Synaptically induced long-term modulation of electrical coupling in the inferior olive

Neuron

Volumn 81, Issue 6, 2014, Pages 1290-1296

  Mathy, Alexandre ^a   Clark, Beverley A ^a   Häusser, Michael ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ION; N METHYL DEXTRO ASPARTIC ACID RECEPTOR;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN FUNCTION; BRAIN REGION; CALCIUM SIGNALING; CONTROLLED STUDY; ELECTROSTIMULATION; FUNCTIONAL ASSESSMENT; INFERIOR OLIVE; LONG TERM DEPRESSION; MOLECULAR DYNAMICS; NERVE CELL PLASTICITY; NEUROMODULATION; NONHUMAN; PATCH CLAMP TECHNIQUE; POSTSYNAPTIC POTENTIAL; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN FUNCTION; RAT; SPIKE WAVE; STIMULUS RESPONSE; SYNAPTIC POTENTIAL; SYNAPTIC TRANSMISSION; CALCIUM TRANSPORT; ELECTRICAL COUPLING; ELECTRICAL SYNAPSE; EXCITATORY POSTSYNAPTIC POTENTIAL; HOMEOSTASIS; NERVOUS SYSTEM FUNCTION; ANIMAL; CYTOLOGY; GAP JUNCTION; NERVE CELL; OLIVARY NUCLEUS; PHYSIOLOGY; SYNAPSE;

ANIMALS; EXCITATORY POSTSYNAPTIC POTENTIALS; GAP JUNCTIONS; LONG-TERM SYNAPTIC DEPRESSION; NEURONAL PLASTICITY; NEURONS; OLIVARY NUCLEUS; RATS; SYNAPSES; SYNAPTIC TRANSMISSION;

EID: 84896301837     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2014.01.005     Document Type: Article

References (58)

