Noradrenergic modulation of the parallel fiber-Purkinje cell synapse in mouse cerebellum

Neuropharmacology

Volumn 89, Issue , 2015, Pages 33-42

  Lippiello, Pellegrino ^a   Hoxha, Eriola ^b   Volpicelli, Floriana ^a,c   Lo Duca, Giuseppina ^b   Tempia, Filippo ^b   Miniaci, Maria Concetta ^a  

^a UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^b UNIVERSITY OF TURIN   (Italy)

^c INSTITUTE OF GENETICS AND BIOPHYSICS ADRIANO BUZZATI TRAVERSO   (Italy)

Author keywords

Cerebellum; Long term potentiation; Noradrenaline; Norepinephrine; Purkinje cell; Synaptic modulation; Synaptic transmission

Indexed keywords

BETA 2 ADRENERGIC RECEPTOR; CYCLIC AMP DEPENDENT PROTEIN KINASE; NORADRENALIN; ADRENERGIC RECEPTOR STIMULATING AGENT; ALPHA 1 ADRENERGIC RECEPTOR; ALPHA 2 ADRENERGIC RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CEREBELLUM CORTEX; CONTROLLED STUDY; ENZYME ACTIVATION; EVOKED CORTICAL RESPONSE; FACILITATION; FEMALE; LONG TERM DEPRESSION; LONG TERM POTENTIATION; MALE; MOUSE; NERVE CELL NETWORK; NERVE CELL PLASTICITY; NEUROMODULATION; NONHUMAN; NORADRENERGIC SYSTEM; PROTEIN EXPRESSION; PURKINJE CELL; SIGNAL TRANSDUCTION; SYNAPSE; ANIMAL; CEREBELLUM; CYTOLOGY; DOSE RESPONSE; DRUG EFFECTS; EXCITATORY POSTSYNAPTIC POTENTIAL; NERVE FIBER; PHYSIOLOGY;

ADRENERGIC AGONISTS; ANIMALS; CEREBELLUM; DOSE-RESPONSE RELATIONSHIP, DRUG; EXCITATORY POSTSYNAPTIC POTENTIALS; FEMALE; MALE; MICE; NERVE FIBERS; PURKINJE CELLS; RECEPTORS, ADRENERGIC, ALPHA-1; RECEPTORS, ADRENERGIC, ALPHA-2; SYNAPSES;

EID: 84907943461     PISSN: 00283908     EISSN: 18737064     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2014.08.016     Document Type: Article

References (66)

