The neuronal code(s) of the cerebellum

Journal of Neuroscience

Volumn 33, Issue 45, 2013, Pages 17603-17609

  Heck, Detlef H ^a   De Zeeuw, Chris I ^b,c   Jaeger, Dieter ^d   Khodakhah, Kamran ^e   Person, Abigail L ^f  

^a UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

^b ERASMUS MEDICAL CENTER   (Netherlands)

^c NETHERLANDS INSTITUTE FOR NEUROSCIENCE   (Netherlands)

^d EMORY UNIVERSITY   (United States)

^e ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

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

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BIOLOGICAL RHYTHM; BODY MOVEMENT; BRAIN ELECTROPHYSIOLOGY; BRAIN FUNCTION; BREATHING; CEREBELLUM; CEREBELLUM CORTEX; CEREBELLUM NUCLEUS; EYELID REFLEX; GRANULE CELL; HUMAN; LICKING; MOSSY FIBER; MOTOR COORDINATION; NERVE POTENTIAL; NONHUMAN; PRIORITY JOURNAL; PURKINJE CELL; SENSORIMOTOR FUNCTION; SPIKE WAVE;

ACTION POTENTIALS; ANIMALS; CEREBELLUM; NERVE NET; NEURONS; PURKINJE CELLS; SYNAPTIC TRANSMISSION;

EID: 84887086724     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2759-13.2013     Document Type: Article

References (99)

