Cerebellar aminergic neuromodulation: Towards a functional understanding

Brain Research Reviews

Volumn 44, Issue 2-3, 2004, Pages 103-116

  Schweighofer, Nicolas ^a   Doya, Kenji ^a   Kuroda, Shinya ^b  

^a ADVANCED TELECOMMUNICATIONS RESEARCH INSTITUTE INTERNATIONAL   (Japan)

^b UNIVERSITY OF TOKYO   (Japan)

Author keywords

Cerebellum; Feedback error learning; Granule cell; Hebbian plasticity; Internal neural model; Long term depression; Motor system and sensory motor integration; Rebound potentiation

Indexed keywords

ACETYLCHOLINE; DOPAMINE; HISTAMINE; NICOTINIC RECEPTOR; NORADRENALIN; SEROTONIN; SEROTONIN RECEPTOR;

ADRENERGIC SYSTEM; CEREBELLUM; CEREBELLUM CORTEX; CHOLINERGIC NERVE; DOPAMINERGIC NERVE CELL; EYELID REFLEX; GRANULE CELL; HUMAN; LEARNING; LONG TERM DEPRESSION; MICRODIALYSIS; MOSSY FIBER; NEUROMODULATION; PONS RETICULAR FORMATION; POTENTIOMETRY; PRIORITY JOURNAL; PURKINJE CELL; REINFORCEMENT; REVIEW; SEROTONINERGIC NERVE CELL; SEROTONINERGIC SYSTEM;

ANIMALS; BIOGENIC AMINES; CEREBELLUM; HUMANS; LEARNING; NERVE NET; NEUROTRANSMITTER AGENTS;

EID: 1442274716     PISSN: 01650173     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainresrev.2003.10.004     Document Type: Review

References (133)

