Synchrony and neural coding in cerebellar circuits

Frontiers in Neural Circuits

Volumn , Issue NOV, 2012, Pages 1-32

  Person, Abigail L ^a   Raman, Indira M ^b  

^a UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^b NORTHWESTERN UNIVERSITY   (United States)

Author keywords

Action potential; Cerebellar nuclei; Corticonuclear; Inhibition; Interpositus; IPSC; Purkinje; Spatiotemporal

Indexed keywords

BRAIN FUNCTION; BRAIN NERVE CELL; CELL SYNCHRONIZATION; CEREBELLUM CORTEX; CEREBELLUM NUCLEUS; CORTICAL SYNCHRONIZATION; EVOKED CORTICAL RESPONSE; HUMAN; INTRACELLULAR SIGNALING; MOTOR SYSTEM; NONHUMAN; PURKINJE CELL; REVIEW; SYNAPTIC POTENTIAL;

EID: 84869802288     PISSN: 16625110     EISSN: None     Source Type: Journal    
DOI: 10.3389/fncir.2012.00097     Document Type: Review

References (169)

1. Aizenman C.D., Manis P.B., Linden D.J. (1998). Polarity of long-term synaptic gain change is related to postsynaptic spike firing at a cerebellar inhibitory synapse. Neuron 21(4), 827-835.
2. Aizenman C.D., Linden D.J. (1999). Regulation of the rebound depolarization and spontaneous firing patterns of deep nuclear neurons in slices of rat cerebellum. J. Neurophysiol. 82(4), 1697-1709.
3. Akam T., Kullmann D.M. (2010). Oscillations and filtering networks support flexible routing of information. Neuron. 67, 308-320.
4. Albus, J.S. (1971). Theory of cerebellar function. Math. Biosci. 10, 25-61.
5. Alviña K., Walter J.T., Kohn A., Ellis-Davies G., Khodakhah K. (2008). Questioning the role of rebound firing in the cerebellum. Nat. Neurosci. 11(11), 1256-1258.
6. Alviña K., Khodakhah K. (2010). The therapeutic mode of action of 4-aminopyridine in cerebellar ataxia. J. Neurosci. 30(21), 7258-7268.
7. Anchisi D., Scelfo B., Tempia F. (2001). Postsynaptic currents in deep cerebellar nuclei. J. Neurophysiol. 85, 323-331.
8. Anderson M.E. and Horak F.B. (1985). Influence of the globus pallidus on arm movements in monkeys. III. Timing of movement-related information. J. Neurophysiol. 54, 433-448.
9. Anderson M.E., Turner R.S. (1991). Activity of neurons in cerebellar-receiving and pallidal receiving areas of the thalamus of the behaving monkey. J. Neurophysiol. 66, 879-893.
10. Andersson G., Oscarsson O. (1978). Climbing fiber microzones in cerebellar vermis and their projection to different groups of cells in the lateral vestibular nucleus. Exp. Brain Res. 32, 565-579.
11. Armstrong D.M., Cogdell B., Harvey R. (1975). Effects of afferent volleys from the limbs on the discharge patterns of interpositus neurons in cats anaesthetized with alpha-chloralose. J. Physiol. 248, 489-517.
12. Armstrong D.M., Edgley S.A. (1984a). Discharges of nucleus interpositus neurones during locomotion in the cat. J. Physiol. 351, 411-432.
13. Armstrong D.M., Edgley S.A. (1984b). Discharges of Purkinje cells in the paravermal part of the cerebellar anterior lobe during locomotion in the cat. J. Physiol. 352, 403-424.
14. Aumann T.D., Fetz E.E. (2004). Oscillatory activity in forelimb muscles of behaving monkeys evoked by microstimulation in the cerebellar nuclei. Neurosci. Lett. 361, 106-110.
15. Baker S.N., Spinks R., Jackson A., Lemon R.N. (2001). Synchronization in monkey motor cortex during a precision grip task. I. Task-dependent modulation in single-unit synchrony. J. Neurophysiol. 85, 869-885.
16. Bartos M., Vida I., Frotscher M., Geiger J.R., Jonas P. (2001). Rapid signaling at inhibitory synapses in a dentate gyrus interneuron network. J. Neurosci. 21, 2687-2698.
17. Bartos M., Vida I., Frotscher M., Meyer A., Monyer H., Geiger J.R., Jonas P. (2002). Fast synaptic inhibition promotes synchronized gamma oscillations in hippocampal interneuron networks. Proc. Natl. Acad. Sci. USA. 99, 13222-13227.