1. L.C. Abbott, and C. Sotelo Ultrastructural analysis of catecholaminergic innervation in weaver and normal mouse cerebellar cortices J. Comp. Neurol. 426 2000 316 329
2. A.S. Basile, and T.V. Dunwiddie Norepinephrine elicits both excitatory and inhibitory responses from Purkinje cells in the in vitro rat cerebellar slice Brain Res. 296 1984 15 25
3. A. Baude, E. Molnar, D. Latawiec, R.A. McIlhinney, and P. Somogyi Synaptic and nonsynaptic localization of the GluR1 subunit of the AMPA-type excitatory amino acid receptor in the rat cerebellum J. Neurosci. 14 1994 2830 2843
4. M.F. Bear, and W. Singer Modulation of visual cortical plasticity by acetylcholine and noradrenaline Nature 320 1986 172 176
5. P. Bickford Motor learning deficits in aged rats are correlated with loss of cerebellar noradrenergic function Brain Res. 620 1993 133 138
6. P. Bickford, C. Heron, D.A. Young, G.A. Gerhardt, and R. De La Garza Impaired acquisition of novel locomotor tasks in aged and norepinephrinedepleted F344 rats Neurobiol. Aging 13 1992 475 481
7. T.V. Bliss, and G.L. Collingridge A synaptic model of memory: long-term potentiation in the hippocampus Nature 361 1993 31 39
8. F.E. Bloom, B.J. Hoffer, and G.R. Siggins Studies on norepinephrine-containing afferents to Purkinje cells of art cerebellum. I. Localization of the fibers and their synapses Brain Res. 25 1971 501 521
9. M.R. Carey, and W.G. Regehr Noradrenergic control of associative synaptic plasticity by selective modulation of instructive signals Neuron 62 2009 112 122 10.1016/j.neuron.2009.02.022
10. M.C. Cartford, T. Gould, and P.C. Bickford A central role for norepinephrine in the modulation of cerebellar learning tasks Behav. Cogn. Neurosci. Rev. 3 2004 131 138
11. M.C. Cartford, C.A. Allgeier, and P.C. Bickford The effects of beta-noradrenergic receptor blockade on acquisition of eyeblink conditioning in 3-month-old F344 rats Neurobiol. Learn. Mem. 78 2002 246 257
12. H.U. Dodt, H. Pawelzik, and W. Zieglgänsberger Actions of noradrenaline on neocortical neurons in vitro Brain Res. 545 1991 307 311
13. H. Eichenbaum Learning from LTP: a comment on recent attempts to identify cellular and molecular mechanisms of memory Learn. Mem. 3 1996 61 73
14. J.A. Esteban, S.H. Shi, C. Wilson, M. Nuriya, R.L. Huganir, and R. Malinow PKA phosphorylation of AMPA receptor subunits controls synaptic trafficking underlying plasticity Nat. Neurosci. 6 2003 136 143
15. J.N. Gelinas, and P.V. Nguyen Beta-adrenergic receptor activation facilitates induction of a protein synthesis-dependent late phase of long-term potentiation J. Neurosci. 25 2005 3294 3303
16. J.N. Gelinas, J.L. Banko, L. Hou, N. Sonenberg, E.J. Weeber, E. Klann, and P.V. Nguyen ERK and mTOR signaling couple beta-adrenergic receptors to translation initiation machinery to gate induction of protein synthesis-dependent long-term potentiation J. Biol. Chem. 282 2007 27527 27535
17. T.J. Gould Beta-adrenergic involvement in acquisition vs. extinction of a classically conditioned eye blink response in rabbits Brain Res. 780 1998 174 177
18. D.C. Haggerty, V. Glykos, N.E. Adams, and F.E. Lebeau Bidirectional modulation of hippocampal gamma (20-80 Hz) frequency activity in vitro via alpha(α)- and beta(β)-adrenergic receptors (AR) Neuroscience 253 2013 142 154 10.1016/j.neuroscience.2013.08.028
19. M. Hirono, W. Matsunaga, T. Chimura, and K. Obata Developmental enhancement of alpha2- adrenoceptor-mediated suppression of inhibitory synaptic transmission onto mouse cerebellar Purkinje cells Neuroscience 156 2008 143 154 10.1016/j.neuroscience.2008.07.018
20. B.J. Hoffer, G.R. Siggins, and F.E. Bloom Studies on norepinephrine-containing afferents to Purkinje cells of rat cerebellum. II. Sensitivity of Purkinje cells to norepinephrine and related substances administered by microiontophoresis Brain Res. 25 1971 523 534
21. C.M. Holloway-Erickson, J.R. McReynolds, and C.K. McIntyre Memory-enhancing intra- basolateral amygdala infusions of clenbuterol increase Arc and CaMKIIα protein expression in the rostral anterior cingulate cortex Front. Behav. Neurosci. 6 2012 17 10.3389/fnbeh.2012.00017
22. Y.Y. Huang, and E.R. Kandel Modulation of both the early and the late phase of mossy fiber LTP by the activation of beta-adrenergic receptors Neuron 16 1996 611 617
