Activity-dependent release and actions of endocannabinoids in the rat hypothalamic supraoptic nucleus

Journal of Physiology

Volumn 569, Issue 3, 2005, Pages 751-760

  Di, Shi ^a   Boudaba, Cherif ^a   Popescu, Ion R ^a   Weng, Feng Ju ^a   Harris, Christina ^a   Marcheselli, Victor L ^b   Bazan, Nicolas G ^b   Tasker, Jeffrey G ^a,c  

^a Tulane University   (United States)

^b LOUISIANA STATE UNIVERSITY HEALTH SCIENCES CENTER   (United States)

^c TULANE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 ARACHIDONOYLGLYCEROL; ANANDAMIDE; ENDOCANNABINOID; GLUCOCORTICOID; GLUTAMIC ACID; CANNABINOID 1 RECEPTOR;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DENDRITE; HYPOTHALAMUS; HYPOTHALAMUS PERIVENTRICULAR NUCLEUS; MAGNOCELLULAR NUCLEUS; MALE; NERVE CELL EXCITABILITY; NEUROENDOCRINE SYSTEM; NEUROSECRETORY CELL; NEUROTRANSMITTER RELEASE; NONHUMAN; PRIORITY JOURNAL; RAT; SUPRAOPTIC NUCLEUS; SYNAPSE; ANIMAL CELL; ANIMAL EXPERIMENT; EVOKED RESPONSE; EXCITATORY POSTSYNAPTIC POTENTIAL; FIRING RATE; GLUTAMATERGIC SYNAPSE; NEUROMODULATION; POSTSYNAPTIC INHIBITION; RETROGRADE NERVE FIBER TRANSPORT; WHOLE CELL PATCH CLAMP;

ANIMALS; ARACHIDONIC ACIDS; BENZYL COMPOUNDS; CANNABINOIDS; ENDOCANNABINOIDS; EXCITATORY POSTSYNAPTIC POTENTIALS; GLUTAMIC ACID; GLYCERIDES; MALE; MORPHOLINES; NAPHTHALENES; NEURONS; PIPERIDINES; POLYUNSATURATED ALKAMIDES; PRESYNAPTIC TERMINALS; PYRAZOLES; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR, CANNABINOID, CB1; RECEPTORS, PRESYNAPTIC; SUPRAOPTIC NUCLEUS; SYNAPTIC TRANSMISSION;

EID: 29244455027     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2005.097477     Document Type: Article

References (56)