18. Bell C.C., Grimm R.J. (1969). Discharge properties of Purkinje cells recorded on single and double microelectrodes. J. Neurophysiol. 32, 1044-1055.
19. Bell C.C., Kawasaki T. (1972). Relations among climbing fiber responses of nearby Purkinje Cells. J. Neurophysiol. 35, 155-169.
20. Bengtsson F., Ekerot C.F., Jörntell H. (2011). In vivo analysis of inhibitory synaptic inputs and rebounds in deep cerebellar nuclear neurons. PLoS One 6(4), e18822.
21. Bishop G.A., McCrea R.A., Lighthall J.W., Kitai S.T. (1979). An HRP and autoradiographi1 c study of the projection from the cerebellar cortex to the nucleus interpositus anterior and nucleus interpositus posterior of the cat. J. Comp. Neurol. 185, 735-756.
22. Blenkinsop T.A., Lang E.J. (2006). Block of inferior olive gap junctional coupling decreases Purkinje cell complex spike synchrony and rhythmicity. J. Neurosci. 26, 1739-1748.
23. Blenkinsop T.A., Lang E.J. (2011). Synaptic action of the olivocerebellar system on cerebellar nuclear spike activity. J. Neurosci. 31, 14707-14720.
24. Bosman L.W., Koekkoek S.K., Shapiro J., Rijken B.F., Zandstra F., van der Ende B., Owens C.B., Potters J.W., de Gruijl J.R., Ruigrok T.J., De Zeeuw C.I. (2010). Encoding of whisker input by cerebellar Purkinje cells. J. Physiol. 588, 3757-3783.
25. Bower J.M. (2002). The organization of cerebellar cortical circuitry revisited: implications for function. Ann. NY Acad. Sci. 978, 135-155.
26. Bower J.M., Woolston D.C. (1983). Congruence of spatial organization of tactile projections to granule cell and Purkinje cell layers of cerebellar hemispheres of the albino rat: vertical organization of cerebellar cortex. J. Neurophysiol. 49, 745-766.
27. Braitenberg V. (1967). Is the cerebellar cortex a biological clock in the millisecond rage? Prog. Brain Res. 25, 334-346.
28. Brunel N., Hakim V., Isope P., Nadal J.P., Barbour B. (2004). Optimal information storage and the distribution of synaptic weights: perceptron versus Purkinje cell. Neuron. 43, 745-757.
29. Buisseret-Delmas C., Angaut P. (1993). The cerebellar olivocorticonuclear connections in the rat. Prog. Neurobiol. 40, 63-87.
30. Caddy K.W., Biscoe T.J. (1979). Structural and quantitative studies on the normal C3H and Lurcher mutant mouse. Phil. Trans. R. Soc. Lond. B Biol. Sci. 287, 167-201.
31. Calderon, D.P., Fremont, R., Kraenzlin, F., Khodakhah, K. (2011). The neural substrates of rapid-onset Dystonia-Parkinsonism. Nat. Neurosci. 143, 57-365.
32. Cao Y., Maran S., Jaeger D., Heck D. (2012). Representation of behaviors in the cerebellum: Spike rate modulation vs spike timing. Program No. 477.07. Neuroscience Meeting Planner. New Orleans, LA: Society for Neuroscience, 2012. Online.
33. Catz N., Dicke P.W., Thier P. (2008). Cerebellar-dependent motor learning is based on pruning a Purkinje cell population response. Proc. Natl. Acad. Sci. USA. 105, 7309-7314.
34. Chan-Palay V. (1977). Cerebellar dentate nucleus. Organization, Cytology, and Transmitters. Springer, New York.
35. Cody F.W., Moore R.B., Richardson H.C. (1981). Patterns of activity evoked in cerebellar inerpositus nuclear neurons by natural somatosensory stimuli in awake cats. J. Physiol. 317, 1-20.
36. Cohen D., Yarom Y. (1998). Patches of synchronized activity in the cerebellar cortex evoked by mossy-fiber stimulation: questioning the role of parallel fibers. Proc. Natl. Acad. Sci. USA. 95, 15032-15036.
37. Courtemanche R., Lamarre Y. (2005). Local field potential oscillations in primate cerebella1 r cortex: synchronization with cerebral cortex during active and passive expectancy. J. Neurophysiol. 93, 2039-2052.
38. Courtemanche R., Pellerin J.P., Lamarre Y. (2002). Local field potential oscillations in primate cerebellar cortex: modulation during active and passive expectancy. J. Neurophysiol. 88, 771-782.
