Role of Olivary Electrical Coupling in Cerebellar Motor Learning

Neuron

Volumn 58, Issue 4, 2008, Pages 599-612

  Van Der Giessen, Ruben S ^a   Koekkoek, Sebastiaan K ^a   van Dorp, Stijn ^a,e   De Gruijl, Jornt R ^a,e   Cupido, Alexander ^a   Khosrovani, Sara ^a   Dortland, Bjorn ^a   Wellershaus, Kerstin ^b   Degen, Joachim ^b   Deuchars, Jim ^c   Fuchs, Elke C ^d   Monyer, Hannah ^d   Willecke, Klaus ^b   De Jeu, Marcel T G ^a   De Zeeuw, Chris I ^a,e  

^a ERASMUS MEDICAL CENTER   (Netherlands)

^b UNIVERSITY OF BONN   (Germany)

^c UNIVERSITY OF LEEDS   (United Kingdom)

^d Interdisciplinary Center for Neuroscience   (Germany)

^e NETHERLANDS INSTITUTE FOR NEUROSCIENCE   (Netherlands)

Author keywords

MOLNEURO; SYSNEURO

Indexed keywords

ACTION POTENTIAL; ANIMAL EXPERIMENT; ARTICLE; CELL INTERACTION; CEREBELLUM; COMPUTER SIMULATION; ELECTRICITY; EYELID REFLEX; GAP JUNCTION; IN VIVO STUDY; LATENT PERIOD; LEARNING; LOCOMOTION; MOTOR CONTROL; MOTOR PERFORMANCE; MOUSE; NONHUMAN; OLIVARY NUCLEUS; OSCILLATION; PRIORITY JOURNAL; SPIKE WAVE; STIMULUS; WHOLE CELL; WILD TYPE;

ACOUSTIC STIMULATION; ACTION POTENTIALS; ANIMALS; BLINKING; CEREBELLUM; COMPUTER SIMULATION; CONNEXINS; GAP JUNCTIONS; LEARNING; LOCOMOTION; MICE; MICE, KNOCKOUT; MODELS, NEUROLOGICAL; NEURONS; OLIVARY NUCLEUS; PATCH-CLAMP TECHNIQUES; REACTION TIME; TIME FACTORS;

EID: 43449090660     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuron.2008.03.016     Document Type: Article

References (65)

