethnopharmacology 93, 99–104.CrossRefGoogle Scholar
Saario, S.M., Savinainen, J.R., Laitinen, J.T. & Niemi, R. (2004). Monoglyceride lipase-like enzymatic activity is responsible for hydrolysis of 2-arachidonoylglycerol in rat cerebellar membranes. Biochemical Pharmacology 67, 1381–1387.CrossRefGoogle Scholar
Sang, N., Zhang, J., Marcheselli, V., Bazan, N.G. & Chen, C. (2005). Postsynaptically synthesized prostaglandin E2 (PGE2) modulates hippocampal synaptic transmission via a presynaptic PGE2 EP2 receptor. Journal of Neuroscience 25, 9858–9870.Google Scholar
Sarker, K.P., Biswas, K.K., Yamakuchi, M., Lee, K.Y., Hahiguchi, T., Kracht, M., Kitajima, I. & Murayama, I. (2003). ASK1-p38 MAPK/JNK signaling cascade mediates anandamide-induced PC12 cell death. Journal of Neurochemistry 85, 50–61.CrossRefGoogle Scholar
Schlicker, E., Timm, J. & Göthert, M. (1996). Cannabinoid receptor-mediated inhibition of dopamine release in the retina. Naunyn-Schmiedebergs Archives of Pharmacology 354, 791–795.CrossRefGoogle Scholar
Sherry, D.M. & Yazulla, S. (1993). Goldfish bipolar cells and axon terminal patterns: A Golgi study. Journal of Comparative Neurology 329, 188–200.CrossRefGoogle Scholar
Skosnik, P.D., Krishnan, G.P., Vohs, J.L. & O'donnell, B.F. (2006). The effect of cannabis use and gender on the visual steady state evoked potential. Clinical Neurophysiology 117, 144–156.CrossRefGoogle Scholar
Slanina, K.A. & Schweitzer, P. (2005). Inhibition of cyclooxygenase-2 elicits a CB1-mediated decrease of excitatory transmission in rat CA1 hippocampus. Neuropharmacology 49, 653–659.CrossRefGoogle Scholar
Stamer, W.D., Golightly, S.F., Hosohata, Y., Ryan, E.P., Porter, A.C., Varga, E., Noecker, R.J., Felder, C.C. & Yamamura, H.I. (2001). Cannabinoid CB(1) receptor expression, activation and detection of endogenous ligand in trabecular meshwork and ciliary process tissues. European Journal of Pharmacology 431, 277–286.CrossRefGoogle Scholar
Stell, W.K. & Hárosi, F.I. (1976). Cone structure and visual pigment in the retina of the goldfish. Vision Research 16, 647–658.CrossRefGoogle Scholar
Stella, S.L., Bryson, E.J., Cadetti, L. & Thoreson, W.B. (2003). Endogenous adenosine reduces glutamatergic output from rods through activation of A(2)-like adenosine receptors. Journal of Neurophysiology 90, 165–174.CrossRefGoogle Scholar
Stella, S.L., Bryson, E.J. & Thoreson, W.B. (2002). A(2) adenosine receptors inhibit calcium influx through L-type calcium channels in rod photoreceptors of the salamander retina. Journal of Neurophysiology 87, 351–360.CrossRefGoogle Scholar
Straiker, A., Stella, N., Piomelli, D., Mackie, K., Karten, H.J. & Maguire, G. (1999). Cannabinoid CB1 receptors and ligands in vertebrate retina: Localization and function of an endogenous signaling system. Proceedings of the National Academy of Sciences of the U.S.A. 96, 14565–14570.CrossRefGoogle Scholar
Straiker, A. & Sullivan, J.M. (2003). Cannabinoid receptor activation differentially modulates ion channels in photoreceptors of the tiger salamander. Journal of Neurophysiology 89, 2647–2654.CrossRefGoogle Scholar
Struik, M., Yazulla, S. & Kamermans, M. (2006). Cannabinoid agonist WIN 55212-2 speeds up the cone light offset response in goldfish. Visual Neuroscience 23, 285–293.CrossRefGoogle Scholar