39. Czubayko U., Sultan F., Thier P., Schwarz C. (2001). Two types of neurons in the rat cerebellar nuclei as distinguished by membrane potentials and intracellular fillings. J. Neurophysiol. 85, 2017-2029.
40. D'Angelo E., De Zeeuw C.I. (2009). Timing and plasticity in the cerebellum: focus on the granular layer. Trends Neurosci. 32, 30-40.
41. D'Angelo E., Koekkoek S.K., Lombardo P., Solinas S., Ros E., Garrido J., Schonewille M., De Zeeuw C.I. (2009). Timing in the cerebellum: oscillations and resonance in the granular layer. Neuroscience 162(3), 805-815.
42. De Schutter E., Steuber V. (2009). Patterns and pauses in Purkinje cell simple spike trains: experiments, modeling and theory. Neuroscience 162, 816-826.
43. de Solages, C., Szapiro G., Brunel N., Hakim V., Isope P., Buisseret P., Rousseau C., Barbour B., Léna C. (2008). High-frequency organization and synchrony of activity in the Purkinje cell layer of the cerebellum. Neuron 58, 775-788.
44. De Zeeuw C.I., Hoebeek F.E., Bosman L.W., Schonewille M., Witter L., Koekkoek S.K. (2011). Spatiotemporal firing patterns in the cerebellum. Nat. Rev. Neurosci. 12, 327-344.
45. De Zeeuw C.I., Koekkoek S.K., Wylie D.R., Simpson J.I. (1997). Association between dendritic lamellar bodies and complex spike synchrony in the olivocerebellar system. J. Neurophysiol. 77, 1747-1758.
46. De Zeeuw C.I., Wylie D.R., DiGiorgi P.L., Simpson J.I. (1994). Projections of individual Purkinje cells of identified zones in the flocculus to the vestibular and cerebellar nuclei in the rabbit. J. Comp. Neurol. 15, 428-447.
47. Dean H.L., Hagan M.A., Pesaran B. (2012). Only coherent spiking in posterior parietal cortex coordinates looking and reaching. Neuron 73, 829-841.
48. DeLong M.R., Crutcher M.D., Georgopoulos A.P. (1985). Primate globus pallidus and subthalamic nucleus: functional organization. J. Neurophysiol. 53, 530-543.
49. Deniau J.M., Chevalier G. (1985). Disinhibition as a basic process in the expression of striatal functions. II. The striato-nigral influence on thalamocortical cells of the ventromedial thalamic nucleus. Brain Res. 334, 227-233.
50. Devor A., Yarom Y. (2002). Electrotonic coupling in the inferior olivary nucleus revealed by simultaneous double patch recordings. J. Neurophysiol. 87, 3048-3058.
51. Dizon M.J., Khodakhah K. (2011). The role of interneurons in shaping Purkinje cell responses in the cerebellar cortex. J. Neurosci. 20, 10463-10473.
52. Dodla R., Svirskis G., Rinzel J. (2006) Well-timed, brief inhibition can promote spiki1 ng: postinhibitory facilitation. J. Neurophysiol. 95(4), 2664-2677.
53. Ebner T.J., Bloedel J.R. (1981). Correlation between activity of Purkinje cells and its modification by natural peripheral stimuli. J. Neurophysiol. 45, 948-961.
54. Eccles J.C., Ito M., Szentagothai J. (1967). The Cerebellum as a Neuronal Machine Springer-Verlag New York Inc.
55. Eccles J.C., Sabah N.H., Schmidt R.F., Taborikova H. (1972). Integration by Purkyne cells of mossy and climbing fibre inputs from cutaneous mecahnoreceptors. Exp. Brain Res. 15, 498-520.
56. Engbers J.D., Anderson D., Tadayonnejad R., Mehaffey W.H., Molineux M.L., Turner R.W. (2011). Distinct roles for I(T) and I(H) in controlling the frequency and timing of rebound spike responses. J. Physiol. 589, 5391-5413.
57. Gauck V., Jaeger D. (2000). The control of rate and timing of spikes in the deep cerebellar nuclei by inhibition. J. Neurosci. 20, 3006-3016.
58. Gauck V., Thomann M., Jaeger D., Borst A. (2001). Spatial distribution of low-and high15 voltage-activated calcium currents in neurons of the deep cerebellar nuclei. J. Neurosci. 21(15), RC158.
59. Gauck V., Jaeger D. (2003). The contribution of NMDA and AMPA conductances to the control of spiking in neurons of the deep cerebellar nuclei. J. Neurosci. 23, 8109-8118.