1. Bengtsson F., and Hesslow G. Cerebellar control of the inferior olive. Cerebellum 5 (2006) 7-14
2. Bennett M.V., and Zukin R.S. Electrical coupling and neuronal synchronization in the Mammalian brain. Neuron 41 (2004) 495-511
3. Blenkinsop T.A., and Lang E.J. Block of inferior olive gap junctional coupling decreases Purkinje cell complex spike synchrony and rhythmicity. J. Neurosci. 26 (2006) 1739-1748
4. Buhl D.L., Harris K.D., Hormuzdi S.G., Monyer H., and Buzsaki G. Selective impairment of hippocampal gamma oscillations in connexin-36 knock-out mouse in vivo. J. Neurosci. 23 (2003) 1013-1018
5. Bullock T.H., Bennett M.V., Johnston D., Josephson R., Marder E., and Fields R.D. Neuroscience. The neuron doctrine, redux. Science 310 (2005) 791-793
6. Chorev E., Yarom Y., and Lampl I. Rhythmic episodes of subthreshold membrane potential oscillations in the rat inferior olive nuclei in vivo. J. Neurosci. 27 (2007) 5043-5052
7. Coesmans M., Weber J.T., De Zeeuw C.I., and Hansel C. Bidirectional parallel fiber plasticity in the cerebellum under climbing fiber control. Neuron 44 (2004) 691-700
8. Condorelli D.F., Parenti R., Spinella F., Trovato Salinaro A., Belluardo N., Cardile V., and Cicirata F. Cloning of a new gap junction gene (Cx36) highly expressed in mammalian brain neurons. Eur. J. Neurosci. 10 (1998) 1202-1208
9. Connors B.W., and Long M.A. Electrical synapses in the mammalian brain. Annu. Rev. Neurosci. 27 (2004) 393-418
10. Cruikshank S.J., Hopperstad M., Younger M., Connors B.W., Spray D.C., and Srinivas M. Potent block of Cx36 and Cx50 gap junction channels by mefloquine. Proc. Natl. Acad. Sci. USA 101 (2004) 12364-12369
11. De Zeeuw C.I., and Yeo C.H. Time and tide in cerebellar memory formation. Curr. Opin. Neurobiol. 15 (2005) 667-674
12. De Zeeuw C.I., Hertzberg E.L., and Mugnaini E. The dendritic lamellar body: a new neuronal organelle putatively associated with dendrodendritic gap junctions. J. Neurosci. 15 (1995) 1587-1604
13. De Zeeuw C.I., Simpson J.I., Hoogenraad C.C., Galjart N., Koekkoek S.K., and Ruigrok T.J. Microcircuitry and function of the inferior olive. Trends Neurosci. 21 (1998) 391-400
14. De Zeeuw C.I., Chorev E., Devor A., Manor Y., Van Der Giessen R.S., De Jeu M.T., Hoogenraad C.C., Bijman J., Ruigrok T.J., French P., et al. Deformation of network connectivity in the inferior olive of connexin 36-deficient mice is compensated by morphological and electrophysiological changes at the single neuron level. J. Neurosci. 23 (2003) 4700-4711
15. Deans M.R., Gibson J.R., Sellitto C., Connors B.W., and Paul D.L. Synchronous activity of inhibitory networks in neocortex requires electrical synapses containing connexin36. Neuron 31 (2001) 477-485
16. Deans M.R., Volgyi B., Goodenough D.A., Bloomfield S.A., and Paul D.L. Connexin36 is essential for transmission of rod-mediated visual signals in the mammalian retina. Neuron 36 (2002) 703-712
17. Degen J., Meier C., Van Der Giessen R.S., Sohl G., Petrasch-Parwez E., Urschel S., Dermietzel R., Schilling K., De Zeeuw C.I., and Willecke K. Expression pattern of lacZ reporter gene representing connexin36 in transgenic mice. J. Comp. Neurol. 473 (2004) 511-525
18. Frisch C., De Souza-Silva M.A., Sohl G., Guldenagel M., Willecke K., Huston J.P., and Dere E. Stimulus complexity dependent memory impairment and changes in motor performance after deletion of the neuronal gap junction protein connexin36 in mice. Behav. Brain Res. 157 (2005) 177-185
19. Garcia K.S., and Mauk M.D. Pharmacological analysis of cerebellar contributions to the timing and expression of conditioned eyelid responses. Neuropharmacology 37 (1998) 471-480
20. Gareri P., Condorelli D., Belluardo N., Citraro R., Barresi V., Trovato-Salinato A., Mudò G., Ibbadu G.F., Russo E., and De Sarro G. Antiabsence effects of carbenoxolone in two genetic animal models of absence epilepsy (WAG/Rij rats and lh/lh mice). Neuropharmacology 49 (2005) 551-563
21. Guldenagel M., Ammermuller J., Feigenspan A., Teubner B., Degen J., Sohl G., Willecke K., and Weiler R. Visual transmission deficits in mice with targeted disruption of the gap junction gene connexin36. J. Neurosci. 21 (2001) 6036-6044
