Alcohol potently modulates climbing fiber→purkinje neuron synapses: Role of metabotropic glutamate receptors

Journal of Neuroscience

Volumn 26, Issue 7, 2006, Pages 1906-1912

  Carta, Mario ^a,c   Mameli, Manuel ^a   Valenzuela, C Fernando ^a,b  

^a UNIVERSITY OF NEW MEXICO HEALTH SCIENCES CENTER   (United States)

^b UNIVERSITY OF NEW MEXICO SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF CAGLIARI   (Italy)

Author keywords

Cerebellum; Electrophysiology; Ethanol; Glutamate; Motor; Slice

Indexed keywords

ALCOHOL; METABOTROPIC RECEPTOR;

ALCOHOL BLOOD LEVEL; ANIMAL TISSUE; ARTICLE; BRAIN SLICE; CELL FUNCTION; CEREBELLUM; CEREBELLUM CORTEX; CLIMBING FIBER; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; ELECTROPHYSIOLOGY; EVOKED RESPONSE; EXCITATION; INFERIOR OLIVE; MALE; NERVE CELL PLASTICITY; NONHUMAN; PATCH CLAMP; POSTSYNAPTIC POTENTIAL; PRIORITY JOURNAL; PROTEIN FUNCTION; PURKINJE CELL; RAT; SYNAPSE;

ALANINE; ANIMALS; ASPARTIC ACID; DISEASE MODELS, ANIMAL; ETHANOL; LONG-TERM DEPRESSION (PHYSIOLOGY); MALE; NERVE FIBERS; PATCH-CLAMP TECHNIQUES; PURKINJE CELLS; QUINOXALINES; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, METABOTROPIC GLUTAMATE; SYNAPSES; XANTHENES;

EID: 33644558094     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4430-05.2006     Document Type: Article

References (64)