23. Y. Izumi, and C.F. Zorumski Norepinephrine promotes long-term potentiation in the adult rat hippocampus in vitro Synapse 31 1999 196 202
24. X.H. Ji, J.Z. Ji, H. Zhang, and B.M. Li Stimulation of alpha2-adrenoceptors suppresses excitatory synaptic transmission in the medial prefrontal cortex of rat Neuropsychopharmacology 33 2008 2263 2271
25. M.L. Joiner, M.F. Lisé, E.Y. Yuen, A.Y. Kam, M. Zhang, D.D. Hall, Z.A. Malik, H. Qian, Y. Chen, J.D. Ulrich, A.C. Burette, R.J. Weinberg, P.Y. Law, A. El-Husseini, Z. Yan, and J.W. Hell Assembly of a beta2- adrenergic receptor-GluR1 signaling complex for localized cAMP signalling EMBO J. 29 2010 482 495 10.1038/emboj.2009.344
26. E.L. Keller, and M.J. Smith Suppressed visual adaptation of the vestibuloocular reflex in catecholamine-depleted cats Brain Res. 258 1983 323 327
27. M. Kobayashi Differential regulation of synaptic transmission by adrenergic agonists via protein kinase A and protein kinase C in layer V pyramidal neurons of rat cerebral cortex Neuroscience 146 2007 1772 1784
28. S. Kondo, and A. Marty Differential effects of noradrenaline on evoked, spontaneous and miniature IPSCs in rat cerebellar stellate cells J. Physiol. 509 1998 233 243
29. A. Konnerth, I. Llano, and C.M. Armstrong Synaptic currents in cerebellar Purkinje cells Proc. Natl. Acad. Sci. U. S. A. 87 1990 2662 2665
30. A.S. Leonard, and J.W. Hell Cyclic AMP-dependent protein kinase and protein kinase C phosphorylate N-methyl-D-aspartate receptors at different sites J. Biol. Chem. 272 1997 12107 12115
31. V. Lev-Ram, S.T. Wong, D.R. Storm, and R.Y. Tsien A new form of cerebellar long-term potentiation is postsynaptic and depends on nitric oxide but not cAMP Proc. Natl. Acad. Sci. U. S. A. 99 2002 8389 8393
32. A.M. Lin, R.K. Freund, and M.R. Palmer Ethanol potentiation of GABA-induced electrophysiological responses in cerebellum: requirement for catecholamine modulation Neurosci. Lett. 122 1991 154 158
33. Y.W. Lin, M.Y. Min, T.H. Chiu, and H.W. Yang Enhancement of associative long-term potentiation by activation of beta-adrenergic receptors at CA1 synapses in rat hippocampal slices J. Neurosci. 23 2003 4173 4181
34. I. Llano, and H.M. Gerschenfeld Beta-adrenergic enhancement of inhibitory synaptic activity in rat cerebellar stellate and Purkinje cells J. Physiol. 468 1993 201 224
35. H.Y. Man, Y. Sekine-Aizawa, and R.L. Huganir Regulation of {alpha} -amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid receptor trafficking through PKA phosphorylation of the Glu receptor 1 subunit Proc. Natl. Acad. Sci. U. S. A. 104 2007 3579 3584
36. T. Manabe, D.J. Wyllie, D.J. Perkel, and R.A. Nicoll Modulation of synaptic transmission and long-term potentiation: effects on paired pulse facilitation and EPSC variance in the CA1 region of the hippocampus J. Neurophysiol. 70 1993 1451 1459
37. H. Mitoma, and S. Konishi Monoaminergic long-term facilitation of GABA-mediated inhibitory transmission at cerebellar synapses Neuroscience 88 1999 871 883
38. H.C. Moises, and D.J. Woodward Potentiation of GABA inhibitory action in cerebellum by locus coeruleus stimulation Brain Res. 182 1980 327 344
39. J. Mori-Okamoto, Y. Namii, and J. Tatsuno Subtypes of adrenergic receptors and intracellular mechanisms involved in modulatory effects of noradrenaline on glutamate Brain Res. 539 1991 67 75
40. J. Mori-Okamoto, and J. Tatsuno Effects of noradrenaline on the responsiveness of cultured cerebellar neurons to excitatory amino acids Brain Res. 448 1988 259 271
41. A.L. Mueller, B.J. Hoffer, and T.V. Dunwiddie Noradrenergic responses in rat hippocampus: evidence for medication by alpha and beta receptors in the in vitro slice Brain Res. 214 1981 113 126
42. F. Naka, T. Shiga, M. Yaguchi, and N. Okado An enriched environment increases noradrenaline concentration in the mouse brain Brain Res. 924 2002 124 126
43. Z. Nusser, E. Mulvihill, P. Streit, and P. Somogyi Subsynaptic segregation of metabotropic and ionotropic glutamate receptors as revealed by immunogold localization Neuroscience 61 1994 421 427
44. M.C. Oh, V.A. Derkach, E.S. Guire, and T.R. Soderling Extrasynaptic membrane trafficking regulated by GluR1 Serine 845 phosphorylation primes AMPA receptors for long-term potentiation J. Biol. Chem. 281 2006 752 758