1. Adell A., Celada P., Abellan M.T., Artigas F. Origin and functional role of the extracellular serotonin in the midbrain raphe nuclei. Brain Res. Brain Res. Rev. 39:2002;154-180.
2. Albus J.S. The theory of cerebellar function. Math Biosci. 10:1971;25-61.
3. Alder R., Barbas H. Complementary distribution of the phosphoproteins DARPP-32 and I-1 in the cerebellar system. NeuroReport. 6:1995;2368-2372.
4. Andre P., Pompeiano O., White S.R. Activation of muscarinic receptors induces a long-lasting enhancement of Purkinje cell responses to glutamate. Brain Res. 617:1993;28-36.
5. Armano S., Rossi P., Taglietti V., D'Angelo E. Long-term potentiation of intrinsic excitability at the mossy fiber-granule cell synapse of rat cerebellum. J. Neurosci. 20:2000;5208-5216.
6. Armstrong D.L., Hay M., Terrian D.M. Modulation of cerebellar granule cell activity by iontophoretic application of serotonergic agents. Brain Res. Bull. 19:1987;699-704.
7. Aston-Jones G., Chiang C., Alexinsky T. Discharge of noradrenergic locus coeruleus neurons in behaving rats and monkeys suggests a role in vigilance. Prog. Brain Res. 88:1991;501-520.
8. Barili P., Bronzetti E., Ricci A., Zaccheo D., Amenta F. Microanatomical localization of dopamine receptor protein immunoreactivity in the rat cerebellar cortex. Brain Res. 854:2000;130-138.
9. Barmack N.H., Baughman R.W., Eckenstein F.P. Cholinergic innervation of the cerebellum of rat, rabbit, cat, and monkey as revealed by choline acetyltransferase activity and immunohistochemistry. J. Comp. Neurol. 317:1992;233-249.
10. Barmack N.H., Baughman R.W., Eckenstein F.P., Shojaku H. Secondary vestibular cholinergic projection to the cerebellum of rabbit and rat as revealed by choline acetyltransferase immunohistochemistry, retrograde and orthograde tracers. J. Comp. Neurol. 317:1992;250-270.
11. Batini C. The cerebellar projections form the neurons of the raphe nuclei and the origin of the serotonergic innervation of the cerebellum. Serotonin, The Cerebellum, and Ataxia. 1993;51-61 Raven Press, New York.
12. Bickford P. Motor learning deficits in aged rats are correlated with loss of cerebellar noradrenergic function. Brain Res. 620:1993;133-138.
13. Bickford P.C., Hoffer B.J., Freedman R. Interaction of norepinephrine with Purkinje cell responses to cerebellar afferent inputs in aged rats. Neurobiol. Aging. 6:1985;89-94.
14. Bishop G.A. Brainstem origin of corticotropin-releasing factor afferents to the nucleus interpositus anterior of the cat. J. Chem. Neuroanat. 15:1998;143-153.
15. Bishop G.A., Ho R.H. The distribution and origin of serotonin immunoreactivity in the rat cerebellum. Brain Res. 331:1985;195-207.
16. Bishop C., Kerr C.W., Chen Y.F., King J.S. The serotonergic system in the cerebellum: origin, ultrastructural relationships, and physiological effects. Serotonin, The Cerebellum, and Ataxia. 1993;91-112 Raven Press, New York.
17. Carlton S.M., Leichnetz G.R., Mayer J.D. Projections from the nucleus parafascicularis prerubralis to medullary raphe nuclei and inferior olive in the rat: a horseradish peroxidase and autoradiography study. Neurosci. Lett. 30:1982;191-197.
18. Cespuglio R., Faradji H., Jouvet M. Voltammetric detection of extracellular 5-hydroxyindole compounds at the level of cell bodies and the terminals of the raphe system: variations during the wake-sleep cycle in the rat in chronic experiments. C. R. Seances Acad. Sci. III. 296:1983;611-616.
19. Chen W.Y., Wang J.J., Yu Q.X. Effects of dorsal raphe stimulation on activities of cerebellar nuclear neurons in the rat. Sheng Li Xue Bao. 48:1996;132-140.
20. Cheun J.E., Yeh H.H. Noradrenergic potentiation of cerebellar Purkinje cell responses to GABA: cyclic AMP as intracellular intermediary. Neuroscience. 74:1996;835-844.
21. Clavier R.M. Afferent projections to the self-stimulation regions of the dorsal pons, including the locus coeruleus, in the rat as demonstrated by the horseradish peroxidase technique. Brain Res. Bull. 4:1979;497-504.