1. Albus JS (1971) A theory of cerebellar function. Math Biosci 10:25-61. CrossRef
2. Apps R, Garwicz M (2000) Precise matching of olivo-cortical divergence and cortico-nuclear convergence between somatotopically corresponding areas in the medial C1 and medial C3 zones of the paravermal cerebellum. Eur J Neurosci 12:205-214. CrossRef Medline
3. Armstrong DM, Edgley SA (1984a) Discharges of Purkinje cells in the paravermal part of the cerebellar anterior lobe during locomotion in the cat. J Physiol 352:403-424. Medline
4. Armstrong DM, Edgley SA (1984b) Discharges of nucleus interpositus neurones during locomotion in the cat. J Physiol 351:411-432. Medline
5. Badura A, Schonewille M, Voges K, Galliano E, Renier N, Gao Z, Witter L, Hoebeek FE, Chedotal A, De Zeeuw CI (2013) Climbing fiber input shapes reciprocity of Purkinje cell firing. Neuron 78:700-713. CrossRef Medline
6. Bell CC, Grimm RJ (1969) Discharge properties of Purkinje cells recorded with single and double microelectrodes. J Neurophysiol 32:1044-1055. Medline
7. Bell CC, Kawasaki T (1972) Relations among climbing fiber responses of nearby Purkinje cells. J Neurophysiol 35:155-169. Medline
8. Bosman LW, Koekkoek SK, Shapiro J, Rijken BF, Zandstra F, van der Ende B, Owens CB, Potters JW, de Gruijl JR, Ruigrok TJ, De Zeeuw CI (2010) Encoding of whisker input by cerebellar Purkinje cells. J Physiol 588: 3757-3783. CrossRef Medline
9. Bryant JL, Boughter JD, Gong S, LeDoux MS, Heck DH (2010) Cerebellar cortical output encodes temporal aspects of rhythmic licking movements and is necessary for normal licking frequency. Eur J Neurosci 32:41-52. CrossRef Medline
10. Cao Y, Maran SK, Jaeger D, Heck DH (2012a) Representation of behaviour in the cerebellum: spike rate modulation vs. spike timing. Soc Neurosci Abstract 477.07.
11. Cao Y, Maran SK, Dhamala M, Jaeger D, Heck DH (2012b) Behavior related pauses in simple spike activity of mouse Purkinje cells are linked to spike rate modulation. J Neurosci 32:8678-8685. CrossRef Medline
12. Chen X, Kovalchuk Y, Adelsberger H, Henning HA, Sausbier M, Wietzorrek G, Ruth P, Yarom Y, Konnerth A (2010) Disruption of the olivocerebellar circuit by Purkinje neuron-specific ablation of BK channels. Proc Natl Acad Sci U S A 107:12323-12328. CrossRef Medline
13. Coltz JD, Johnson MT, Ebner TJ (1999) Cerebellar Purkinje cell simple spike discharge encodes movement velocity in primates during visuomotor arm tracking. J Neurosci 19:1782-1803. Medline
14. Courtemanche R, Lamarre Y (2005) Local field potential oscillations in primate cerebellar cortex: synchronization with cerebral cortex during active and passive expectancy. J Neurophysiol 93:2039-2052. CrossRef Medline
15. Courtemanche R, Pellerin JP, Lamarre Y (2002) Local field potential oscillations in primate cerebellar cortex: modulation during active and passive expectancy. J Neurophysiol 88:771-782. Medline
16. Cramer NP, Li Y, Keller A (2007) The whisking rhythm generator: a novel mammalian network for the generation of movement. J Neurophysiol 97:2148-2158. CrossRef Medline
17. De Schutter E, Steuber V (2009) Patterns and pauses in Purkinje cell simple spike trains: experiments, modeling and theory. Neuroscience 162:816-826. CrossRef Medline
18. de Solages C, Szapiro G, Brunel N, Hakim V, Isope P, Buisseret P, Rousseau C, Barbour B, Lena C (2008) High-frequency organization and synchrony of activity in the Purkinje cell layer of the cerebellum. Neuron 58:775-788. CrossRef Medline
19. De Zeeuw CI, Holstege JC, Calkoen F, Ruigrok TJ, Voogd J (1988) A new combination of WGA-HRP anterograde tracing and GABA immunocytochemistry applied to afferents of the cat inferior olive at the ultrastructural level. Brain Res 447:369-375. CrossRef Medline