60. Gauck V., Jaeger D. (2000). The control of rate and timing of spikes in the deep cerebellar nuclei by inhibition. J. Neurosci. 20, 3006-3016.
61. Gilbert, P.F., Thach, W.T. (1977). Purkinje cell activity during motor learning. Brain Res. 128, 309-328.
62. Glasauer S., Rössert C., Strupp M. (2011). The role of regularity and synchrony of cerebellar Purkinje cells for pathological nystagmus. Ann. NY Acad. Sci. 1233, 162-167.
63. Goldberg J.H., Fee M.S. (2012a). A cortical motor nucleus drives the basal ganglia-recipient thalamus in singing birds. Nat. Neurosci. 15, 620-627.
64. Goldberg J.H., Fee M.S. (2012b). Integration of cortical and pallidal inputs in the basal ganglia28 recipient thalamus of singing birds. J. Neurophysiol. 108, 1403-1429.
65. Groenewegen H.J., Voogd J. (1977). The parasagittal zonation within the olivocerebellar projection. I. Climbing fiber distribution in the vermis of the cat cerebellum. J. Comp. Neurol. 174, 417-488.
66. Gundappa-Sulur G., De Schutter E., Bower J.M. (1999). Ascending granule cell axon: an important component of cerebellar cortical circuitry. J. Comp. Neurol. 408, 580-596.
67. Harvey R.J., Napper R.M. (1991). Quantitative studies on the mammalian cerebellum. Prog. Neurobiol. 36, 437-463.
68. Hatsopoulos N.G., Ojakangas C.L., Paninski L., Donoghue J.P. (1998). Information about movement direction obtained from synchronous activity of motor cortical neurons. Proc. Natl. Acad. Sci. USA. 95, 15706-15711.
69. Häusser M., Clark B.A. (1997). Tonic synaptic inhibition modulates neuronal output pattern rn and spatiotemporal synaptic integration. Neuron 19, 665-678.
70. Heck D.H., Thach W.T., Keating J.G. (2007). On-beam synchrony in the cerebellum as the mechanism for the timing and coordination of movement. Proc. Natl. Acad. Sci. USA. 104, 7658-7663.
71. Heckroth, J.A. (1994). Quantitative morphological analysis of the cerebellar nuclei in normal and lurcher mutant mice. I. Morphology and cell number. J. Comp. Neurol. 343, 173-182.
72. Hikosaka O., Wurtz R.H. (1983). Visual and oculomotor functions of monkey substantia nigra pars reticulata. IV. Relation of substantia nigra to superior colliculus. J. Neurophysiol. 49, 1285-1301.
73. Holdefer R.N., Miller L.E., Chen L.L., Houk J.C. (2000). Functional connectivity between cerebellum and primary motor cortex in the awake monkey. J. Neurophysiol. 84, 585-590.
74. Hull C., Regehr W.G. (2012). Identification of an inhibitory circuit that regulates cerebellar Golgi cell activity. Neuron. 73(1), 149-158.
75. Inase M., Buford J.A., Anderson M.E. (1996). Changes in control of arm position, movement, and thalamic discharge during local inactivation in the globus pallidus of the monkey. J. Neurophysiol. 75, 1087-1104.
76. Isope P., Barbour B. (2002). Properties of unitary granule cell-->Purkinje cell synapses in adult rat cerebellar slices. J. Neurosci. 22, 9668-9678.
77. Ito M., Yoshida M. (1966). The origin of cerebral-induced inhibition of Deiters neurones. I. Monosynaptic initiation of the inhibitory postsynaptic potentials. Exp. Brain Res. 2(4), 330-349.
78. Ito M., Yoshida M., Obata K., Kawai N., Udo M. (1970). Inhibitory control of intracerebellar nuclei by the Purkinje cell axons. Exp. Brain Res. 10(1), 64-80.
79. Jadhav S.P., Wolfe J., Feldman D.E. (2009). Sparse temporal coding of elementary tactile features during active whisker sensation. Nat. Neurosci. 12, 792-800.
80. Jaeger D. (2003). No parallel fiber volleys in the cerebellar cortex: evidence from cross27 correlation analysis between Purkinje cells in a computer model and in recordings from anesthetized rats. J. Comput. Neurosci. 14, 311-327.
81. Jahnsen H. (1986a). Electrophysiological characteristics of neurones in the guinea-pig deep cerebellar nuclei in vitro. J. Physiol. 372, 129-147.
82. Jahnsen H. (1986b). Extracellular activation and membrane conductances of neurones in the guinea-pig deep cerebellar nuclei in vitro. J. Physiol. 372, 149-168.