45. L. Olson, and K. Fuxe On the projections from the locus coeruleus noradrealine neurons: the cerebellar innervation Brain Res. 28 1971 165 171
46. R. Papay, R. Gaivin, A. Jha, D.F. McCune, J.C. McGrath, M.C. Rodrigo, P.C. Simpson, V.A. Doze, and D.M. Perez Localization of the mouse alpha1A-adrenergic receptor (AR) in the brain: alpha1AAR is expressed in neurons, GABAergic interneurons, and NG2 oligodendrocyte progenitors J. Comp. Neurol. 497 2006 209 222
47. R. Papay, R. Gaivin, D.F. McCune, B.R. Rorabaugh, W.B. Macklin, J.C. McGrath, and D.M. Perez Mousealpha1B-adrenergic receptor is expressed in neurons and NG2 oligodendrocytes J. Comp. Neurol. 478 2004 1 10
48. D.J. Perkel, S. Hestrin, P. Sah, and R.A. Nicoll Excitatory synaptic currents in Purkinje cells Proc. Biol. Sci. 241 1990 116 121
49. O. Pompeiano Noradrenergic influences on the cerebellar cortex: effects on vestibular reflexes under basic and adaptive conditions Otolaryngol. Head Neck Surg. 119 1998 93 105
50. 2-Adrenergic receptor supports prolonged theta tetanus-induced LTP J. Neurophysiol. 107 2012 2703 2712 10.1152/jn.00374.2011
51. B. Sacchetti, B. Scelfo, F. Tempia, and P. Strata Long-term synaptic changes induced in the cerebellar cortex by fear conditioning Neuron 42 2004 973 982
52. F. Saitow, S. Satake, J. Yamada, and S. Konishi beta-adrenergic receptor-mediated presynaptic facilitation of inhibitory GABAergic transmission at cerebellar interneuron-Purkinje cell synapses J. Neurophysiol. 84 2000 2016 2025
53. W. Schultz, and A. Dickinson Neuronal coding of prediction errors Annu. Rev. Neurosci. 23 2000 473 500
54. N. Schweighofer, K. Doya, and S. Kuroda Cerebellar aminergic neuromodulation: towards a functional understanding Brain Res. Brain Res. Rev. 44 2004 103 116
55. B.S. Skalhegg, and K. Tasken Specificity in the cAMP/PKA signaling pathway. Differential expression, regulation, and subcellular localization of subunits of PKA Front. Biosci. 5 2000 D678 D693
56. V.A. Skeberdis, V. Chevaleyre, C.G. Lau, J.H. Goldberg, D.L. Pettit, S.O. Suadicani, Y. Lin, M.V. Bennett, R. Yuste, P.E. Castillo, and R.S. Zukin Protein kinase A regulates calcium permeability of NMDA receptors Nat. Neurosci. 9 2006 501 510
57. T. Straube, and J.U. Frey Involvement of beta-adrenergic receptors in protein synthesis-dependent late long-term potentiation (LTP) in the dentate gyrus of freely moving rats: the critical role of the LTP induction strength Neuroscience 119 2003 473 479
58. S.S. Taylor, R. Ilouz, P. Zhang, and A.P. Kornev Assembly of allosteric macromolecular switches: lessons from PKA Nat. Rev. Mol. Cell Biol. 13 2012 646 658 10.1038/nrm3432
59. F. Tempia, M.C. Miniaci, D. Anchisi, and P. Strata Postsynaptic current mediated by metabotropic glutamate receptors in cerebellar Purkinje cells J. Neurophysiol. 80 1998 520 528
60. M.J. Thomas, T.D. Moody, M. Makhinson, and T.J. O'Dell Activity-dependent beta-adrenergic modulation of low frequency stimulation induced LTP in the hippocampal CA1 region Neuron 17 1996 475 482
61. D.J. Wang, L.D. Su, Y.N. Wang, D. Yang, C.L. Sun, L. Zhou, X.X. Wang, and Y. Shen Long-term potentiation at cerebellar parallel fiber-Purkinje cell synapses requires presynaptic and postsynaptic signaling cascades J. Neurosci. 34 2014 2355 2364 10.1523/JNEUROSCI.4064-13.2014
62. M. Watson, and J.G. McElligott Cerebellar norepinephrine depletion and impaired acquisition of specific locomotor tasks in rats Brain Res. 296 1984 129 138
63. F. Yi, S.S. Liu, F. Luo, X.H. Zhang, and B.M. Li Signaling mechanism underlying α2A -adrenergic suppression of excitatory synaptic transmission in the medial prefrontal cortex of rats Eur. J. Neurosci. 38 2013 2364 2373 10.1111/ejn.12257
64. 2-adrenoceptor enhances synaptic potentiation and behavioral memory via cAMP-PKA signaling in the medial prefrontal cortex of rats Learn. Mem. 20 2013 274 284 10.1101/lm.030411.113
65. Y.D. Zhou, T.J. Turner, and K. Dunlap Enhanced G protein-dependent modulation of excitatory synaptic transmission in the cerebellum of the Ca2+ channel-mutant mouse, tottering J. Physiol. 547 2003 497 507
66. L. Zhu, B. Scelfo, N.A. Hartell, P. Strata, and B. Sacchetti The effects of fear conditioning on cerebellar LTP and LTD Eur. J. Neurosci. 26 2007 219 227