22. Cornea-Hebert V., Riad M., Wu C., Singh S.K., Descarries L. Cellular and subcellular distribution of the serotonin 5-HT2A receptor in the central nervous system of adult rat. J. Comp. Neurol. 409:1999;187-209.
23. Crepel F., Jalliard D. Protein kinases, nitric oxide and long term depression of synapses in the cerebellum. NeuroReport. 1:1990;133-136.
24. Cumming-Hood P.A., Strahlendorf H.K., Strahlendorf J.C. Effects of serotonin and the 5-HT2/1C receptor agonist DOI on neurons of the cerebellar dentate/interpositus nuclei: possible involvement of a GABAergic interneuron. Eur. J. Pharmacol. 236:1993;457-465.
25. Daniel H., Levenes C., Crepel F. Cellular mechanisms of cerebellar LTD. Trends Neurosci. 21:1998;401-407.
26. Darrow E.J., Strahlendorf H.K., Strahlendorf J.C. Response of cerebellar Purkinje cells to serotonin and the 5-HT1A agonists 8-OH-DPAT and ipsapirone in vitro. Eur. J. Pharmacol. 175:1990;145-153.
27. Dean I., Robertson S.J., Edwards F.A. Serotonin drives a novel GABAergic synaptic current recorded in rat cerebellar Purkinje cells: a Lugaro cell to Purkinje cell synapse. J. Neurosci. 23:2003;4457-4469.
28. Diener H.C., Hore J., Ivry R., Dichgans J. Cerebellar dysfunction of movement and perception. Can. J. Neurol. Sci. 20(Suppl. 3):1993;S62-S69.
29. Dieudonne S., Dumoulin A. Serotonin-driven long-range inhibitory connections in the cerebellar cortex. J. Neurosci. 20:2000;1837-1848.
30. Dillon-Carter O., Chuang D.M. Homologous desensitization of muscarinic cholinergic, histaminergic, adrenergic, and serotonergic receptors coupled to phospholipase C in cerebellar granule cells. J. Neurochem. 52:1989;598-603.
31. Doya K. Metalearning and neuromodulation. Math. Sci. 38:2000;19-24.
32. Doya K., Samejima K., Katagiri K., Kawato M. Multiple model-based reinforcement learning. Neural Comput. 14:2002;1347-1369.
33. Duxon M.S., Flanigan T.P., Reavley A.C., Baxter G.S., Blackburn T.P., Fone K.C. Evidence for expression of the 5-hydroxytryptamine-2B receptor protein in the rat central nervous system. Neuroscience. 76:1997;323-329.
34. Eldracher M., Staller A., Pompl R. Adaptive encoding strongly improves function approximation with CMAC. Neural Comput. 9:1997;403-417.
35. Fox E.A., Gruol D.L. Corticotropin-releasing factor suppresses the afterhyperpolarization in cerebellar Purkinje neurons. Neurosci. Lett. 149:1993;103-107.
36. Freedman R., Hoffer B.J., Puro D., Woodward D.J. Noradrenaline modulation of the responses of the cerebellar Purkinje cell to afferent synaptic activity. Br. J. Pharmacol. 57:1976;603-605.
37. Gao J.H., Parsons L.M., Bower J.M., Xiong J., Li J., Fox P.T. Cerebellum implicated in sensory acquisition and discrimination rather than motor control. Science. 272:1996;545-547.
38. Geurts F.J., De Schutter E., Timmermans J.P. Localization of 5-HT2A, 5-HT3, 5-HT5A and 5-HT7 receptor-like immunoreactivity in the rat cerebellum. J. Chem. Neuroanat. 24:2002;65-74.
39. Gould T.J., Adams C.E., Bickford P.C. Beta-adrenergic modulation of GABAergic inhibition in the deep cerebellar nuclei of F344 rats. Neuropharmacology. 36:1997;75-81.
40. Graham A., Court J.A., Martin-Ruiz C.M., Jaros E., Perry R., Volsen S.G., Bose S., Evans N., Ince P., Kuryatov A., Lindstrom J., Gotti C., Perry E.K. Immunohistochemical localisation of nicotinic acetylcholine receptor subunits in human cerebellum. Neuroscience. 113:2002;493-507.
41. Hamann M., Rossi D.J., Attwell D. Tonic and spillover inhibition of granule cells control information flow through cerebellar cortex. Neuron. 33:2002;625-633.
42. Haruno M., Wolpert D.M., Kawato M. Mosaic model for sensorimotor learning and control. Neural Comput. 13:2001;2201-2220.
43. Hasselmo M.E., Linster C. Neuromodulation and memory functions. Katz P.S. Beyond Neurotransmission. 1999;319-348 Oxford Univ. Press, Oxford.