1. Alev C., Urschel S., Sonntag S., Zoidl G., Fort A.G., Höher T., Matsubara M., Willecke K., Spray D.C., Dermietzel R. The neuronal connexin36 interacts with and is phosphorylated by CaMKII in a way similar toCaMKII interaction with glutamate receptors. Proc. Natl. Acad. Sci. USA 2008, 105:20964-20969.
2. Apps R., Garwicz M. Anatomical and physiological foundations of cerebellar information processing. Nat. Rev. Neurosci. 2005, 6:297-311.
3. Armstrong D.M., Rawson J.A. Activity patterns of cerebellar cortical neurones and climbing fibre afferents in the awake cat. J.Physiol. 1979, 289:425-448.
4. Bartos M., Vida I., Frotscher M., Meyer A., Monyer H., Geiger J.R., Jonas P. Fast synaptic inhibition promotes synchronized gamma oscillations in hippocampal interneuron networks. Proc. Natl. Acad. Sci. USA 2002, 99:13222-13227.
5. Bazzigaluppi P., Ruigrok T., Saisan P., De Zeeuw C.I., de Jeu M. Properties of the nucleo-olivary pathway: an invivo whole-cell patch clamp study. PLoS ONE 2012, 7:e46360.
6. Beierlein M., Gibson J.R., Connors B.W. A network of electrically coupled interneurons drives synchronized inhibition in neocortex. Nat. Neurosci. 2000, 3:904-910.
7. Bennett M.V., Zukin R.S. Electrical coupling and neuronal synchronization in the Mammalian brain. Neuron 2004, 41:495-511.
8. Blenkinsop T.A., Lang E.J. Block of inferior olive gap junctional coupling decreases Purkinje cell complex spike synchrony and rhythmicity. J.Neurosci. 2006, 26:1739-1748.
9. Bliss T.V., Collingridge G.L. A synaptic model of memory: long-term potentiation in the hippocampus. Nature 1993, 361:31-39.
10. Boyden E.S., Katoh A., Raymond J.L. Cerebellum-dependent learning: the role of multiple plasticity mechanisms. Annu. Rev. Neurosci. 2004, 27:581-609.
11. Cachope R., Mackie K., Triller A., O'Brien J., Pereda A.E. Potentiation of electrical and chemical synaptic transmission mediated by endocannabinoids. Neuron 2007, 56:1034-1047.
12. Chorev E., Yarom Y., Lampl I. Rhythmic episodes of subthreshold membrane potential oscillations in the rat inferior olive nuclei invivo. J.Neurosci. 2007, 27:5043-5052.
13. Connors B.W., Long M.A. Electrical synapses in the mammalian brain. Annu. Rev. Neurosci. 2004, 27:393-418.
14. De Gruijl J.R., Bazzigaluppi P., de Jeu M.T., De Zeeuw C.I. Climbing fiber burst size and olivary sub-threshold oscillations in a network setting. PLoS Comput. Biol. 2012, 8:e1002814.
15. de Zeeuw C.I., Holstege J.C., Ruigrok T.J., Voogd J. Ultrastructural study of the GABAergic, cerebellar, and mesodiencephalic innervation of the cat medial accessory olive: anterograde tracing combined with immunocytochemistry. J.Comp. Neurol. 1989, 284:12-35.
16. de Zeeuw C.I., Holstege J.C., Ruigrok T.J., Voogd J. Mesodiencephalic and cerebellar terminals terminate upon the same dendritic spines in the glomeruli of the cat and rat inferior olive: an ultrastructural study using a combination of [3H]leucine and wheat germ agglutinin coupled horseradish peroxidase anterograde tracing. Neuroscience 1990, 34:645-655.
17. de Zeeuw C.I., Ruigrok T.J., Holstege J.C., Jansen H.G., Voogd J. Intracellular labeling of neurons in the medial accessory olive of the cat: II. Ultrastructure of dendritic spines and their GABAergic innervation. J.Comp. Neurol. 1990, 300:478-494.
18. De Zeeuw C.I., Simpson J.I., Hoogenraad C.C., Galjart N., Koekkoek S.K., Ruigrok T.J. Microcircuitry and function of the inferior olive. Trends Neurosci. 1998, 21:391-400.
19. Deans M.R., Gibson J.R., Sellitto C., Connors B.W., Paul D.L. Synchronous activity of inhibitory networks in neocortex requires electrical synapses containing connexin36. Neuron 2001, 31:477-485.
20. Devor A., Yarom Y. Electrotonic coupling in the inferior olivary nucleus revealed by simultaneous double patch recordings. J.Neurophysiol. 2002, 87:3048-3058.
21. Gibson J.R., Beierlein M., Connors B.W. Two networks of electrically coupled inhibitory neurons in neocortex. Nature 1999, 402:75-79.
22. Haas J.S., Zavala B., Landisman C.E. Activity-dependent long-term depression of electrical synapses. Science 2011, 334:389-393.
23. Hansel C., Linden D.J., D'Angelo E. Beyond parallel fiber LTD: the diversity of synaptic and non-synaptic plasticity in the cerebellum. Nat. Neurosci. 2001, 4:467-475.
24. Hestrin S., Galarreta M. Electrical synapses define networks of neocortical GABAergic neurons. Trends Neurosci. 2005, 28:304-309.
25. Hoge G.J., Davidson K.G., Yasumura T., Castillo P.E., Rash J.E., Pereda A.E. The extent and strength of electrical coupling between inferior olivary neurons is heterogeneous. J.Neurophysiol. 2011, 105:1089-1101.
26. Horikawa K., Armstrong W.E. A versatile means of intracellular labeling: injection of biocytin and its detection with avidin conjugates. J.Neurosci. Methods 1988, 25:1-11.
27. Jacobson G.A., Rokni D., Yarom Y. A model of the olivo-cerebellar system as a temporal pattern generator. Trends Neurosci. 2008, 31:617-625.