Sugiura, T., Kondo, S., Sukagawa, A., Nakane, S., Shinoda, A., Itoh, K., Yamashita, A. & Waku, K. (1995). 2-Arachidonoylglycerol: A possible endogenous cannabinoid receptor ligand in brain. Biochemical & Biophysical Research Communications 215, 89–97.CrossRefGoogle Scholar
Tachibana, M. & Kaneko, A. (1984). g-Aminobutyric acid acts at axon terminals of turtle photoreceptors: Difference in sensitivity among cell types. Proceedings of the National Academy of Science of the USA 81, 7961–7964.CrossRefGoogle Scholar
Toth, A., Boczan, J., Kedei, N., Lizanecz, E., Bagi, Z., Papp, Z., Edes, I., Csiba, L. & Blumberg, P.M. (2005). Expression and distribution of vanilloid receptor 1 (TRPV1) in the adult rat brain. Journal of Neuroscience Research 50, 1047–1052.Google Scholar
Vanderstelt, M. & Di Marzo, V. (2005). Cannabinoid receptors and their role in neuroprotection. Neuromolecular Medicine 7, 37–50.CrossRefGoogle Scholar
Varma, N., Carlson, G.C., Ledent, C. & Alger, B.E. (2001). Metabotropic glutamate receptors drive the endocannabinoid system in hippocampus. Journal of Neuroscience 21, RC188.Google Scholar
Verweij, J., Kamermans, M. & Spekreijse, H. (1996). Horizontal cells feed back to cones by shifting the cone calcium-current activation range. Vision Research 36, 3943–3953.CrossRefGoogle Scholar
Willoughby, K.A., Moore, S.F., Martin, B.R. & Ellis, E.F. (1997). The biodisposition and metabolism of anandamide in mice. Journal of Pharmacology & Experimental Therapeutics 282, 243–247.Google Scholar
Wilson, R.I. & Nicoll, R.A. (2001). Endogenous cannabinoids mediate retrograde signaling at hippocampal synapses. Nature 410, 588–592.CrossRefGoogle Scholar
Wong, K.Y., Cohen, E.D. & Dowling, J.E. (2004). Retinal Bipolar Cell Input Mechanisms in Giant Danio: II. Patch-Clamp Analysis of ON Bipolar Cells. Journal of Neurophysiology 93, 94–107.Google Scholar
Yazulla, S., Studholme, K.M., Fan, S.F. & Mora-Ferrer, C. (2001). Neuromodulation of voltage-dependent K+ channels in bipolar cells: Immunocytochemical and electrophysiological studies. Progress in Brain Research 131, 201–214.CrossRefGoogle Scholar
Yazulla, S., Studholme, K.M., McIntosh, H.H. & Deutsch, D.G. (1999). Immunocytochemical localization of cannabinoid CB1 receptor and fatty acid amide hydrolase in rat retina. Journal of Comparative Neurology 415, 80–90.3.0.CO;2-H>CrossRefGoogle Scholar
Yazulla, S., Studholme, K.M., McIntosh, H.H. & Fan, S.F. (2000). Cannabinoid receptors on goldfish retinal bipolar cells: Electron-microscope immunocytochemistry and whole-cell recordings. Visual Neuroscience 17, 391–401.CrossRefGoogle Scholar
Yu, M., Ives, D. & Ramesha, C.S. (1997). Synthesis of prostaglandin E2 ethanolamide from anandamide by cyclooxygenase-2. Journal of Biological Chemistry 272, 21181–21186.CrossRefGoogle Scholar
Zhu, P., Genc, A., Zhang, X., Zhang, J., Bazan, N.G. & Chen, C. (2005). Heterogeneous expression and regulation of PGE2 receptors in the hippocampus. Journal of Neuroscience Research 81, 817–826.CrossRefGoogle Scholar
Zhu, P.J. & Lovinger, D.M. (2005). Retrograde endocannabinoid signaling in a postsynaptic neuron/synaptic bouton preparation from basolateral amygdala. Journal of Neuroscience 25, 6199–6207.Google Scholar