44. Hertz J., Krogh A., Palmer R. Introduction to the Theory of Neural Computation. 1991;Addison-Wesley Pub. Comp. Redwood City, CA.
45. Ikai Y., Takada M., Shinonaga Y., Mizuno N. Dopaminergic and non-dopaminergic neurons in the ventral tegmental area of the rat project, respectively, to the cerebellar cortex and deep cerebellar nuclei. Neuroscience. 51:1992;719-728.
46. Imamizu H., Miyauchi S., Tamada T., Sasaki Y., Takino R., Putz B., Yoshioka T., Kawato M. Human cerebellar activity reflecting an acquired internal model of a new tool. Nature. 403:2000;192-195.
47. Imamizu H., Kuroda T., Miyauchi S., Yoshioka T., Kawato M. Modular organization of internal models of tools in the human cerebellum. Proc. Natl. Acad. Sci. U. S. A. 100:2003;5461-5466.
48. Inglis W.L., Winn P. The pedunculopontine tegmental nucleus: where the striatum meets the reticular formation. Prog. Neurobiol. 47:1995;1-29.
49. Inoue K., Kawashima R., Satoh K., Kinomura S., Goto R., Koyama M., Sugiura M., Ito M., Fukuda H. PET study of pointing with visual feedback of moving hands. J. Neurophysiol. 79:1998;117-125.
50. Ito M. The Cerebellum and Neuronal Control. 1984;Raven Press, New York.
51. Ito M. Long-term depression. Annu. Rev. Neurosci. 12:1989;85-102.
52. Ito M., Sakurai M., Tongroach P. Climbing fiber induced long term depression of both mossy fiber responsiveness and glutamate sensitivity of cerebellar Purkinje cells. J. Physiol. 1982;113-134.
53. Jaarsma D., Ruigrok T.J., Caffe R., Cozzari C., Levey A.I., Mugnaini E., Voogd J. Cholinergic innervation and receptors in the cerebellum. Prog. Brain Res. 114:1997;67-96.
54. Jueptner M., Ottinger S., Fellows S.J., Adamschewski J., Flerich L., Muller S.P., Diener H.C., Thilmann A.F., Weiller C. The relevance of sensory input for the cerebellar control of movements. NeuroImage. 5:1997;41-48.
55. Kandel E.R., Schwartz J.H., Jessel T.M. Principles of Neural Science. 2000;McGraw-Hill, New York.
56. Kano M., Rexhausen U., Dreessen J., Konnerth A. Synaptic excitation produces a long-lasting rebound potentiation of inhibitory synaptic signals in cerebellar Purkinje cells. Nature. 356:1992;601-604.
57. Katz P.S. Beyond Neurotransmission. 2000;Oxford Univ. Press, Oxford.
58. Kawaguchi S., Hirano T. Suppression of inhibitory synaptic potentiation by presynaptic activity through postsynaptic GABA(B) receptors in a Purkinje neuron. Neuron. 27:2000;339-347.
59. Kawaguchi S.Y., Hirano T. Signaling cascade regulating long-term potentiation of GABA(A) receptor responsiveness in cerebellar Purkinje neurons. J. Neurosci. 22:2002;3969-3976.
60. Kawato M., Gomi H. A computational model of four regions of the cerebellum based on feedback-error learning. Biol. Cybern. 68:1992;95-103.
61. Kawato M., Wolpert D. Internal models for motor control. Novartis Found. Symp. 218:1998;291-304. (discussion 304-297).
62. Kerr C.W., Bishop G.A. Topographical organization in the origin of serotoninergic projections to different regions of the cat cerebellar cortex. J. Comp. Neurol. 304:1991;502-515.
63. Kerr C.W., Bishop G.A. The physiological effects of serotonin are mediated by the 5HT1A receptor in the cat's cerebellar cortex. Brain Res. 591:1992;253-260.
64. Kimoto Y., Satoh K., Sakumoto T., Tohyama M., Shimizu N. Afferent fiber connections from the lower brain stem to the rat cerebellum by the horseradish peroxidase method combined with MAO staining, with special reference to noradrenergic neurons. J. Hirnforsch. 19:1978;85-100.
65. Kimoto Y., Tohyama M., Satoh K., Sakumoto T., Takahashi Y., Shimizu N. Fine structure of rat cerebellar noradrenaline terminals as visualized by potassium permanganate 'in situ perfusion' fixation method. Neuroscience. 6:1981;47-58.
66. King J.S., Madtes P. Jr., Bishop G.A., Overbeck T.L. The distribution of corticotropin-releasing factor (CRF), CRF binding sites and CRF1 receptor mRNA in the mouse cerebellum. Prog. Brain Res. 114:1997;55-66.
