Cannabinoid-induced presynaptic inhibition at the primary afferent trigeminal synapse of juvenile rat brainstem slices

Journal of Physiology

Volumn 555, Issue 1, 2004, Pages 85-96

  Liang, Ying Ching ^a   Huang, Chiung Chun ^a   Hsu, Kuei Sen ^a   Takahashi, Tomoyuki ^b  

^a NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

^b UNIVERSITY OF TOKYO   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

2,3 DIHYDRO 5 METHYL 3 (MORPHOLINOMETHYL) 6 (1 NAPHTHOYL)PYRROLO[1,2,3 DE][1,4]BENZOXAZINE; 5 (4 CHLORO 3 METHYLPHENYL) 1 (4 METHYLBENZYL) N (1,3,3 TRIMETHYLBICYCLO[2.2.1]HEPTAN 2 YL) 3 PYRAZOLECARBOXAMIDE; ANANDAMIDE; BARIUM ION; CADMIUM; CALCIUM CHANNEL N TYPE; CANNABINOID; CANNABINOID 1 RECEPTOR; GLUTAMIC ACID; OMEGA AGATOXIN; OMEGA CONOTOXIN GVIA; RIMONABANT; TETRODOTOXIN; CALCIUM CHANNEL L TYPE;

AFFERENT NERVE GROUP 1; AMPLITUDE MODULATION; ANALGESIA; ANIMAL CELL; ANIMAL TISSUE; ATTENUATION; BRAIN SLICE; BRAIN STEM; CONCENTRATION RESPONSE; CONTROLLED STUDY; DELTA NERVE FIBER; EXCITATORY POSTSYNAPTIC POTENTIAL; EXOCYTOSIS; HYPERPOLARIZATION; LATENT PERIOD; MALE; MANDIBULAR NERVE; MONOSYNAPTIC PATHWAY; NERVE ENDING; NERVE FIBER C; NERVE STIMULATION; NEUROTRANSMITTER RELEASE; NOCICEPTION; NONHUMAN; PRESYNAPTIC INHIBITION; PRIORITY JOURNAL; RAT; RECORDING; REVIEW; SENSORY NERVE; SYNAPSE; TRIGEMINAL NUCLEUS; ANIMAL EXPERIMENT; ARTICLE; ELECTROPHYSIOLOGY; JUVENILE ANIMAL; NERVE CELL; PRIMARY AFFERENT TRIGEMINAL SYNAPSE;

AFFERENT PATHWAYS; AGING; ANIMALS; BRAIN STEM; CANNABINOIDS; EXCITATORY POSTSYNAPTIC POTENTIALS; MALE; NEURAL INHIBITION; PRESYNAPTIC TERMINALS; RATS; RATS, SPRAGUE-DAWLEY; SYNAPSES; TRIGEMINAL NUCLEI;

EID: 1542269784     PISSN: 00223751     EISSN: None     Source Type: Journal    
DOI: 10.1113/jphysiol.2003.056986     Document Type: Review

References (60)