20. De Zeeuw CI, Wylie DR, Stahl JS, Simpson JI (1995) Phase relations of Purkinje cells in the rabbit flocculus during compensatory eye movements. J Neurophysiol 74:2051-2064. Medline
21. De Zeeuw CI, Koekkoek SK, Wylie DR, Simpson JI (1997) Association between dendritic lamellar bodies and complex spike synchrony in the olivocerebellar system. J Neurophysiol 77:1747-1758. Medline
22. De Zeeuw CI, Hoebeek FE, Schonewille M (2008) Causes and consequences of oscillations in the cerebellar cortex. Neuron 58:655-658. CrossRef Medline
23. De Zeeuw CI, Hoebeek FE, Bosman LW, Schonewille M, Witter L, Koekkoek SK (2011) Spatiotemporal firing patterns in the cerebellum. Nat Rev Neurosci 12:327-344. CrossRef Medline
24. Dizon MJ, Khodakhah K (2011) The role of interneurons in shaping Purkinje cell responses in the cerebellar cortex. J Neurosci 31:10463-10473. CrossRef Medline
25. Ebner TJ, Bloedel JR (1981) Correlation between activity of Purkinje cells and its modification by natural peripheral stimuli. J Neurophysiol 45: 948-961. Medline
26. Ebner TJ, Hewitt AL, Popa LS (2011) What features of limb movements are encoded in the discharge of cerebellar neurons? Cerebellum 10:683-693. CrossRef Medline
27. Ebner TJ, Wang X, Gao W, Cramer SW, Chen G (2012) Parasagittal zones in the cerebellar cortex differ in excitability, information processing, and synaptic plasticity. Cerebellum 11:418-419. CrossRef Medline
28. Eccles JC (1973) The cerebellum as a computer: patterns in space and time. J Physiol 229:1-32. Medline
29. Fatemi SH, Aldinger KA, Ashwood P, Bauman ML, Blaha CD, Blatt GJ, Chauhan A, Chauhan V, Dager SR, Dickson PE, Estes AM, Goldowitz D, Heck DH, Kemper TL, King BH, Martin LA, Millen KJ, Mittleman G, Mosconi MW, Persico AM, et al. (2012) Consensus paper: pathological role of the cerebellum in autism. Cerebellum 11:777-807. CrossRef Medline
30. Feldman JL, Mitchell GS, Nattie EE (2003) Breathing: rhythmicity, plasticity, chemosensitivity. Annu Rev Neurosci 26:239-266. CrossRef Medline
31. Fortier PA, Kalaska JF, Smith AM (1989) Cerebellar neuronal activity related to whole-arm reaching movements in the monkey. J Neurophysiol 62:198-211. Medline
32. Galliano E, Gao Z, Schonewille M, Todorov B, Simons E, Pop AS, D'Angelo E, van den Maagdenberg AM, Hoebeek FE, De Zeeuw CI (2013) Silencing the majority of cerebellar granule cells uncovers their essential role in motor learning and consolidation. Cell Rep 3:1239-1251. CrossRef Medline
33. Gao Z, van Beugen BJ, De Zeeuw CI (2012) Distributed synergistic plasticity and cerebellar learning. Nat Rev Neurosci 13:619-635. CrossRef Medline
34. 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. Medline
35. Graham DJ, Wylie DR (2012) Zebrin-immunopositive and -immunonegative stripe pairs represent functional units in the pigeon vestibulocerebellum. J Neurosci 32:12769-12779. CrossRef Medline
36. Harvey RJ, Porter R, Rawson JA (1977) The natural discharges of Purkinje cells in paravermal regions of lobules V and VI of the monkey's cerebellum. J Physiol 271:515-536. Medline
37. Hayar A, Bryant JL, Boughter JD, Heck DH (2006) A low-cost solution to measure mouse licking in an electrophysiological setup with a standard analog-to-digital converter. J Neurosci Methods 2:203-207. CrossRef Medline
38. Heck DH, Howell JW (2013) Prefrontal cortical-cerebellar interaction deficits in autism spectrum disorders. Autism 4:1. CrossRef
39. Heck DH, Thach WT, Keating JG (2007) On-beam synchrony in the cerebellum as the mechanism for the timing and coordination of movement. Proc Natl Acad Sci U S A 104:7658-7663. CrossRef Medline