67. Kitazawa S., Kimura T., Yin P.B. Cerebellar complex spikes encode both destinations and errors in arm movements. Nature. 392:1998;494-497.
68. Kitzman P.H., Bishop G.A. The origin of serotoninergic afferents to the cat's cerebellar nuclei. J. Comp. Neurol. 340:1994;541-550.
69. Kobayashi Y., Kawano K., Takemura A., Inoue Y., Kitama T., Gomi H., Kawato M. Temporal firing patterns of Purkinje cells in the cerebellar ventral paraflocculus during ocular following responses in monkeys: II. Complex spikes. J. Neurophysiol. 80:1998;832-848.
70. Kobayashi Y., Saito Y., Isa T. Facilitation of saccade initiation by brainstem cholinergic system. Brain Dev. 23(Suppl. 1):2001;S24-S27.
71. Kreitzer A.C., Carter A.G., Regehr W.G. Inhibition of interneuron firing extends the spread of endocannabinoid signaling in the cerebellum. Neuron. 34:2002;787-796.
72. Kuroda S., Schweighofer N., Kawato M. Exploration of signal transduction pathways in cerebellar long-term depression by kinetic simulation. J. Neurosci. 21:2001;5693-5702.
73. Lee M., Strahlendorf J.C., Strahlendorf H.K. Modulatory action of serotonin on glutamate-induced excitation of cerebellar Purkinje cells. Brain Res. 361:1985;107-113.
74. Li W.C., Tang X.H., Li H.Z., Wang J.J. Histamine excites rat cerebellar granule cells in vitro through H1 and H2 receptors. J. Physiol. (Paris). 93:1999;239-244.
75. Llinas R., Yarom Y. Oscillatory properties of guinea-pig inferior olivary neurones and their pharmacological modulation: an in vitro study. J. Physiol. 376:1986;163-182.
76. Maeshima T., Shutoh F., Hamada S., Senzaki K., Hamaguchi-Hamada K., Ito R., Okado N. Serotonin2A receptor-like immunoreactivity in rat cerebellar Purkinje cells. Neurosci. Lett. 252:1998;72-74.
77. Marder E., Thirumalai V. Cellular, synaptic and network effects of neuromodulation. Neural Netw. 15:2002;479-493.
78. Marr D. A theory of cerebellar cortex. J. Physiol. 202:1969;437-470.
79. Maura G., Raiteri M. Serotonin 5-HT1D and 5-HT1A receptors respectively mediate inhibition of glutamate release and inhibition of cyclic GMP production in rat cerebellum in vitro. J. Neurochem. 66:1996;203-209.
80. Maura G., Ricchetti A., Raiteri M. Serotonin inhibits the depolarization-evoked release of endogenous glutamate from rat cerebellar nerve endings. Neurosci. Lett. 67:1986;218-222.
81. Maura G., Roccatagliata E., Ulivi M., Raiteri M. Serotonin-glutamate interaction in rat cerebellum: involvement of 5-HT1 and 5-HT2 receptors. Eur. J. Pharmacol. 145:1988;31-38.
82. McCormick D.A. Cholinergic and noradrenergic modulation of thalamocortical processing. Trends Neurosci. 12:1989;215-221.
83. McCormick D.A., Thompson R.F. Locus coeruleus lesions and resistance to extinction of a classically conditioned response: involvement of the neocortex and hippocampus. Brain Res. 245:1982;239-249.
84. Mendlin A., Martin F.J., Rueter L.E., Jacobs B.L. Neuronal release of serotonin in the cerebellum of behaving rats: an in vivo microdialysis study. J. Neurochem. 67:1996;617-622.
85. Miall R.C., Weir D.J., Wolpert D.M., Stein J.F. Is the cerebellum a Smith Predictor? J. Mot. Behav. 25:1993;203-216.
86. Mihailoff G.A., Kosinski R.J., Azizi S.A., Border B.G. Survey of noncortical afferent projections to the basilar pontine nuclei: a retrograde tracing study in the rat. J. Comp. Neurol. 282:1989;617-643.
87. Mitoma H., Konishi S. Long-lasting facilitation of inhibitory transmission by monoaminergic and cAMP-dependent mechanism in rat cerebellar GABAergic synapses. Neurosci. Lett. 217:1996;141-144.
88. Mitoma H., Konishi S. Monoaminergic long-term facilitation of GABA-mediated inhibitory transmission at cerebellar synapses. Neuroscience. 88:1999;871-883.
89. Miyata M., Okada D., Hashimoto K., Kano M., Ito M. Corticotropin- releasing factor plays a permissive role in cerebellar long-term depression. Neuron. 22:1999;763-775.