1. Autti-Ramo I, Autti T, Korkman M, Kettunen S, Salonen O, Valanne L (2002) MRI findings in children with school problems who had been exposed prenatally to alcohol. Dev Med Child Neurol 44:98-106.
2. Basile A, Hoffer B, Dunwiddie T (1983) Differential sensitivity of cerebellar Purkinje neurons to ethanol in selectively outbred lines of mice: maintenance in vitro independent of synaptic transmission. Brain Res 264:69-78.
3. Brenowitz SD, Regehr WG (2005) Associative short-term synaptic plasticity mediated by endocannabinoids. Neuron 45:419-431.
4. 2+ ion permeability and single-channel properties of the metabotropic slow EPSC of rat Purkinje neurons. J Neurosci 24:3563-3573.
5. Carta M, Ariwodola OJ, Weiner JL, Valenzuela CF (2003) Alcohol potently inhibits the kainate receptor-dependent excitatory drive of hippocampal interneurons. Proc Natl Acad Sci USA 100:6813-6818.
6. Carta M, Mameli M, Valenzuela CF (2004) Alcohol enhances GABAergic transmission to cerebellar granule cells via an increase in Golgi cell excitability. J Neurosci 24:3746-3751.
7. Cerminara NL, Rawson JA (2004) Evidence that climbing fibers control an intrinsic spike generator in cerebellar Purkinje cells. J Neurosci 24:4510-4517.
8. Coesmans M, Weber JT, De Zeeuw CI, Hansel C (2004) Bidirectional parallel fiber plasticity in the cerebellum under climbing fiber control. Neuron 44:691-700.
9. Coffin JM, Baroody S, Schneider K, O'Neill J (2005) Impaired cerebellar learning in children with prenatal alcohol exposure: a comparative study of eyeblink conditioning in children with ADHD and dyslexia. Cortex 41:389-398.
10. Criswell HE, Breese GR (2005) A conceptualization of integrated actions of ethanol contributing to its GABAmimetic profile: a commentary. Neuropsychopharmacology 30:1407-1425.
11. Diamond I, Messing RO (1994) Neurologic effects of alcoholism. West J Med 161:279-287.
12. Dinh-Zarr T, Goss C, Heitman E, Roberts I, DiGuiseppi C (2004) Interventions for preventing injuries in problem drinkers. Cochrane Database Syst Rev:CD001857.
13. Dzubay JA, Otis TS (2002) Climbing fiber activation of metabotropic glutamate receptors on cerebellar Purkinje neurons. Neuron 36:1159-1167.
14. Freund RK, Palmer MR (1997) Beta adrenergic sensitization of gamma-aminobutyric acid receptors to ethanol involves a cyclic AMP/protein kinase A second-messenger mechanism. J Pharmacol Exp Ther 280:1192-1200.
15. Galindo R, Zamudio P, Valenzuela C (2005) Alcohol is a potent stimulant of immature neuronal networks: implications for fetal alcohol spectrum disorder. J Neurochem 94:1500-1511.
16. + depolarization in cultured cerebellar Purkinje neurons. Brain Res 773:82-89.
17. Hall AC, Lieb WR, Franks NP (1994) Insensitivity of P-type calcium channels to inhalational and intravenous general anesthetics. Anesthesiology 81:117-123.
18. A receptor activity. Nat Neurosci 8:339-345.
19. Hansel C, Linden DJ (2000) Long-term depression of the cerebellar climbing fiber-Purkinje neuron synapse. Neuron 26:473-482.
20. Hansel C, Linden DJ, D'Angelo E (2001) Beyond parallel fiber LTD: the diversity of synaptic and non-synaptic plasticity in the cerebellum. Nat Neurosci 4:467-475.
21. Hendricson AW, Thomas MP, Lippmann MJ, Morrisett RA (2003) Suppression of L-type voltage-gated calcium channel-dependent synaptic plasticity by ethanol: analysis of miniature synaptic currents and dendritic calcium transients. J Pharmacol Exp Ther 307:550-558.
22. Hernandez LL, Valentine JD, Powell DA (1986) Ethanol enhancement of Pavlovian conditioning. Behav Neurosci 100:494-503.
23. Khaliq ZM, Raman IM (2005) Axonal propagation of simple and complex spikes in cerebellar Purkinje neurons. J Neurosci 25:454-463.
24. Kim SJ, Kim YS, Yuan JP, Petralia RS, Worley PF, Linden DJ (2003) Activation of the TRPC1 cation channel by metabotropic glutamate receptor mGluR1. Nature 426:285-291.
25. Kitazawa S, Kimura T, Yin PB (1998) Cerebellar complex spikes encode both destinations and errors in arm movements. Nature 392:494-497.
26. Klintsova AY, Cowell RM, Swain RA, Napper RM, Goodlett CR, Greenough WT (1998) Therapeutic effects of complex motor training on motor performance deficits induced by neonatal binge-like alcohol exposure in rats. I. Behavioral results. Brain Res 800:48-61.
27. Klintsova AY, Scamra C, Hoffman M, Napper RM, Goodlett CR, Greenough WT (2002) Therapeutic effects of complex motor training on motor performance deficits induced by neonatal binge-like alcohol exposure in rats: II. A quantitative stereological study of synaptic plasticity in female rat cerebellum. Brain Res 937:83-93.
28. Lee RS, Smith SS, Chapin JK, Shimizu N, Waterhouse BD, Maddus BN, Woodward DJ (1995) Effects of systemic and local ethanol on responses of rat cerebellar Purkinje neurons to iontophoretically applied norepinephrine and gamma-aminobutyric acid. Brain Res 687:12-21.
29. Lin AM, Freund RK, Hoffer BJ, Palmer MR (1994) Ethanol-induced depressions of cerebellar Purkinje neurons are potentiated by beta-adrenergic mechanisms in rat brain. J Pharmacol Exp Ther 271:1175-1180.
30. Llinas R, Sugimori M (1980a) Electrophysiological properties of in vitro Purkinje cell somata in mammalian cerebellar slices. J Physiol (Lond) 305:171-195.
31. Llinas R, Sugimori M (1980b) Electrophysiological properties of in vitro Purkinje cell dendrites in mammalian cerebellar slices. J Physiol (Lond) 305:197-213.
32. Lovinger DM, White G, Weight FF (1989) Ethanol inhibits NMDA-activated ion current in hippocampal neurons. Science 243:1721-1724.
33. Lovinger DM, White G, Weight FF (1990) NMDA receptor-mediated synaptic excitation selectively inhibited by ethanol in hippocampal slice from adult rat. J Neurosci 10:1372-1379.
