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

Journal of Neuroscience

Volumn 23, Issue 11, 2003, Pages 4700-4711

  De Zeeuw, Chris I ^a   Chorev, Edilzh ^b   Devor, Anna ^b   Manor, Yait ^c   Van Der Giessen, Ruben S ^a   De Jeu, Marcel T ^a   Hoogenraad, Casper C ^a   Bijman, Jan ^a   Ruigrok, Tom J H ^a   French, Pim ^a   Jaarsma, Dick ^a   Kistler, Werner M ^a   Meier, Carola ^d   Petrasch Parwez, Elisabeth ^d   Dermietzel, Rolf ^d   Sohl, Goran ^e   Gueldenagel, Martin ^d   Willecke, Klaus ^e   Yarom, Yosi ^b  

^a ERASMUS MEDICAL CENTER   (Netherlands)

^b HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^c BEN GURION UNIVERSITY OF THE NEGEV   (Israel)

^d RUHR UNIVERSITY BOCHUM   (Germany)

^e UNIVERSITY OF BONN   (Germany)

Author keywords

Cerebellum; Connexins; Dynamic clamp; Electrotonic coupling; Gap junction; Inferior olive; Motor coordination; Ultrastructure

Indexed keywords

CONNEXIN 36; MESSENGER RNA;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN ELECTROPHYSIOLOGY; CALCIUM CONDUCTANCE; CELL ULTRASTRUCTURE; CEREBELLUM; CONTROLLED STUDY; CYTOARCHITECTURE; DENDRITE; ELECTRON MICROSCOPY; GAP JUNCTION; GOLGI COMPLEX; IMMUNOCYTOCHEMISTRY; IN SITU HYBRIDIZATION; INFERIOR OLIVE; MOTOR COORDINATION; MOUSE; NERVE CELL NETWORK; NONHUMAN; OSCILLATION; PATCH CLAMP; PRIORITY JOURNAL;

EID: 0037779295     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.23-11-04700.2003     Document Type: Article

References (54)