90. Mock M., Schwarz C., Thier P. Serotonergic control of cerebellar mossy fiber activity by modulation of signal transfer by rat pontine nuclei neurons. J. Neurophysiol. 88:2002;549-564.
91. Morton D.B., Bredt D.S. Norepinephrine increases cyclic GMP levels in cerebellar cells from neuronal nitric oxide synthase knockout mice. J. Neurochem. 71:1998;440-443.
92. Naka F., Shiga T., Yaguchi M., Okado N. An enriched environment increases noradrenaline concentration in the mouse brain. Brain Res. 924:2002;124-126.
93. Nawrot M., Rizzo M. Chronic motion perception deficits from midline cerebellar lesions in human. Vision Res. 38:1998;2219-2224.
94. Oscarsson O. Functional organization of olivary projection to the cerebellar anterior lobe. J.C.et al. The Inferior Olivary Nucleus: Anatomy and Physiology. 1980;279-289 Raven Press, New York.
95. Panula P., Takagi H., Inagaki N., Yamatodani A., Tohyama M., Wada H., Kotilainen E. Histamine-containing nerve fibers innervate human cerebellum. Neurosci. Lett. 160:1993;53-56.
96. Pompeiano O. Noradrenergic influences on the cerebellar cortex: effects on vestibular reflexes under basic and adaptive conditions. Otolaryngol. Head Neck Surg. 119:1998;93-105.
97. Powers R.E., O'Connor D.T., Price D.L. Noradrenergic innervation of human inferior olivary complex. Brain Res. 523:1990;151-155.
98. Prast H., Philippu A. Nitric oxide as modulator of neuronal function. Prog. Neurobiol. 64:2001;51-68.
99. Raymond J.R., Mukhin Y.V., Gelasco A., Turner J., Collinsworth G., Gettys T.W., Grewal J.S., Garnovskaya M.N. Multiplicity of mechanisms of serotonin receptor signal transduction. Pharmacol. Ther. 92:2001;179-212.
100. Reynolds J.N., Hyland B.I., Wickens J.R. A cellular mechanism of reward-related learning. Nature. 413:2001;67-70.
101. Roger M., Cadusseau J. Afferents to the zona incerta in the rat: a combined retrograde and anterograde study. J. Comp. Neurol. 241:1985;480-492.
102. Saitow F., Konishi S. Excitability increase induced by beta-adrenergic receptor-mediated activation of hyperpolarization-activated cation channels in rat cerebellar basket cells. J. Neurophysiol. 84:2000;2026-2034.
103. Saitow F., Satake S., Yamada J., Konishi S. Beta-adrenergic receptor-mediated presynaptic facilitation of inhibitory GABAergic transmission at cerebellar interneuron-Purkinje cell synapses. J. Neurophysiol. 84:2000;2016-2025.
104. Schultz W. Predictive reward signal of dopamine neurons. J. Neurophysiol. 80:1998;1-27.
105. Schweighofer N., Arbib M.A. A model of cerebellar metaplasticity. Learn Mem. 1998;421-428.
106. Schweighofer N., Ferriol G. Diffusion of nitric oxide can facilitate cerebellar learning: a simulation study. Proc. Natl. Acad. Sci. U. S. A. 97:2000;10661-10665.
107. Schweighofer N., Arbib M.A., Dominey P.F. A model of the cerebellum in adaptive control of saccadic gain: I. The model and its biological substrate. Biol. Cybern. 75:1996;19-28.
108. Schweighofer N., Arbib M.A., Dominey P.F. A model of the cerebellum in adaptive control of saccadic gain: II. Simulation results. Biol. Cybern. 75:1996;29-36.
109. Schweighofer N., Arbib M.A., Kawato M. Role of the cerebellum in reaching movements in humans: I. Distributed inverse dynamics control. Eur. J. Neurosci. 10:1998;86-94.
110. Schweighofer N., Spoelstra J., Arbib M.A., Kawato M. Role of the cerebellum in reaching movements in humans: II. A neural model of the intermediate cerebellum. Eur. J. Neurosci. 10:1998;95-105.
111. Schweighofer N., Doya K., Kawato M. Electrophysiological properties of inferior olive neurons: a compartmental model. J. Neurophysiol. 82:1999;804-817.
112. Schweighofer N., Doya K., Lay F. Unsupervised learning of granule cell sparse codes enhances cerebellar adaptive control. Neuroscience. 103:2001;35-50.