1. Alger BE (2002). Retrograde signaling in the regulation of synaptic transmission: focus on endocannabinoids. Prog Neurobiol 68, 247-286.
2. Ames F (1958). A clinical and metabolic study of acute intoxication with Cannabis sativa and its role in the model psychoses. J Ment Sci 104, 972-999.
3. Armstrong WE & Stern JE (1997). Electrophysiological and morphological characteristics of neurons in perinuclear zone of supraoptic nucleus. J Neurophysiol 78, 2427-2437.
4. Boudaba C, Linn DM, Halmos KC & Tasker JG (2003). Increased tonic activation of presynaptic metabotropic glutamate receptors in the rat supraoptic nucleus following chronic dehydration. J Physiol 551, 815-823.
5. Boudaba C, Schrader LA & Tasker JG (1997). Physiological evidence for local excitatory synaptic circuits in the rat hypothalamus. J Neurophysiol 77, 3396-3400.
6. Bourque CW (1998). Osmoregulation of vasopressin neurons: a synergy of intrinsic and synaptic processes. Prog Brain Res 119, 59-76.
7. Bourque CW & Richard D (2001). Axonal projections from the organum vasculosum lamina terminalis to the supraoptic nucleus: functional analysis and presynaptic modulation. Clin Exp Pharmacol Physiol 28, 570-574.
8. Brown SP, Brenowitz SD & Regehr WG (2003). Brief presynaptic bursts evoke synapse-specific retrograde inhibition mediated by endogenous cannabinoids. Nat Neurosci 6, 1048-1057.
9. Brown TT & Dobs AS (2002). Endocrine effects of marijuana. J Clin Pharmacol 42, 90S-96S.
10. Brown SP, Safo PK & Regehr WG (2004). Endocannabinoids inhibit transmission at granule cell to Purkinje cell synapses by modulating three types of presynaptic calcium channels. J Neurosci 24, 5623-5631.
11. Davies SN, Pertwee RG & Riedel G (2002). Functions of cannabinoid receptors in the hippocampus. Neuropharmacology 42, 993-1007.
12. Di S, Malcher-Lopes R, Halmos KC & Tasker JG (2003). Nongenomic glucocorticoid inhibition via endocannabinoid release in the hypothalamus: a fast feedback mechanism. J Neurosci 23, 4850-4857.
13. Di S, Malcher-Lopes R, Marcheselli VL, Bazan NG & Tasker JG (2005). Rapid glucocorticoid-mediated endocannabinoid release and opposing regulation of glutamate and GABA inputs to hypothalamic magnocellular neurons. Endocrinology 146, 4292-4301.
14. Di S & Tasker JG (2004). Dehydration-induced synaptic plasticity in magnocellular neurons of the hypothalamic supraoptic nucleus. Endocrinology 145, 5141-5149.
15. Freund TF, Katona I & Piomelli D (2003). Role of endogenous cannabinoids in synaptic signaling. Physiol Rev 83, 1017-1066.
16. Hajos N, Ledent C & Freund TF (2001). Novel cannabinoid-sensitive receptor mediates inhibition of glutamatergic synaptic transmission in the hippocampus. Neuroscience 106, 1-4.
17. Hatton GI (1997). Function-related plasticity in hypothalamus. Annu Rev Neurosci 20, 375-397.
18. Hirasawa M, Schwab Y, Natah S, Hillard CJ, Mackie K, Sharkey KA & Pittman QJ (2004). Dendritically released transmitters cooperate via autocrine and retrograde actions to inhibit afferent excitation. J Physiol 559, 611-624.
19. Howlett AC, Breivogel CS, Childers SR, Deadwyler SA, Hampson RE & Porrino Q (2004). Cannabinoid physiology and pharmacology: 30 years of progress. Neuropharmacology 47 (Suppl. 1), 345-358.
20. Inenaga K, Honda E, Hirakawa T, Nakamura S & Yamashita H (1998). Glutamatergic synaptic inputs to mouse supraoptic neurons in calcium-free medium in vitro. J Neuroendocrinol 10, 1-7.
21. Israel JM, Le Masson G, Theodosis DT & Poulain DA (2003). Glutamatergic input governs periodicity and synchronization of bursting activity in oxytocin neurons in hypothalamic organotypic cultures. Eur J Neurosci 17, 2619-2629.
22. Iversen L (2003). Cannabis and the brain. Brain 126, 1252-1270.
23. Kaneko M & Takahashi T (2004). Presynaptic mechanism underlying cAMP-dependent synaptic potentiation. J Neurosci 24, 5202-5208.
24. Kim J, Isokawa M, Ledent C & Alger BE (2002). Activation of muscarinic acetylcholine receptors enhances the release of endogenous cannabinoids in the hippocampus. J Neuroscience 22, 10182-10191.
25. Kombian SB, Hirasawa M, Mouginot D, Chen X & Pittman QJ (2000). Short-term potentiation of miniature excitatory synaptic currents causes excitation of supraoptic neurons. J Neurophysiol 83, 2542-2553.
26. Kreitzer AC & Regehr WG (2001). Retrograde inhibition of presynaptic calcium influx by endogenous cannabinoids at excitatory synapses onto Purkinje cells. Neuron 29, 717-727.
27. Lambert RC, Moos FC & Richard P (1993). Action of endogenous oxytocin within the paraventricular or supraoptic nuclei: a powerful link in the regulation of the bursting pattern of oxytocin neurons during the milk-ejection reflex in rats. Neuroscience 57, 1027-1038.
28. Maejima T, Hashimoto K, Yoshida T, Aiba A & Kano M (2001a). Presynaptic inhibition caused by retrograde signal from metabotropic glutamate to cannabinoid receptors. Neuron 31, 463-475.
29. Maejima T, Ohno-Shosaku T & Kano M (2001b). Endogenous cannabinoid as a retrograde messenger from depolarized postsynaptic neurons to presynaptic terminals. Neurosci Res 40, 205-210.