22. Hesslow G. Correspondence between climbing fibre input and motor output in eyeblink-related areas in cat cerebellar cortex. J. Physiol. 476 (1994) 229-244
23. Hesslow G., Svensson P., and Ivarsson M. Learned movements elicited by direct stimulation of cerebellar mossy fiber afferents. Neuron 24 (1999) 179-185
24. Kenyon G.T., Medina J.F., and Mauk M.D. A mathematical model of the cerebellar-olivary system I: self-regulating equilibrium of climbing fiber activity. J. Comput. Neurosci. 5 (1998) 17-33
25. Kistler W.M., De Jeu M.T., Elgersma Y., Van Der Giessen R.S., Hensbroek R., Luo C., Koekkoek S.K., Hoogenraad C.C., Hamers F.P., Gueldenagel M., et al. Analysis of Cx36 knockout does not support tenet that olivary gap junctions are required for complex spike synchronization and normal motor performance. Ann. N Y Acad. Sci. 978 (2002) 391-404
26. Khosrovani S., Van Der Giessen R.S., De Zeeuw C.I., and De Jeu M.T. In vivo mouse inferior olive neurons exhibit heterogeneous subthreshold oscillations and spiking patterns. Proc. Natl. Acad. Sci. USA 104 (2007) 15911-15916
27. Koekkoek S.K., Den Ouden W.L., Perry G., Highstein S.M., and De Zeeuw C.I. Monitoring kinetic and frequency-domain properties of eyelid responses in mice with magnetic distance measurement technique. J. Neurophysiol. 88 (2002) 2124-2133
28. Koekkoek S.K., Hulscher H.C., Dortland B.R., Hensbroek R.A., Elgersma Y., Ruigrok T.J., and De Zeeuw C.I. Cerebellar LTD and learning-dependent timing of conditioned eyelid responses. Science 301 (2003) 1736-1739
29. Koekkoek S.K., Yamaguchi K., Milojkovic B.A., Dortland B.R., Ruigrok T.J., Maex R., De Graaf W., Smit A.E., VanderWerf F., Bakker C.E., et al. Deletion of FMR1 in Purkinje cells enhances parallel fiber LTD, enlarges spines, and attenuates cerebellar eyelid conditioning in Fragile X syndrome. Neuron 47 (2005) 339-352
30. Landisman C.E., Long M.A., Beierlein M., Deans M.R., Paul D.L., and Connors B.W. Electrical synapses in the thalamic reticular nucleus. J. Neurosci. 22 (2002) 1002-1009
31. Lang E.J., Sugihara I., and Llinas R. GABAergic modulation of complex spike activity by the cerebellar nucleoolivary pathway in rat. J. Neurophysiol. 76 (1996) 255-275
32. Leznik E., and Llinas R. Role of gap junctions in synchronized neuronal oscillations in the inferior olive. J. Neurophysiol. 94 (2005) 2447-2456
33. Leznik E., Makarenko V., and Llinas R. Electrotonically mediated oscillatory patterns in neuronal ensembles: an in vitro voltage-dependent dye-imaging study in the inferior olive. J. Neurosci. 22 (2002) 2804-2815
34. Llinas R., and Yarom Y. Electrophysiology of mammalian inferior olivary neurones in vitro. Different types of voltage-dependent ionic conductances. J. Physiol. 315 (1981) 549-567
35. Llinas R., and Sasaki K. The functional organization of the olivo-cerebellar system as examined by multiple purkinje cell recordings. Eur. J. Neurosci. 1 (1989) 587-602
36. Long M.A., Deans M.R., Paul D.L., and Connors B.W. Rhythmicity without synchrony in the electrically uncoupled inferior olive. J. Neurosci. 22 (2002) 10898-10905
37. Long M.A., Jutras M.J., Connors B.W., and Burwell R.D. Electrical synapses coordinate activity in the suprachiasmatic nucleus. Nat. Neurosci. 8 (2005) 61-66
38. Mann-Metzer P., and Yarom Y. Electrotonic coupling interacts with intrinsic properties to generate synchronized activity in cerebellar networks of inhibitory interneurons. J. Neurosci. 19 (1999) 3298-3306
39. Margineanu D.G., and Klitgaard H. The connexin 36 blockers quinine, quinidine and mefloquine inhibit cortical spreading depression in a rat neocortical slice model in vitro. Brain Res. Bull. 71 (2006) 23-28
40. Marshall S.P., Van Der Giessen R.S., De Zeeuw C.I., and Lang E.J. Altered olivocerebellar activity patterns in the connexin36 knockout mouse. Cerebellum 6 (2007) 287-299
41. Martin F.C., and Handforth A. Carbenoxolone and mefloquine suppress tremor in the harmaline mouse model of essential tremor. Mov. Disord. 21 (2006) 1641-1649