1. Ameri A (1999). The effects of cannabinoids on the brain. Prog Neurobiol 58, 315-348.
2. Ataka T, Kumamoto E, Shimoji K & Yoshimura M (2000). Baclofen inhibits more effectively C-afferent than Aδ-afferent glutamatergic transmission in substantia gelatinosa neurons of adult rat spinal cord slices. Pain 86, 273-282.
3. Auclair N, Otani S, Soubrie P & Crépel F (2000). Cannabinoids modulate synaptic strength and plasticity at glutamatergic synapses of rat prefrontal cortex pyramidal neurons. J Neurophysiol 83, 3287-3293.
4. 2+ channels governing generation of miniature and evoked excitatory synaptic currents in spinal laminae I and II. J Neurosci 18, 8740-8750.
5. Basbaum AI & Jessell TM (2000). The perception of pain. In Principles of Neural Science, 4th edn, ed. Kandel ER, Schwartz JH & Jessell TM, pp. 472-491. McGraw-Hill Companies, Columbus.
6. Calignano A, La Rana G, Giuffrida A & Piomelli D (1998). Control of pain initiation by endogenous cannabinoids. Nature 394, 277-281.
7. Chan PKY & Yung WH (1999). Inhibitory postsynaptic currents of rat substantia nigra pars reticulata neurons: role of GABA receptors and GABA uptake. Brain Res 838, 18-26.
8. Chen L & Huang LYM (1990). Ionic currents in retrogradely labeled trigeminothalamic neurons in slices of rat medulla. Neurosci Lett 110, 66-71.
9. Compton DR, Gold LH, Ward SJ, Balster RL & Martin BR (1992). Aminoalkylindole analogs: cannabimimetic activity of a class of compounds structurally distinct from delta 9-tetrahydrocannabinol. J Pharmacol Exp Ther 263, 1118-1126.
10. Dewey WL (1986). Cannabinoid pharmacology. Pharmacol Rev 38, 151-178.
11. 35S]GTPγS binding in the dorsal horn of the spinal cord of noninflamed and inflamed rats. Eur J Neurosci 12, 2079-2086.
12. Dubner R & Bennett GJ (1983). Spinal and trigeminal mechanisms of nociception. Ann Rev Neurosci 6, 381-418.
13. Edwards FA, Konnerth A, Sakmann B & Takahashi T (1989). A thin slice preparation for patch clamp recordings from neurones of the mammalian central nervous system. Pflugers Arch 414, 600-612.
14. Fox AP, Nowycky MC & Tsien RW (1987). Kinetic and pharmacological properties distinguishing three types of calcium currents in chick sensory neurones. J Physiol 394, 149-172.
15. Fulton BP (1997). Postnatal changes in conduction velocity and soma action potential paramaters of rat dorsal root ganglion neurones. Neurosci Lett 73, 125-130.
16. 1 cannabinoid receptor inhibits synaptic release of glutamate in rat dorsolateral striatum. J Neurophysiol 85, 468-471.
17. Grudt TJ & Williams JT (1994). Mu-opioid agonists inhibit spinal trigeminal substantia gelatinosa neurons in guinea pig and rat. J Neurosci 14, 1646-1654.
18. Hagiwara S, Miyazaki S, Moody W & Patlak J (1978). Blocking effects of barium and hydrogen ions on the potassium current during anomalous rectification in the starfish egg. J Physiol 279, 167-185.
19. Hamba M (1998). Stimulation-induced responses of the trigeminal caudal neurons in the brainstem preparation isolated from newborn rats. Brain Res 785, 66-74.
20. Hamba M, Hisamitsu H & Muro M (1992). Wind-up of tooth pulp-evoked responses and its suppression in rat trigeminal caudal neurons. Brain Res Bull 29, 883-889.
21. Hamba M & Onimaru H (1998). Newborn rat brainstem preparation with the trigeminal nerve attached for pain study. Brain Res Protoc 3, 7-13.
22. Hamba M, Onodera K & Takahashi T (2000). Long-term potentiation of primary afferent neurotransmission at trigeminal synapses of juvenile rats. Eur J Neurosci 12, 1128-1134.
23. A synaptic transmission in the hippocampus. J Neurosci 20, 2470-2479.
24. Hohmann AG & Herkenham M (1998). Regulation of cannabinoid and μ-opioid receptors in rat lumbar spinal cord following neonatal capsaicin treatment. Neurosci Lett 252, 13-16.
25. Hohmann AG, Martin WJ, Tsou K & Walker JM (1995). Inhibition of noxious stimulus-evoked activity of spinal cord dorsal horn neurons by the cannabinoid WIN 55,212-2. Life Sci 56, 2111-2118.
26. Hohmann AG, Tsou K & Walker JM (1999). Cannabinoid suppression of noxious heat-evoked activity in wide dynamic range neurons in the lumbar dorsal horn of the rat. J Neurophysiol 81, 575-583.
27. Hu JW, Dostrovsky JO & Sessle BJ (1981). Functional properties of neurons in cat trigeminal subnucleus caudalis (medullary dorsal horn). I. Responses to oral-facial noxious and nonnoxious stimuli and projections to thalamus and subnucleus oralis. J Neurophysiol 45, 173-192.
28. Huang CC & Hsu KS (1999). Protein tyrosine kinase is required for the induction of long-term potentiation in the rat hippocampus. J Physiol 520, 783-796.
29. Huang CC, Lo SW & Hsu KS (2001). Presynaptic mechanisms underlying cannabinoid inhibition of excitatory synaptic transmission in rat striatal neurons. J Physiol 532, 731-748.
30. Jennings EA, Vaughan CW & Christie MJ (2001). Cannabinoid actions on rat superficial medullary dorsal horn neurons in vitro. J Physiol 534, 805-812.
31. B receptor. Proc Natl Acad Sci U S A 98, 8054-8058.