83. Kanichay R.T., Silver R.A. (2008). Synaptic and cellular properties of the feedforward inhibitory circuit within the input layer of the cerebellar cortex. J. Neurosci. 28, 8955-8967.
84. Khaliq Z.M., Raman I.M. (2005). Axonal propagation of simple and complex spikes in cerebellar Purkinje neurons. J. Neurosci. 25, 454-463.
85. Kilavik B.E., Roux S., Ponce-Alvarez A., Confais J., Grün S., Riehle A. (2009). Long-term modifications in motor cortical dynamics induced by intensive practice. J. Neurosci. 29, 12653-12663.
86. Kistler W.M., De Zeeuw C.I. (2003). Time windows and reverberating loops: a reverse1-engineering approach to cerebellar function. Cerebellum 2, 44-54.
87. Kopell N., Ermentrout B. (2004). Chemical and electrical synapses perform complementary in the synchronization of interneuronal networks. Proc. Natl. Acad. Sci. USA. 101(43), 15482-15487.
88. Kravitz A.V., Freeze B.S., Parker P.R., Kay K. Thwin M.T., Deisseroth K., Kreitzer A.C. (2010). Regulation of Parkinsonian motor behaviours by optogenetic control of basal ganglia circuitry. Nature. 466, 622-626
89. Lampl I., Yarom Y. (1993). Subthreshold oscillations of the membrane potential: a functional synchronizing and timing device. J. Neurophysiol. 70, 2181-2186.
90. Latham A., Paul D.H. (1971). Spontaneous activity of cerebellar Purkinje cells and their responses to impulses in climbing fibres. J. Physiol. 213, 135-156.
91. LeDoux, M.S., Hurst, D.C., Lorden, J.F. (1998). Single-unit activity of cerebellar nuclear cells the awake genetically dystonic rat. Neuroscience 86, 533-545.
92. LeDoux, M.S., Lorden, J.F., Ervin, J.M. (1993). Cerebellectomy eliminates the motor syndrome of the genetically dystonic rat. Exp. Neurol. 120, 302-310.
93. Levin, S.I., Khaliq, Z.M., Aman, T.K., Grieco, T.M., Kearney, J.A., Raman, I.M., Meisler, M. (2006). Impaired motor function in mice with cell-specific knockout of sodium channel Scn8a (NaV1.6) in cerebellar purkinje neurons and granule cells. J. Neurophysiol. 96, 785-793.
94. Lisberger S.G., Fuchs A.F. (1978). Role of primate flocculus during rapid behavioral modification of vestibuloocular reflex. I. Purkinje cell activity during visually guided horizontal smooth-pursuit eye movements and passive head rotation. J. Neurophysiol. 41, 733-763.
95. Llinás, R., Sugimori, M. (1980). Electrophysiological properties of in vitro Purkinje cell somata in mammalian cerebellar slices. J. Physiol. 305, 171-195.
96. Llinás R., Mühlethaler M. (1988). Electrophysiology of guinea-pig cerebellar nuclear cells in in vitro brain stem-cerebellar preparation. J. Physiol. 404, 241-258.
97. Llinás R., Yarom Y. (1986). Oscillatory properties of guinea-pig inferior olivary neurones and their pharmacological modulation: an in vitro study. J. Physiol. 376, 163-182.
98. Lu B., Su Y., Das S., Liu J., Xia J., Ren D. (2007). The neuronal channel NALCN contributes resting sodium permeability and is required for normal respiratory rhythm. Cell 129, 371-383.
99. MacKay W.A., Murphy J.T. (1976). Integrative versus delay line characteristics of cerebellar cortex. Can. J. Neurol. Sci. 3, 85-97.
100. Marr, D. (1969). A theory of cerebellar cortex. J. Physiol. 202, 437-470.
101. Mauk, M.D., Buonomano, D.V. (2004). The neural basis of temporal processing. Ann. Rev. Neurosci. 27, 307-340.
102. McDevitt C.J., Ebner T.J., Bloedel J.R. (1982). The changes in Purkinje cell simple spike activity following spontaneous climbing fiber inputs. Brain Res. 237, 484-491.
103. McDevitt C.J., Ebner T.J., Bloedel J.R. (1987). Relationships between simultaneously recorde1 d Purkinje cells and nuclear neurons. Brain Res. 425, 1-13.
104. Medina, J.F., Nores, W.L., Mauk, M.D. (2002). Inhibition of climbing fibers is a signal for the extinction of conditioned eyelid responses. Nature 416, 330-333.