34. Lu SM, Yeh HH (1999) Ethanol modulates AMPA-induced current responses of primary somatosensory cortical neurons. Neurochem Int 35:175-183.
35. + flux. J Gen Physiol 125:569-585.
36. Lyall V, Heck GL, Phan TH, Mummalaneni S, Malik SA, Vinnikova AK, Desimone JA (2005b) Ethanol modulates the VR-1 variant amiloride-insensitive salt taste receptor. II. Effect on chorda tympani salt responses. J Gen Physiol 125:587- 600.
37. Mameli M, Zamudio P, Carta M, Valenzuela C (2005a) Effect of ethanol on GABAergic transmission in cerebellar Purkinje neurons. Soc Neurosci Abstr 31:955.2.
38. Mameli M, Zamudio PA, Carta M, Valenzuela CF (2005b) Developmentally regulated actions of alcohol on hippocampal glutamatergic transmission. J Neurosci 25:8027- 8036.
39. Manzardo AM, Penick EC, Knop J, Nickel EJ, Hall S, Jensen P, Gabrielli Jr WF (2005) Developmental differences in childhood motor coordination predict adult alcohol dependence: proposed role for the cerebellum in alcoholism. Alcohol Clin Exp Res 29:353-357.
40. Minami K, Gereau RW, Minami M, Heinemann SF, Harris RA (1998) Effects of ethanol and anesthetics on type 1 and 5 metabotropic glutamate receptors expressed in Xenopus laevis oocytes. Mol Pharmacol 53:148-156.
41. Miyakawa T, Yagi T, Kitazawa H, Yasuda M, Kawai N, Tsuboi K, Niki H (1997) Fyn-kinase as a determinant of ethanol sensitivity: relation to NMDA-receptor function. Science 278:698-701.
42. Monsivais P, Clark BA, Roth A, Hausser M (2005) Determinants of action potential propagation in cerebellar Purkinje cell axons. J Neurosci 25:464-472.
43. Moykkynen T, Korpi ER, Lovinger DM (2003) Ethanol inhibits alpha-amino-3-hydyroxy-5-methyl-4-isoxazolepropionic acid (AMPA) receptor function in central nervous system neurons by stabilizing desensitization. J Pharmacol Exp Ther 306:546-555.
44. Mu J, Carden WB, Kurukulasuriya NC, Alexander GM, Godwin DW (2003) Ethanol influences on native T-type calcium current in thalamic sleep circuitry. J Pharmacol Exp Ther 307:197-204.
45. Netzeband JG, Gruol DL (1995) Modulatory effects of acute ethanol on metabotropic glutamate responses in cultured Purkinje neurons. Brain Res 688:105-113.
46. Overstreet LS, Pasternak JF, Colley PA, Slater NT, Trommer BL (1997) Metabotropic glutamate receptor mediated long-term depression in developing hippocampus. Neuropharmacology 36:831-844.
47. Roberto M, Madamba SG, Moore SD, Tallent MK, Siggins GR (2003) Ethanol increases GABAergic transmission at both pre- and postsynaptic sites in rat central amygdala neurons. Proc Natl Acad Sci USA 100:2053-2058.
48. Rogers J, Siggins GR, Schulman JA, Bloom FE (1980) Physiological correlates of ethanol intoxication tolerance, and dependence in rat cerebellar Purkinje cells. Brain Res 196:183-198.
49. Rogers J, Madamba SG, Staunton DA, Siggins GR (1986) Ethanol increases single unit activity in the inferior olivary nucleus. Brain Res 385:253-262.
50. Schmolesky MT, Weber JT, De Zeeuw CI, Hansel C (2002) The making of a complex spike: ionic composition and plasticity. Ann NY Acad Sci 978:359-390.
51. Schuckit MA (1994) Low level of response to alcohol as a predictor of future alcoholism. Am J Psychiatry 151:184-189.
52. + channels. J Pharmacol Exp Ther 309:987-994.
53. Siggins GR, French E (1979) Central neurons are depressed by iontophoretic and micropressure application of ethanol and tetrahydropapaveroline. Drug Alcohol Depend 4:239-243.
54. Sorensen S, Palmer M, Dunwiddie T, Hoffer B (1980) Electrophysiological correlates of ethanol-induced sedation in differentially sensitive lines of mice. Science 210:1143-1145.
55. Sullivan EV, Harding AJ, Pentney R, Dlugos C, Martin PR, Parks MH, Desmond JE, Chen SH, Pryor MR, De Rosa E, Pfefferbaum A (2003) Disruption of frontocerebellar circuitry and function in alcoholism. Alcohol Clin Exp Res 27:301-309.
56. Trevisani M, Smart D, Gunthorpe MJ, Tognetto M, Barbieri M, Campi B, Amadesi S, Gray J, Jerman JC, Brough SJ, Owen D, Smith GD, Randall AD, Harrison S, Bianchi A, Davis JB, Geppetti P (2002) Ethanol elicits and potentiates nociceptor responses via the vanilloid receptor-1. Nat Neurosci 5:546-551.
57. Trevisani M, Gazzieri D, Benvenuti F, Campi B, Dinh QT, Groneberg DA, Rigoni M, Emonds-Alt X, Creminon C, Fischer A, Geppetti P, Harrison S (2004) Ethanol causes inflammation in the airways by a neurogenic and TRPV1-dependent mechanism. J Pharmacol Exp Ther 309:1167-1173.
58. Valenzuela CF, Carta M, Mameli M (2005) Letter to the editor. Alcohol Clin Exp Res 29:1356-1357.
59. Walter HJ, Messing RO (1999) Regulation of neuronal voltage-gated calcium channels by ethanol. Neurochem Int 35:95-101.
60. Weber JT, De Zeeuw CI, Linden DJ, Hansel C (2003) Long-term depression of climbing fiber-evoked calcium transients in Purkinje cell dendrites. Proc Natl Acad Sci USA 100:2878-2883.
61. Weiner JL, Dunwiddie TV, Valenzuela CF (1999) Ethanol inhibition of synaptically evoked kainate responses in rat hippocampal CA3 pyramidal neurons. Mol Pharmacol 56:85-90.
62. Yang X, Criswell HE, Breese GR (2000) Ethanol modulation of gamma-aminobutyric acid (GABA)-mediated inhibition of cerebellar Purkinje neurons: relationship to GABAb receptor input. Alcohol Clin Exp Res 24:682-690.
63. Yuan JP, Kiselyov K, Shin DM, Chen J, Shcheynikov N, Kang SH, Dehoff MH, Schwarz MK, Seeburg PH, Muallem S, Worley PF (2003) Homer binds TRPC family channels and is required for gating of TRPC1 by IP3 receptors. Cell 114:777-789.
64. Zhu L, Strata P, Andjus PR (2005) Pharmacology of the metabotropic glutamate receptor mediated current at the climbing fiber to Purkinje cell synapse. Prog Brain Res 148:299-306.