32. Lèvènés C, Daniel H, Soubrie P & Crepel F (1998 . Cannabinoids decrease excitatory synaptic transmission and impair long-term depression in rat cerebellar Purkinje cells. J Physiol 510, 867-879.
33. Light AR & Perl ER (1979). Re-examination of the dorsal root projection to the spinal dorsal horn including observations on the differential termination of coarse and fine fibers. J Com Neurol 186, 117-131.
34. Luo C, Kumamoto E, Furue H, Chen J & Yoshimura M (2002a). Anandamide inhibits excitatory transmission to rat substantia gelatinosa neurons in a manner different from that of capsaicin. Neurosci Lett 321, 17-20.
35. Luo C, Kumamoto E, Furue H, Chen J & Yoshimura M (2002b). Nociceptin inhibits excitatory but not inhibitory transmission to substantia gelatinosa neurones of adult rat spinal cord. Neuroscience 109, 349-358.
36. Mao J, Price DD, Lu J, Keniston L & Mayer DJ (2000). Two distinctive antinociceptive systems in rats with pathological pain. Neurosci Lett 280, 13-16.
37. Martin WJ, Hohmann AG & Walker JM (1996). Suppression of noxious stimulus-evoked activity in the ventral posterolateral nucleus of the thalamus by a cannabinoid agonist: correlation between electrophysiological and antinociceptive effects. J Neurosci 16, 6601-6611.
38. Martin WJ, Lai NK, Patrick SL, Tsou K & Walker JM (1993). Antinociceptive actions of cannabinoids following intraventricular administration in rats. Brain Res 629, 300-304.
39. Martin WJ, Tsou K & Walker JM (1998). Cannabinoid receptor-mediated inhibition of the rat tail-flick reflex after microinjection into the rostral ventromedial medulla. Neurosci Lett 242, 33-36.
40. Morisset V & Urban L (2001). Cannabinoid-induced presynaptic inhibition of glutamatergic EPSCs in substantia gelatinosa neurons of the rat spinal cord. J Neurophysiol 86, 40-48.
41. Onodera K, Hamba M & Takahashi T (2000). Primary afferent synaptic responses recorded from trigeminal caudal neurons in a mandibular nerve-brainstem preparation of neonatal rats. J Physiol 524, 503-512.
42. Price TJ, Helesic G, Parghi D, Hargreaves KM & Flores CM (2003). The neuronal distribution of cannabinoid receptor type 1 in the trigeminal ganglion of the rat. Neuroscience 120, 155-162.
43. Rice ASC (2001). Cannabinoids and pain. Curr Opin Invest Drugs 2, 399-414.
44. 1 cannabinoid receptor isoforms. J Pharmacol Exp Ther 278, 871-878.
45. 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.
46. Sessle BJ (1987). The neurobiology of facial and dental pain: present knowledge, future directions. J Dent Res 66, 962-981.
47. Shen M & Thayer SA (1998). The cannabinoid agonist WIN55212-2 inhibits calcium channels by receptor-mediated and direct pathways in cultured rat hippocampal neurons. Brain Res 783, 77-84.
48. Shire D, Carillon C, Kaghad M, Calandra B, Rinaldi-Carmona M, Le Fur G, Caput D & Ferrara P (1995). An amino-terminal variant of the central cannabinoid receptor resulting from alternative splicing. J Biol Chem 270, 3726-3731.
49. Smith FL, Cichewicz D, Martin ZL & Welch SP (1998). The enhancement of morphine antinociception in mice by delta9-tetrahydrocannabinol. Pharmacol Biochem Behav 60, 559-566.
50. Stragman NM, Patrick SL, Hohmann AG, Tsou K & Walker JM (1998). Evidence for a role of endogenous cannabinoids in the modulation of acute and tonic pain sensitivity. Brain Res 813, 323-328.
51. Stragman NM & Walker JM (1999). Cannabinoid WIN 55,212-2 inhibits the activity-dependent facilitation of spinal nociceptive responses. J Neurophysiol 82, 472-477.
52. Sugimoto T, Fujiyoshi Y, He YF, Xiao C & Ichikawa H (1997). Trigeminal primary projection to the rat brain stem sensory trigeminal nuclear complex and surrounding structures revealed by anterograde transport of cholera toxin B subunit-conjugated and Bandeiraea simplicifolia isolectin B4-conjugated horseradish peroxidase. Neurosci Res 28, 361-371.
53. Sugiura Y, Lee CL & Perl ER (1986). Central projections of identified, unmyelinated (C) afferent fibers innervating mammalian skin. Science 234, 358-361.
54. Sullivan JM (1999). Mechanisms of cannabinoid receptor-mediated inhibition of synaptic transmission in cultured hippocampal pyramidal neurons. J Neurophysiol 82, 1286-1294.
55. B receptor. J Neurosci 18, 3138-3146.
56. Takahashi T & Momiyama A (1993). Different types of calcium channels mediate central synaptic transmission. Nature 366, 156-158.
57. Travagli RA (1996). Muscarine receptor activation in the substantia gelatinosa of the spinal trigeminal nucleus of the guinea pig. J Neurophysiol 76, 3817-3822.
58. 1 receptors in the rat central nervous system. Neuroscience 83, 393-411.
59. Twitchell W, Brown S & Mackie K (1997). Cannabinoids inhibit N- and P/Q-type calcium channels in cultured rat hippocampal neurons. J Neurophysiol 78, 43-50.
60. Vaughan CW, McGregor IS & Christie MJ (1999). Cannabinoid receptor activation inhibits GABAergic neurotransmission in rostral ventromedial medulla neurons in vitro. Br J Pharmacol 127, 935-940.