42. Mauk M.D., and Donegan N.H. A model of Pavlovian eyelid conditioning based on the synaptic organization of the cerebellum. Learn. Mem. 4 (1997) 130-158
43. Mauk M.D., Steinmetz J.E., and Thompson R.F. Classical conditioning using stimulation of the inferior olive as the unconditioned stimulus. Proc. Natl. Acad. Sci. USA 83 (1986) 5349-5353
44. Medina J.F., and Mauk M.D. Computer simulation of cerebellar information processing. Nat. Neurosci. 3 Suppl (2000) 1205-1211
45. Medina J.F., Nores W.L., and Mauk M.D. Inhibition of climbing fibres is a signal for the extinction of conditioned eyelid responses. Nature 416 (2002) 330-333
46. Perrett S.P., Ruiz B.P., and Mauk M.D. Cerebellar cortex lesions disrupt learning-dependent timing of conditioned eyelid responses. J. Neurosci. 13 (1993) 1708-1718
47. Pijpers A., Voogd J., and Ruigrok T.J. Topography of olivo-cortico-nuclear modules in the intermediate cerebellum of the rat. J. Comp. Neurol. 492 (2005) 193-213
48. Placantonakis D.G., Bukovsky A.A., Zeng X.H., Kiem H.P., and Welsh J.P. Fundamental role of inferior olive connexin 36 in muscle coherence during tremor. Proc. Natl. Acad. Sci. USA 101 (2004) 7164-7169
49. Placantonakis D.G., Bukovsky A.A., Aicher S.A., Kiem H.P., and Welsh J.P. Continuous electrical oscillations emerge from a coupled network: a study of the inferior olive using lentiviral knockdown of connexin36. J. Neurosci. 26 (2006) 5008-5016
50. Porras-Garcia E., Cendelin J., Dominguez-del-Toro E., Vozeh F., and Delgado-Garcia J.M. Purkinje cell loss affects differentially the execution, acquisition and prepulse inhibition of skeletal and facial motor responses in Lurcher mice. Eur. J. Neurosci. 21 (2005) 979-988
51. Raymond J.L., Lisberger S.G., and Mauk M.D. The cerebellum: a neuronal learning machine?. Science 272 (1996) 1126-1131
52. Rozental R., Srinivas M., and Spray D.C. How to close a gap junction channel. Efficacies and potencies of uncoupling agents. Methods Mol. Biol. 154 (2001) 447-476
53. Ruigrok T.J.H., and Voogd J. Cerebellar influence on olivary excitability in the cat. Eur. J. Neurosci. 7 (1995) 679-693
54. Ruigrok T.J., and Voogd J. Organization of projections from the inferior olive to the cerebellar nuclei in the rat. J. Comp. Neurol. 426 (2000) 209-228
55. Ruigrok T.J., and Apps R. A light microscope-based double retrograde tracer strategy to chart central neuronal connections. Nat. Protocols 2 (2007) 1869-1878
56. Saffitz J.E., Laing J.G., and Yamada K.A. Connexin expression and turnover: implications for cardiac excitability. Circ. Res. 86 (2000) 723-728
57. Schweighofer N., Doya K., and Kawato M. Electrophysiological properties of inferior olive neurons: A compartmental model. J. Neurophysiol. 82 (1999) 804-817
58. Seto-Ohshima A., Emson P.C., Berchtold M.W., and Heizmann C.W. Localization of parvalbumin mRNA in rat brain by in situ hybridization histochemistry. Exp. Brain Res. 75 (1989) 653-658
59. Simpson J.I., Wylie D.R., and De Zeeuw C.I. On climbing fiber signals and their consequences. Behav. Brain Sci. 19 (1996) 380-395
60. Sohl G., Degen J., Teubner B., and Willecke K. The murine gap junction gene connexin36 is highly expressed in mouse retina and regulated during brain development. FEBS Lett. 428 (1998) 27-31
61. Theis M., Magin T.M., Plum A., and Willecke K. General or cell type-specific deletion and replacement of connexin-coding DNA in the mouse. Methods 20 (2000) 205-218
62. Van Alphen A.M., Schepers T., Luo C., and De Zeeuw C.I. Motor performance and motor learning in Lurcher mice. Ann. N Y Acad. Sci. 978 (2002) 413-424
63. Van Der Giessen R.S., Maxeiner S., French P.J., Willecke K., and De Zeeuw C.I. Spatiotemporal distribution of Connexin45 in the olivocerebellar system. J. Comp. Neurol. 495 (2006) 173-184
64. Voogd J., and Glickstein M. The anatomy of the cerebellum. Trends Neurosci. 21 (1998) 370-375
65. Wang S.S., Denk W., and Hausser M. Coincidence detection in single dendritic spines mediated by calcium release. Nat. Neurosci. 3 (2000) 1266-1273