105. Middleton S.J., Racca C., Cunningham M.O., Traub R.D., Monyer H., Knöpfel T., Schofield I.S., Jenkins A., Whittington M.A. (2008). High-frequency network oscillations in cerebellar cortex. Neuron. 58, 763-774.
106. Mittmann W., Koch U., Häusser M. (2005). Feed-forward inhibition shapes the spike output of cerebellar Purkinje cells. J. Physiol. 563(Pt 2), 369-378.
107. Molineux M.L., McRory J.E., McKay B.E., Hamid J., Mehaffey W.H., Rehak R., Snutch T.P., Zamponi G.W., Turner R.W. (2006). Specific T-type calcium channel isoforms are associated with distinct burst phenotypes in deep cerebellar nuclear neurons. Proc. Natl. Acad. Sci. USA. 103, 5555-5560.
108. Monsivais P., Clark B.A., Roth A., Häusser M. (2005). Determinants of action potential propagation in cerebellar Purkinje cell axons. J. Neurosci. 25, 464-472.
109. Morcuende S., Delgado-Garcia J.M., Ugolini G. (2002). Neuronal premotor networks involved in eyelid responses: retrograde transneuronal tracing with rabies virus from the orbicularis oculi muscle in the rat. J. Neurosci. 22, 8808-8818.
110. Mouginot D., Gähwiler B.H. (1995). Characterization of synaptic connections between cortex and deep nuclei of the rat cerebellum in vitro. Neuroscience 64, 699-712.
111. Mukamel E.A., Nimmerjahn A., Schnitzer M.J. (2009). Automated analysis of cellular signals from large-scale calcium imaging data. Neuron 63, 747-760.
112. Mullen, R.J., Eicher, E.M., Sidman, R.L. (1976). Purkinje cell degeneration, a new neurological mutation in the mouse. Proc. Natl. Acad. Sci. USA 73, 208-212.
113. Muri R., Knöpfel T. (1994). Activity induced elevations of intracellular calcium concentration in neurons of the deep cerebellar nuclei. J. Neurophysiol. 71, 420-428.
114. Murphy J.T., Sabah N.H. (1971). Cerebellar Purkinje cell responses of afferent inputs. I. Climbing fiber activation. Brain Res. 25, 449-467.
115. Murphy J.T., Johnson F., Kwan H.C., Mackay W.A. (1976). Activation of mossy fiber inputs to cerebellar cortex by natural stimulation. Brain Res. 43, 635-639.
116. Nambu A., Tokuno H., Takada M. (2002). Functional significance of the cortico-subthalamo32 pallidal hyperdirect pathway. Neurosci. Res. 43, 111-117.
117. Ozden I., Sullivan M.R., Lee H.M., Wang S.S. (2009). Reliable coding emerges from coactivation of climbing fibers in microbands of cerebellar Purkinje neurons. J. Neurosci. 29, 10463-10473.
118. Palkovits M., Mezey E., Hamori J., Szentagothai J. (1977). Quantitative histological analysis of the cerebellar nuclei in the cat. I. Numerical data on cells and on synapses. Exp. Brain Res. 28 (1-2), 189-209.
119. Pedroarena C.M., Schwarz C. (2003). Efficacy and short-term plasticity at GABAergic synapse1 between Purkinje and cerebellar nuclei neurons. J. Neurophysiol. 89, 704-715.
120. Person A.L., Perkel D.J. (2007). Pallidal neuron activity increases during sensory relay through thalamus in a songbird circuit essential for learning. J. Neurosci. 8, 8687-8698.
121. Person A.L., Raman I.M. (2012). Purkinje neuron synchrony elicits time-locked spiking in the cerebellar nuclei. Nature 481, 502-505.
122. Pugh J.R., Raman I.M. (2006). Potentiation of mossy fiber EPSCs in the cerebellar nuclei by NMDA receptor activation followed by postinhibitory rebound current. Neuron 51(1), 113-123.
123. Raman I.M., Bean B.P. (1997). Resurgent sodium current and action potential formation in dissociated cerebellar Purkinje neurons. J. Neurosci. 17, 4517-4526.
124. Raman I.M., Gustafson A.E., Padgett D.E. (2000). Ionic currents and spontaneous firing in neurons isolated from the cerebellar nuclei. J. Neurosci. 20(24), 9004-9016.
125. Riehle A., Grün S., Diesmann M., Aertsen A. (1997). Spike synchronization and rate modulation differentially involved in motor cortical function. Science 278, 1950-1953.