28. Khosrovani S., Van Der Giessen R.S., De Zeeuw C.I., De Jeu M.T. Invivo mouse inferior olive neurons exhibit heterogeneous subthreshold oscillations and spiking patterns. Proc. Natl. Acad. Sci. USA 2007, 104:15911-15916.
29. Kothmann W.W., Massey S.C., O'Brien J. Dopamine-stimulated dephosphorylation of connexin 36 mediates AII amacrine cell uncoupling. J.Neurosci. 2009, 29:14903-14911.
30. Kothmann W.W., Trexler E.B., Whitaker C.M., Li W., Massey S.C., O'Brien J. Nonsynaptic NMDA receptors mediate activity-dependent plasticity of gap junctional coupling in the AII amacrine cell network. J.Neurosci. 2012, 32:6747-6759.
31. Landisman C.E., Connors B.W. Long-term modulation of electrical synapses in the mammalian thalamus. Science 2005, 310:1809-1813.
32. Lang E.J. GABAergic and glutamatergic modulation of spontaneous and motor-cortex-evoked complex spike activity. J.Neurophysiol. 2002, 87:1993-2008.
33. Lang E.J., Sugihara I., Llinás R. GABAergic modulation ofcomplex spike activity by the cerebellar nucleoolivary pathway in rat. J.Neurophysiol. 1996, 76:255-275.
34. Lang E.J., Sugihara I., Welsh J.P., Llinás R. Patterns of spontaneous purkinje cell complex spike activity in the awake rat. J.Neurosci. 1999, 19:2728-2739.
35. Leznik E., Llinás R. Role of gap junctions in synchronized neuronal oscillations in the inferior olive. J.Neurophysiol. 2005, 94:2447-2456.
36. Lisman J., Schulman H., Cline H. The molecular basis of CaMKII function in synaptic and behavioural memory. Nat. Rev. Neurosci. 2002, 3:175-190.
37. Llinás R. Eighteenth Bowditch lecture. Motor aspects of cerebellar control. Physiologist 1974, 17:19-46.
38. Llinas R., Baker R., Sotelo C. Electrotonic coupling between neurons in cat inferior olive. J.Neurophysiol. 1974, 37:560-571.
39. Long M.A., Deans M.R., Paul D.L., Connors B.W. Rhythmicity without synchrony in the electrically uncoupled inferior olive. J.Neurosci. 2002, 22:10898-10905.
40. Malenka R.C., Bear M.F. LTP and LTD: an embarrassment of riches. Neuron 2004, 44:5-21.
41. Manor Y., Rinzel J., Segev I., Yarom Y. Low-amplitude oscillations in the inferior olive: a model based on electrical coupling of neurons with heterogeneous channel densities. J.Neurophysiol. 1997, 77:2736-2752.
42. Marshall S.P., Lang E.J. Local changes in the excitability of thecerebellar cortex produce spatially restricted changes in complex spike synchrony. J.Neurosci. 2009, 29:14352-14362.
43. Marshall S.P., van der Giessen R.S., de Zeeuw C.I., Lang E.J. Altered olivocerebellar activity patterns in the connexin36 knockout mouse. Cerebellum 2007, 6:287-299.
44. Mathy A., Ho S.S., Davie J.T., Duguid I.C., Clark B.A., Häusser M. Encoding of oscillations by axonal bursts in inferior olive neurons. Neuron 2009, 62:388-399.
45. Mills S.L., Massey S.C. Differential properties of two gap junctional pathways made by AII amacrine cells. Nature 1995, 377:734-737.
46. Payton B.W., Bennett M.V., Pappas G.D. Temperature-dependence of resistance at an electrotonic synapse. Science 1969, 165:594-597.
47. Pereda A.E., Faber D.S. Activity-dependent short-term enhancement of intercellular coupling. J.Neurosci. 1996, 16:983-992.
48. 2+/calmodulin-dependent kinase II mediates simultaneous enhancement of gap-junctional conductance and glutamatergic transmission. Proc. Natl. Acad. Sci. USA 1998, 95:13272-13277.
49. Rash J.E., Dillman R.K., Bilhartz B.L., Duffy H.S., Whalen L.R., Yasumura T. Mixed synapses discovered and mapped throughout mammalian spinal cord. Proc. Natl. Acad. Sci. USA 1996, 93:4235-4239.
50. Sloper J.J., Powell T.P. Gap junctions between dendrites and somata of neurons in the primate sensori-motor cortex. Proc. R. Soc. Lond. B Biol. Sci. 1978, 203:39-47.
51. Smith M., Pereda A.E. Chemical synaptic activity modulates nearby electrical synapses. Proc. Natl. Acad. Sci. USA 2003, 100:4849-4854.
52. Sotelo C., Llinas R., Baker R. Structural study of inferior olivary nucleus of the cat: morphological correlates of electrotonic coupling. J.Neurophysiol. 1974, 37:541-559.
53. Stuart G.J., Dodt H.U., Sakmann B. Patch-clamp recordings from the soma and dendrites of neurons in brain slices using infrared video microscopy. Pflugers Arch. 1993, 423:511-518.
54. 2+/calmodulin-dependent protein kinase II. J.Biol. Chem. 1990, 265:4315-4320.
55. Van Der Giessen R.S., Koekkoek S.K., van Dorp S., De Gruijl J.R., Cupido A., Khosrovani S., Dortland B., Wellershaus K., Degen J., Deuchars J., et al. Role of olivary electrical coupling in cerebellar motor learning. Neuron 2008, 58:599-612.
56. Vervaeke K., Lorincz A., Gleeson P., Farinella M., Nusser Z., Silver R.A. Rapid desynchronization of an electrically coupled interneuron network with sparse excitatory synaptic input. Neuron 2010, 67:435-451.
57. Wise A.K., Cerminara N.L., Marple-Horvat D.E., Apps R. Mechanisms of synchronous activity in cerebellar Purkinje cells. J.Physiol. 2010, 588:2373-2390.
58. Yang X.D., Korn H., Faber D.S. Long-term potentiation of electrotonic coupling at mixed synapses. Nature 1990, 348:542-545.