40. Heck DH, Zhao Y, Roy S, LeDoux MS, Reiter LT (2008) Analysis of cerebellar function in Ube3a deficient mice reveals novel genotype specific behaviors. Hum Mol Gen 17:2181-2189. CrossRef Medline
41. Heck DH, Gu W, Cao Y, Qi S, Lacaria M, Lupski JR (2012) Opposing phenotypes in mice with Smith-Magenis deletion and Potocki-Lupski duplication syndromes suggest gene dosage effects on fluid consumption behavior. Am J Med Genet 158A:2807-2814. CrossRef Medline
42. Hoebeek FE, Witter L, Ruigrok TJ, De Zeeuw CI (2010) Differential olivocerebellar cortical control of rebound activity in the cerebellar nuclei. Proc Natl Acad Sci U S A 107:8410-8415. CrossRef Medline
43. Holdefer RN, Miller LE, Chen LL, Houk JC (2000) Functional connectivity between cerebellum and primary motor cortex in the awake monkey. J Neurophysiol 84:585-590. Medline
44. Ito M (1984) The cerebellum and neural control. New York: Raven.
45. Ito M, Yoshida M (1966) The origin of cerebellar-induced inhibition of Deiters neurons: I. Monosynaptic initiation of the inhibitory postynatic potentials. Exp Brain Res 2:330-349. Medline
46. Ito M, Yoshida M, Obata K, Kawai N, Udo M (1970) Inhibitory control of intracerebellar nuclei by the Purkinje cell axons. Exp Brain Res 10:64-80. CrossRef Medline
47. Ito M, Yoshida M, Obata K (1964) Monosynaptic inhibition of the intracerebellar nuclei induced from the cerebellar cortex. Experientia 20:575-576. CrossRef Medline
48. Kim CH, Oh SH, Lee JH, Chang SO, Kim J, Kim SJ (2012) Lobule-specific membrane excitability of cerebellar Purkinje cells. J Physiol 590:273-288. CrossRef Medline
49. Koziol LF, Budding DE, Chidekel D (2012) From movement to thought: executive function, embodied cognition, and the cerebellum. Cerebellum 11:505-525. CrossRef Medline
50. Lu L, Cao Y, Tokita K, Heck DH, Boughter JD Jr (2013) Medial cerebellar nuclear projections and activity patterns link cerebellar output to orofacial and respiratory behavior. Front Neural Circuits 7:56. CrossRef Medline
51. MacKay WA, Murphy JT (1976) Integrative versus delay line characteristics of cerebellar cortex. Can J Neurol Sci 3:85-97. Medline
52. McDevitt CJ, Ebner TJ, Bloedel JR (1987) Relationships between simultaneously recorded Purkine cells and cerebellar nuclear neurons. Brain Res 425:1-13. CrossRef Medline
53. Medina JF, Lisberger SG (2007) Variation, signal, and noise in cerebellar sensory-motor processing for smooth-pursuit eye movements. J Neurosci 27:6832-6842. CrossRef Medline
54. Mittleman G, Goldowitz D, Heck DH, Blaha CD (2008) Cerebellar modulation of frontal cortex dopamine efflux in mice: relevance to autism and schizophrenia. Synapse 62:544-550. CrossRef Medline
55. Oscarsson O (1979) Functional units of the cerebellum-sagittal zones and microzones. Trends Neurosci 2:143-145. CrossRef
56. Palay SL, Chan-Palay V (1974) Cerebellar cortex: cytology and organization. Berlin: Springer.
57. Pasalar S, Roitman AV, Durfee WK, Ebner TJ (2006) Force field effects on cerebellar Purkinje cell discharge with implications for internal models. Nat Neurosci 9:1404-1411. CrossRef Medline
58. Person AL, Raman IM (2010) Deactivation of L-type Ca current by inhibition controls LTP at excitatory synapses in the cerebellar nuclei. Neuron 66:550-559. CrossRef Medline
59. Person AL, Raman IM (2012) Purkinje neuron synchrony elicits timelocked spiking in the cerebellar nuclei. Nature 481:502-505. CrossRef Medline
60. Popa LS, Hewitt AL, Ebner TJ (2012) Predictive and feedback performance errors are signaled in the simple spike discharge of individual Purkinje cells. J Neurosci 32:15345-15358. CrossRef Medline