126. Rowland N.C., Jaeger D. (2005). Coding of tactile response properties in the rat deep cerebellar nuclei. J. Neurophysiol. 94, 1236-1251.
127. Rowland N.C., Jaeger D. (2008) Responses to tactile stimulation in deep cerebellar nucleus neurons result from recurrent activation in multiple pathways. J. Neurophysiol. 99, 704-717
128. Rowland N.C., Goldberg J.A., Jaeger D. (2010) Cortico-cerebellar coherence and causal connectivity during slow-wave activity. Neuroscience. 166,698-711
129. Ruigrok T.J.H., Pijpers A., Goedknegt-Sabel E., Coulon P. (2008). Multiple cerebellar zones are involved in the control of individual muscles: a retrograde transneuronal tracing study with rabies virus in the rat. Eur. J. Neurosci. 28, 181-200.
130. Salinas E., Sejnowski T.J. (2001). Correlated neuronal activity and the flow of neural information. Nat. Rev. Neurosci. 2, 539-550.
131. Sangrey T., Jaeger D. (2010). Analysis of distinct short and prolonged components in rebound spiking of deep cerebellar nucleus neurons. Eur. J. Neurosci. 32(10), 1646-1657.
132. Sasaki K., Bower J.M., Llinás R. (1989). Multiple Purkinje cell recording in rodent cerebellar cortex. Eur. J. Neurosci. 1, 572-586.
133. Sawyer S.F., Young S.J., Groves P.M., Tepper J.M. (1994). Cerebellar-responsive neurons in the thalamic ventroanterior-ventrolateral complex of rats: in vivo electrophysiology. Neuroscience 63, 711-724.
134. Schieber M.H. (2002). Training and synchrony in the motor system. J. Neurosci. 22, 5277-5281.
135. Schoffelen J.M., Oostenveld R., Fries P. (2005). Neuronal coherence as a mechanism of effective corticospinal interaction. Science 308, 111-113.
136. Schultz S.R., Kitamura K., Post-Uiterweer A., Krupic J., Häusser M. (2009). Spatial pattern coding of sensory information by climbing fiber-evoked calcium signals in networks of neighboring cerebellar Purkinje neurons. J. Neurosci. 29, 8005-8015.
137. Shadlen M.N., Movshon J.A. (1999). Synchrony unbound: a critical evaluation of the tempora1 l binding hypothesis. Neuron 24, 67-77.
138. Shin S.L., De Schutter E. (2006). Dynamic synchronization of Purkinje cell simple spikes. J. Neurophysiol. 96, 3485-3491.
139. Shinoda Y., Futami T., Mitoma H., Yokota J. (1988). Morphology of single neurons in the cerebello-rubrospinal system. Behav. Brain Res. 28, 59-64
140. Sims R.E., Hartell N.A. (2005). Differences in transmission properties and susceptibility to long8 term depression reveal functional specialization of ascending axon and parallel fiber synapses to Purkinje cells. J. Neurosci. 25, 3246-3257.
141. Sims R.E., Hartell N.A. (2006). Differential susceptibility to synaptic plasticity reveals a functional specialization of ascending axon and parallel fiber synapses to cerebellar Purkinje cells. J. Neurosci. 26, 5153-5159.
142. Soteropoulos D.S., Baker S.N. (2006). Cortico-cerebellar coherence during a precision grip task in the monkey. J. Neurophysiol. 95, 1194-1206.
143. Steuber V., Mittmann W., Hoebeek F.E., Silver R.A., De Zeeuw C.I., Häusser M, De Schutter E. (2007). Cerebellar LTD and pattern recognition by Purkinje cells. Neuron. 54,121-136
144. Sugihara I., Fujita H., Na J., Quy P.N., Li B.Y., Ikeda D. (2009). Projection of reconstructed single Purkinje cell axons in relation to the cortical and nuclear aldolase C compartments of the rat cerebellum. J. Comp. Neurol. 512, 282-304.
145. Sun L.W. (2012). Transsynaptic tracing of conditioned eyeblink circuits in the mouse cerebellum. Neuroscience. 203, 122-34.
146. Telgkamp P., Raman I.M. (2002). Depression of inhibitory synaptic transmission between Purkinje cells and neurons of the cerebellar nuclei. J. Neurosci. 22, 8447-8457.
147. Telgkamp P., Padgett D.E., Ledoux V.A., Woolley C.S., Raman I.M. (2004). Maintenance of high-frequency transmission at Purkinje to cerebellar nuclear synapses by spillover from boutons with multiple release sites. Neuron 41, 113-126.