113. Senba E., Takagi H., Shiosaka S., Sakanaka M., Inagaki S., Takatsuki K., Tohyama M. On the afferent projections from some meso-diencephalic nuclei to n. raphe magnus of the rat. Brain Res. 211:1981;387-392.
114. Shidara M., Kawano K., Gomi H., Kawato M. Inverse-dynamics model eye movement control by Purkinje cells in the cerebellum. Nature. 365:1993;50-52.
115. Strahlendorf J.C., Hubbard G.D. Serotonergic interactions with rat cerebellar Purkinje cells. Brain Res. Bull. 11:1983;265-269.
116. Strahlendorf J.C., Lee M., Strahlendorf H.K. Effects of serotonin on cerebellar Purkinje cells are dependent on the baseline firing rate. Exp. Brain Res. 56:1984;50-58.
117. Sugihara I., Lang E.J., Llinas R. Serotonin modulation of inferior olivary oscillations and synchronicity: a multiple-electrode study in the rat cerebellum. Eur. J. Neurosci. 7:1995;521-534.
118. Sutton R.S. Adapting bias by gradient descent: an incremental version of the delta-bar-delta. The Tenth National Conference on Artificial Intelligence. 1992;171-176 MIT Press, Cambridge, MA.
119. Thach W.T. Discharge of Purkinje and cerebellar nuclear neurons during rapidly alternating arm movements in the monkey. J. Neurophysiol. 31:1968;785-797.
120. Thellung S., Barzizza A., Maura G., Raiteri M. Serotonergic inhibition of the mossy fibre-granule cell glutamate transmission in rat cerebellar slices. Naunyn Schmiedeberg's Arch. Pharmacol. 348:1993;347-351.
121. Thompson R.F. The neurobiology of learning and memory. Science. 233:1986;932-947.
122. Tian L., Wen Y.Q., Li H.Z., Xiong H.B., Wang J.J. The excitatory effects of histamine on cerebellar cortical Purkinje cells in the rat. Sheng Li Xue Bao. 51:1999;219-223.
123. Trouillas P. The cerebellar serotoninergic system and its possible involvement in cerebellar ataxia. Can. J. Neurol. Sci. 20(Suppl. 3):1993;S78-S82.
124. van Kan P.L., Gibson A.R., Houk J.C. Movement-related inputs to intermediate cerebellum of the monkey [published erratum appears in J Neurophysiol 1993 Mar;69(3): following table of contents]. J. Neurophysiol. 69:1993;74-94.
125. Veasey S.C., Fornal C.A., Metzler C.W., Jacobs B.L. Response of serotonergic caudal raphe neurons in relation to specific motor activities in freely moving cats. J. Neurosci. 15:1995;5346-5359.
126. Veasey S.C., Fornal C.A., Metzler C.W., Jacobs B.L. Single-unit responses of serotonergic dorsal raphe neurons to specific motor challenges in freely moving cats. Neuroscience. 79:1997;161-169.
127. Wang Y., Strahlendorf J.C., Strahlendorf H.K. Serotonin reduces a voltage-dependent transient outward potassium current and enhances excitability of cerebellar Purkinje cells. Brain Res. 571:1992;345-349.
128. Watson M., McElligott J.G. Cerebellar norepinephrine depletion and impaired acquisition of specific locomotor tasks in rats. Brain Res. 296:1984;129-138.
129. Weiss M., Pellet J. Raphe-cerebellum interactions: I. Effects of cerebellar stimulation and harmaline administration on single unit activity of midbrain raphe neurons in the rat. Exp. Brain Res. 48:1982;163-170.
130. Weiss M., Pellet J. Raphe-cerebellum interactions: II. Effects of midbrain raphe stimulation and harmaline administration on single unit activity of cerebellar cortical cells in the rat. Exp. Brain Res. 48:1982;171-176.
131. Wiklund L., Bjorklund A., Sjolund B. The indolaminergic innervation of the inferior olive: 1. Convergence with the direct spinal afferents in the areas projecting to the cerebellar anterior lobe. Brain Res. 131:1977;1-21.
132. Xu J., Chuang D.M. Serotonergic, adrenergic and histaminergic receptors coupled to phospholipase C in cultured cerebellar granule cells of rats. Biochem. Pharmacol. 36:1987;2353-2358.
133. Yoshida T., Hashimoto K., Zimmer A., Maejima T., Araishi K., Kano M. The cannabinoid CB1 receptor mediates retrograde signals for depolarization-induced suppression of inhibition in cerebellar Purkinje cells. J. Neurosci. 22:2002;1690-1697.