30. Melis M, Pistis M, Perra S, Muntoni AL, Pillolla G & Gessa GL (2004). Endocannabinoids mediate presynaptic inhibition of glutamatergic transmission in rat ventral tegmental area dopamine neurons through activation of CB1 receptors. J Neurosci 24, 53-62.
31. Miyata S, Nakashima T & Kiyohara T (1994). Structural dynamics of neural plasticity in the supraoptic nucleus of the rat hypothalamus during dehydration and rehydration. Brain Res Bull 34, 169-175.
32. Mueller NK, Di S, Paden CM & Herman JP (2005). Activity-dependent modulation of neurotransmitter innervation to vasopressin neurons of the supraoptic nucleus. Endocrinology 146, 348-354.
33. Murphy LL, Munoz RM, Adrian BA & Villanua MA (1998). Function of cannabinoid receptors in the neuroendocrine regulation of hormone secretion. Neurobiol Dis 5, 432-446.
34. Neher E (1992). Correction for liquid junction potentials in patch clamp experiments. Meth Enzymol 207, 123-131.
35. Ohno-Shosaku T, Maejima T & Kano M (2001). Endogenous cannabinoids mediate retrograde signals from depolarized postsynaptic neurons to presynaptic terminals. Neuron 29, 729-738.
36. Ohno-Shosaku T, Tsubokawa H, Mizushima I, Yoneda N, Zimmer A & Kano M (2002). Presynaptic cannabinoid sensitivity is a major determinant of depolarization-induced retrograde suppression at hippocampal synapses. J Neurosci 22, 3864-3872.
37. Oliet SH, Piet R & Poulain DA (2001). Control of glutamate clearance and synaptic efficacy by glial coverage of neurons. Science 292, 923-926.
38. Pertwee RG & Ross RA (2002). Cannabinoid receptors and their ligands. Prostagland Leukotr Essent Fatty Acids 66, 101-121.
39. Puder M, Weidenfeld J, Chowers I, Nir I, Conforti N & Siegel RA (1982). Corticotrophin and corticosterone secretion following Δ1-tetrahydrocannabinol, in intact and in hypothalamic deafferentated male rats. Exp Brain Res 46, 85-88.
40. Robbe D, Alonso G, Duchamp F, Bockaert J & Manzoni OJ (2001). Localization and mechanisms of action of cannabinoid receptors at the glutamatergic synapses of the mouse nucleus accumbens. J Neurosci 21, 109-116.
41. Sofia RD, Knobloch LC, Harakal JJ & Erikson DJ (1977). Comparative diuretic activity of Δ9-tetrahydrocannabinol, cannabidiol, cannabinol and hydrochlorothiazide in the rat. Arch Int Pharmacodyn Ther 225, 77-87.
42. Stella N, Schweitzer P & Piomelli D (1997). A second endogenous cannabinoid that modulates long-term potentiation. Nature 388, 773-778.
43. Stern JE, Hestrin S & Armstrong WE (2000). Enhanced neurotransmitter release at glutamatergic synapses on oxytocin neurones during lactation in the rat. J Physiol 526, 109-114.
44. Tasker JG & Dudek FE (1991). Electrophysiological properties of neurones in the region of the paraventricular nucleus in slices of rat hypothalamus. J Physiol 434, 271-293.
45. Theodosis DT (2002). Oxytocin-secreting neurons: a physiological model of morphological neuronal and glial plasticity in the adult hypothalamus. Front Neuroendocrinol 23, 101-135.
46. Theodosis DT & Poulain DA (2001). Maternity leads to morphological synaptic plasticity in the oxytocin system. Prog Brain Res 133, 49-58.
47. Tyrey L & Murphy LL (1984). Effects of delta-9-tetrahydrocannabinol on reproductive neuroendocrine function in the female: animal studies. NIDA Res Monogr 55, 42-51.
48. Tyrey L & Murphy LL (1988). Inhibition of suckling-induced milk ejections in the lactating rat by delta 9-tetrahydrocannabinol. Endocrinology 123, 469-472.
49. Varma N, Carlson GC, Ledent C & Alger BE (2001). Metabotropic glutamate receptors drive the endocannabinoid system in hippocampus. J Neurosci 21, RC188.
50. Wenger T, Jamali KA, Juaneda C, Leonardelli I & Tramu G (1997). Arachidonyl ethanolamide (anandamide) activates the parvocellular part of hypothalamic paraventricular nucleus. Biochem Biophys Res Commun 237, 724-728.
51. Wenger T, Ledent C & Tramu G (2003). The endogenous cannabinoid, anandamide, activates the hypothalamo-pituitary-adrenal axis in CB1 cannabinoid receptor knockout mice. Neuroendocrinology 78, 294-300.
52. Wenger T & Moldrich G (2002). The role of endocannabinoids in the hypothalamic regulation of visceral function. Prostaglandins Leukot Essent Fatty Acids 66, 301-307.
53. Wilson RI, Kunos G & Nicoll RA (2001). Presynaptic specificity of endocannabinoid signaling in the hippocampus. Neuron 31, 453-462.
54. Wilson RI & Nicoll RA (2001). Endogenous cannabinoids mediate retrograde signalling at hippocampal synapses. Nature 410, 588-592.
55. Yoshida T, Hashimoto K, Zimmer A, Maejima T, Araishi K & Kano M (2002). The cannabinoid CB1 receptor mediates retrograde signals for depolarization-induced suppression of inhibition in cerebellar Purkinje cells. J Neurosci 22, 1690-1697.
56. Zhuang SY, Bridges D, Grigorenko E, McCloud S, Boon A, Hampson RE & Deadwyler SA (2005). Cannabinoids produce neuroprotection by reducing intracellular calcium release from ryanodine-sensitive stores. Neuropharmacology 48, 1086-1096.