61. Popa LS, Hewitt AL, Ebner TJ (2013) Purkinje cell simple spike discharge encodes error signals consistent with a forward internal model. Cerebellum 12:331-333. CrossRef Medline
62. Pugh JR, Raman IM (2009) Nothing can be coincidence: synaptic inhibition and plasticity in the cerebellar nuclei. Trends Neurosci 32:170-177. CrossRef Medline
63. Raman IM, Gustafson AE, Padgett D (2000) Ionic currents and spontaneous firing in neurons isolated from the cerebellar nuclei. J Neurosci 20: 9004-9016. Medline
64. Robinson FR, Fuchs AF (2001) The role of the cerebellum in voluntary eye movements. Annu Rev Neurosci 24:981-1004. CrossRef Medline
65. Rogers TD, Dickson PE, Heck DH, Goldowitz D, Mittleman G, Blaha CD (2011) Connecting the dots of the cerebro-cerebellar role in cognitive function: neuronal pathways for cerebellar modulation of dopamine release in the prefrontal cortex. Synapse 65:1204-1212. CrossRef Medline
66. Rogers TD, Dickson PE, McKimm E, Heck DH, Goldowitz D, Blaha CD, Mittleman G (2013) Reorganization of circuits underlying cerebellar modulation of prefrontal cortical dopamine in mouse models of autism spectrum disorder. Cerebellum 12:547-556. CrossRef Medline
67. Roitman AV, Pasalar S, Johnson MT, Ebner TJ (2005) Position, direction of movement, and speed tuning of cerebellar Purkinje cells during circular manual tracking in monkey. J Neurosci 25:9244-9257. CrossRef Medline
68. Roy S, Zhao Y, Allensworth M, Farook MF, LeDoux MS, Reiter LT, Heck DH (2011) Comprehensive motor testing in Fmr1-KO mice exposes temporal defects in oromotor coordination. Behav Neurosci 125:962-969. CrossRef Medline
69. Schmahmann JD, Caplan D (2006) Cognition, emotion and the cerebellum. Brain 129:290-292. CrossRef Medline
70. Schonewille M, Belmeguenai A, Koekkoek SK, Houtman SH, Boele HJ, van Beugen BJ, Gao Z, Badura A, Ohtsuki G, Amerika WE, Hosy E, Hoebeek FE, Elgersma Y, Hansel C, De Zeeuw CI (2010) Purkinje cell-specific knockout of the protein phosphatase PP2B impairs potentiation and cerebellar motor learning. Neuron 67:618-628. CrossRef Medline
71. Schonewille M, Gao Z, Boele HJ, Veloz MF, Amerika WE, Simek AA, De Jeu MT, Steinberg JP, Takamiya K, Hoebeek FE, Linden DJ, Huganir RL, De Zeeuw CI (2011) Reevaluating the role of LTD in cerebellar motor learning. Neuron 70:43-50. CrossRef Medline
72. Shidara M, Kawano K, Gomi H, Kawato M (1993) Inverse-dynamics model eye movement control by Purkinje cells in the cerebellum. Nature 365: 50-52. CrossRef Medline
73. Shin SL, De Schutter E (2006) Dynamic synchronization of Purkinje cell simple spikes. J Neurophysiol 96:3485-3491. CrossRef Medline
74. Shinoda Y, Sugiuchi Y, Futami T, Izawa R (1992) Axon collaterals of mossy fibers from the pontine nucleus in the cerebellar dentate nucleus. J Neurophysiol 67:547-560. Medline
75. Smith AM, Dugas C, Fortier P, Kalaska J, Picard N (1993) Comparing cerebellar and motor cortical activity in reaching and grasping. Can J Neurol Sci 20 [Suppl 3]:S53-S61.
76. Steuber V, Schultheiss NW, Silver RA, De Schutter E, Jaeger D (2011) Determinants of synaptic integration and heterogeneity in rebound firing explored with data-driven models of deep cerebellar nucleus cells. J Comput Neurosci 30:633-658. CrossRef Medline
77. Stoodley CJ (2011) The cerebellum and cognition: evidence from functional imaging studies. Cerebellum 11:362-365. CrossRef Medline
78. Strata P (ed.) (1989) The olivocerebellar system in motor-control. Berlin: Springer.
79. Sugihara I, Marshall SP, Lang EJ (2007) Relationship of complex spike synchrony bands and climbing fiber projection determined by reference to aldolase C compartments in crus IIa of the rat cerebellar cortex. J Comp Neurol 501:13-29. CrossRef Medline