148. Teune T.M., van der Burg J., de Zeeuw C.I., Voogd J., Ruigrok T.J. (1998). Single Purkinje cell can innervate multiple classes of projection neurons in the cerebellar nuclei of the rat: a light microscopic and ultrastructural triple-tracer study in the rat. J. Comp. Neurol. 392, 164-178.
149. Thach W.T. (1968). Discharge of Purkinje and cerebellar nuclear neurons during rapidly alternating arm movements in the monkey. J. Neurophysiol. 31(5), 785-797.
150. Thach W.T. (1970a). Discharge of cerebellar neurons related to two maintained postures and two prompt movements. I. Nuclear cell output. J. Neurophysiol. 33, 527-536.
151. Thach W.T. (1970b). Discharge of cerebellar neurons related to two maintained postures and two prompt movements. II. Purkinje cell output and input. J. Neurophysiol. 33, 537-547.
152. Thach W.T. (1968). Discharge of Purkinje and cerebellar nuclear neurons during rapidly alternating arm movements in the monkey. J. Neurophysiol. 31, 785-797.
153. Thier P., Dicke P.W., Haas R., Barash S. (2000). Encoding of movement time by populations of cerebellar Purkinje cells. Nature 405, 72-76.
154. Toyama K., Tsukahara N., Kosaka K., Matsunami K. (1970). Synaptic excitation of red nucle1 us neurones by fibres from interpositus nucleus. Exp. Brain Res. 11(2), 187-198.
155. Tuner R.S., Anderson M.E. (1997). Pallidal discharge related to the kinematics of reaching movement in two dimensions. J. Neurophysiol. 77, 1051-1074.
156. Uusisaari M., Obata K, Knöpfel T. (2007). Morphological and electrophysiological properties of GABAergic and non-GABAergic cells in the deep cerebellar nuclei. J. Neurophysiol. 97,901-911.
157. Uusisaari M., Knöpfel T. (2008). GABAergic synaptic communication in the GABAergic and non-GABAergic cells in the deep cerebellar nuclei. Neuroscience. 156, 537-549.
158. Vervaeke K., Lorincz A., Gleeson P., Farinella M., Nusser Z., Silver R.A. (2010). Rapid desynchronization of an electrically coupled interneuron network with sparse excitatory synaptic input. Neuron 67, 435-451.
159. Walter J.T., Dizon M.J., Khodakhah K. (2009). The functional equivalence of ascending and parallel fiber inputs in cerebellar computation. J. Neurosci. 29, 8462-8473.
160. Walter J.T., Khodakhah K. (2006). The linear computational algorithm of cerebellar Purkinje cells. J. Neurosci. 26, 12861-12872.
161. Walter J.T., Khodakhah K. (2009). The advantages of linear information processing for cerebellar computation. Proc. Natl. Acad. Sci. USA. 106, 4471-4476.
162. Wang X.J., Buzsáki G. (1996). Gamma oscillation by synaptic inhibition in a hippocampal interneuronal network model. J. Neurosci. 16, 6402-6413.
163. Welsh J.P., Lang E.J., Sugihara I., Llinás R. (1995). Dynamic organization of motor control within the olivocerebellar system. Nature 374, 453-457.
164. Wise A.K., Cerminara N.L., Marple-Horvat D.E., Apps R. (2010). Mechanisms of synchronous activity in cerebellar Purkinje cells. J. Physiol. 588, 2373-2390.
165. Wylie, D.R., De Zeeuw, C.I., DiGiorgio, P.L., Simpson, J.I. (1994). Projections of individual Purkinje cells of identified zones in the ventral nodulus to the vestibular and cerebellar nuclei in the rabbit. J. Comp. Neurol. 349, 448-63.
166. Zhang W., Linden D.J. (2012). Calcium influx measured at single presynaptic boutons of cerebellar granule cell ascending axons and parallel fibers. Cerebellum 11, 121-131.
167. Zhang W., Linden D.J. (2006). Long-term depression at the mossy fiber-deep cerebellar nucleus synapse. J. Neurosci. 2006 Jun 28;26(26), 6935-6944.
168. Zheng N., Raman I.M. (2009). Ca currents activated by spontaneous firing and synaptic disinhibition in neurons of the cerebellar nuclei. J. Neurosci. 29, 9826-9838.
169. Zheng N., Raman I.M. (2011). Prolonged postinhibitory rebound firing in the cerebellar nuclei mediated by group I metabotropic glutamate receptor potentiation of L-type calcium currents. J. Neurosci. 31(28), 10283-10292.