80. Ten Brinke M, Boele H, De Zeeuw CI (2013) Combining single unit electrophysiology and eyeblink conditioning in (transgenic) mice to elucidate molecular mechanisms underlying cerebellar learning. Abstract, Gordon Conference on Cerebellum. Aug. 11-16, 2013, New London, NH.
81. Thach WT (1968) Discharge of cerebellar Purkinje and nuclear neurons during rapidly alternating arm movements in the monkey. J Neurophysiol 31:785-797. Medline
82. Thach WT (1970a) Discharge of cerebellar neurons related to two maintained postures and two prompt movements: II. Purkinje cell output and input. J Neurophysiol 33:537-547. Medline
83. Thach WT (1970b) Discharge of derebellar neurons related to two maintained postures and two prompt movements: I. Nuclear cell output. J Neurophysiol 33:527-536. Medline
84. Thach WT (1972) Cerebellar output: properties, synthesis and uses. Brain Res 40:89-102. CrossRef Medline
85. Thach WT (1978) Correlation of neural discharge with pattern and force of muscular activity, joint position, and direction of intended next movement in motor cortex and cerebellum. J Neurophysiol 41:654-676. Medline
86. Thier P, Dicke PW, Haas R, Barash S (2000) Encoding of movement time by populations of cerebellar Purkinje cells. Nature 405:72-76. CrossRef Medline
87. Travers JB, Dinardo LA, Karimnamazi H (1997) Motor and premotor mechanisms of licking. Neurosci Biobehav Rev 21:631-647. CrossRef Medline
88. Van Der Giessen RS, Koekkoek SK, van Dorp S, De Gruijl JR, Cupido A, Khosrovani S, Dortland B, Wellershaus K, Degen J, Deuchars J, Fuchs EC, Monyer H, Willecke K, De Jeu MT, De Zeeuw CI (2008) Role of olivary electrical coupling in cerebellar motor learning. Neuron 58:599-612. CrossRef Medline
89. Voogd J, Barmack NH (2006) Oculomotor cerebellum. Prog Brain Res 151: 231-268. CrossRef Medline
90. Voogd J, Schraa-Tam CK, van der Geest JN, De Zeeuw CI (2012) Visuomotor cerebellum in human and nonhuman primates. Cerebellum 11:392-410. CrossRef Medline
91. Wadiche JI, Jahr CE (2005) Patterned expression of Purkinje cell glutamate transporters controls synaptic plasticity. Nat Neurosci 8:1329-1334. CrossRef Medline
92. Walter JT, Khodakhah K (2009) The advantages of linear information processing for cerebellar computation. Proc Natl Acad Sci U S A 106:4471-4476. CrossRef Medline
93. Weijnen JA, Wouters J, van Hest JM (1984) Interaction between licking and swallowing in the drinking rat. Brain Behav Evol 25:117-127. CrossRef Medline
94. Welsh JP, Lang EJ, Suglhara I, Llinas R (1995) Dynamic organization of motor control within the olivocerebellar system. Nature 374:453-457. CrossRef Medline
95. Welzl H, Bures J (1977) Lick-synchronized breathing in rats. Physiol Behav 18:751-753. CrossRef Medline
96. Wise AK, Cerminara NL, Marple-Horvat DE, Apps R (2010) Mechanisms of synchronous activity in cerebellar Purkinje cells. J Physiol 588:2373-2390. CrossRef Medline
97. Witter L, Canto CB, Hoogland TM, de Gruijl JR, De Zeeuw CI (2013) Strength and timing of motor responses mediated by rebound firing in the cerebellar nuclei after Purkinje cell activation. Front Neural Circuits 7:133. CrossRef Medline
98. Wulff P, Schonewille M, Renzi M, Viltono L, Sassoe-Pognetto M, Badura A, Gao Z, Hoebeek FE, van Dorp S, Wisden W, Farrant M, De Zeeuw CI (2009) Synaptic inhibition of Purkinje cells mediates consolidation of vestibulo-cerebellar motor learning. Nat Neurosci 12:1042-1049. CrossRef Medline
99. Zhou H, Lin Z, Voges K, Gao Z, Ruigrok TJ, Hoebeek FE, De Zeeuw CI, Schonewille M (2013) Cerebellar modules operate at different frequencies. Abstract, Gordon Conference on Cerebellum, Aug. 11-16, 2013, New London, NH.