1. Bacskai T, Matesz C (2002) Primary afferent fibers establish dye-coupled connections in the frog central nervous system. Brain Res Bull 57:317-319.
2. Bal T, McCormick DA (1997) Synchronized oscillations in the inferior olive are controlled by the hyperpolarization-activated cation current I(h). J Neurophysiol 77:3145-3156.
3. Belluardo N, Mud G, Trovato-Salinaro A, Le Gurun S, Charollais A, Serre-Beinier V, Amato G, Haefliger JA, Meda P, Condorelli DF (2000) Expression of connexin36 in the adult and developing rat brain. Brain Res 865:121-138.
4. Bennett MV (2002) Neoreticularism and neuronal polarization. Prog Brain Res 136:189-201.
5. Condorelli DF, Parenti R, Spinella F, Trovato Salinaro A, Belluardo N, Cardile V, Cicirata F (1998) Cloning of a new gap junction gene (Cx36) highly expressed in mammalian brain neurons. Eur J Neurosci 10:1202-1208.
6. Deans MR, Gibson JR, Sellitto C, Connors BW, Paul DL (2001) Synchronous activity of inhibitory networks in neocortex requires electrical synapses containing connexin 36. Neuron 31:477-485.
7. Devor A, Yarom Y (2000) GABAergic modulation of olivary oscillations. Prog Brain Res 124:213-220.
8. Devor A, Yarom Y (2002a) Electrotonic coupling in the inferior olivary nucleus revealed by simultaneous double patch recordings. J Neurophysiol 87:3048-3058.
9. Devor A, Yarom Y (2002b) Generation and propagation of subthreshold waves in a network of inferior olivary neurons. J Neurophysiol 87:3059-3069.
10. De Zeeuw CI, Holstege JC, Ruigrok TJ, Voogd J (1989) Ultrastructural study of the GABAergic, cerebellar, and mesodiencephalic innervation of the cat medial accessory olive: anterograde tracing combined with immunocytochemistry. J Comp Neurol 284:12-35.
11. De Zeeuw CI, Wylie DR, DiGiorgi PL, Simpson JI (1994) Projections of individual Purkinje cells of identified zones in the flocculus to the vestibular and cerebellar nuclei in the rabbit. J Comp Neurol 349:428-447.
12. De Zeeuw CI, Hertzberg EL, Mugnaini E (1995) The dendritic lamellar body: a new neuronal organelle putatively associated with dendrodendritic gap junctions. J Neurosci 15:1587-1604.
13. De Zeeuw CI, Hoogenraad CC, Goedknegt E, Hertzberg E, Neubauer A, Grosveld F, Galjart N (1997) CLIP-115, a novel brain specific cytoplasmic linker protein, mediates the localisation of dendritic lamellar bodies. Neuron 19:1187-1199.
14. De Zeeuw CI, Simpson JI, Hoogenraad CC, Galjart N, Koekkoek SKE, Ruigrok TJH (1998) Microcircuitry and function of the inferior olive. Trends Neurosci 21:391-400.
15. Gueldenagel M, Ammermuller J, Feigenspan A, Teubner B, Degen J, Sohl G, Willecke K, Weiler R (2001) Visual transmission deficits in mice with targeted disruption of the gap junction gene connexin 36. J Neurosci 21:6036-6044.
16. Hinrichsen CF, Larramendi LM (1968) Synapses and cluster formation of the mouse mesencephalic fifth nucleus. Brain Res 7:296-299.
17. Hormuzdi SG, Pais I, LeBeau FE, Towers SK, Rozov A, Buhl EH, Whittington MA., Monyer H (2001) Impaired electrical signaling disrupts gamma frequency oscillations in connexin 36 deficient mice. Neuron 31:487-495.
18. Ivry RB (1996) The representation of temporal information in perception and motor control. Curr Opin Neurobiol 6:851-857.
19. King JS (1980) The synaptic organization of the inferior olivary nucleus. In: The inferior olivary nucleus (Courville J, De Montigny C, Lammare Y, eds), pp 1-35. New York: Raven.
20. Kistler WM, van Hemmen JL, De Zeeuw CI (2000) Time window control: a model for cerebellar function based on synchronization, reverberation, and time slicing. In: Cerebellar modules: molecules, morphology, and function (De Zeeuw CI, Ruigrok TJH, Gerrits NGM, eds), pp 275-299. Amsterdam: Elsevier.
21. Kistler WM, De Jeu MTG, Elgersma Y, van der Giessen RS, Hensbroek R, Luo C, Koekkoek SKE, Hoogenraad CC, Hamers FPT, Gueldenagel M, Sohl G, Willecke K, De Zeeuw CI (2002) Analysis of Cx36 knock out does not support tenet that olivary gap junctions are required for complex spike synchronization and normal motor performance. Ann NY Acad Sci 978:391-405.
22. Koponen JK, Turunen AM, Yla-Herttuala S (2002) Escherichia coli DNA contamination in AmpliTaq gold polymerase interferes with TaqMan analysis of lacZ. Mol Ther 5:220-222.
23. Lampl I, Yarom Y (1993) Sub-threshold oscillations of the membrane potential: a functional synchronizing and timing device. J Neurophysiol 70:2181-2186.
24. Lampl I, Yarom Y (1997) Sub-threshold oscillations and resonant behavior: two manifestations of the same mechanism. Neuroscience 78:325-341.
25. Landis DMD, Reese TS, Raviola E (1974) Differences in membrane structure between excitatory and inhibitory components of the reciprocal synapse in the olfactory bulb. J Comp Neurol 155:67-92.
26. Lang EJ (2001) Organization of olivocerebellar activity in the absence of excitatory glutamatergic input. J Neurosci 21:1663-1675.
27. Llinás R, Yarom Y (1981a) Electrophysiology of mammalian inferior olivary neurones in vitro. Different types of voltage-dependent ionic conductances. J Physiol (Lond) 315:549-567.
28. Llinás R, Yarom Y (1981b) Properties and distribution of ionic conductances generating electro-responsiveness of mammalian inferior olivary neurons in vitro. J Physiol (Lond) 315:569-584.
29. Llinás R, Yarom Y (1986) Oscillatory properties of guinea-pig inferior olivary neurones and their pharmacological modulation: an in vitro study. J Physiol (Lond) 376:163-182.
30. Llinás R, Yarom Y (1987) Long-term modifiability of anomalous and delayed rectification in guinea pig inferior olivary neurons. J Neurosci 7:1166-1177.
31. Loewenstein Y, Yarom Y, Sompolinsky H (2001) The generation of oscillations in networks of electrically coupled cells. Proc Natl Acad Sci USA 98:8095-8100.
32. Long MA, Deans MR, Paul DL, Connors BW (2002) Rhythmicity without synchrony in the electrically uncoupled inferior olive. J Neurosci 22:10898-10905.
33. MacLean JN, Zhang Y, Johnson BR, Harris-Warrick RM (2003) Activity-independent homeostasis in rhythmically active neurons. Neuron 37:109-120.
34. MacVicar BA, Dudek FE (1981) Electrotonic coupling between pyramidal cells: a direct demonstration in rat hippocampal slices. Science 213:782-785.
35. Maier N, Guldenagel M, Sohl G, Siegmund H, Willecke K, Draguhn A (2002) Reduction of high-frequency network oscillations (ripples) and pathological network discharges in hippocampal slices from connexin 36-deficient mice. J Physiol (Lond) 541:521-528.
36. Manor Y, Rinzel J, Segev I, Yarom Y (1997) Low-amplitude oscillations in the inferior olive: a model based on electrical coupling of neurons with heterogeneous channel densities. J Neurophysiol 77:2736-2752.
37. Manor Y, Yarom Y, Chorev E, Devor A (2000) To beat or not to beat: a decision taken at the network level. J Physiol (Lond) 94:375-390.
38. Matsumoto A, Arnold AP, Zampighi GA, Micevych PE (1988) Androgenic regulation of gap junctions between motoneurons in rat spinal cord. J Neurosci 8:4177-4183.
39. Peters A (1980) Morphological correlates of epilepsy: cells in the cerebral cortex. Adv Neurol 27:21-48.
40. Rash JE, Staines WA, Yasumura T, Patel D, Furman CS, Stelmack GL, Nagy JI (2000) Immunogold evidence that neuronal gap junctions in adult rat brain and spinal cord contain connexin-36 but not connexin-32 or connexin-43. Proc Natl Acad Sci USA 97:7573-7578.
41. Raviola E, Gilula NB (1975) Intramembrane organization of specialized contacts in the outer plexiform layer of the retina. A freeze-fracture study in monkeys and rabbits. J Cell Biol 65:192-222.
42. Rutherford JG, Gwyn DG (1977) Gap junctions in the inferior olivary nucleus of the squirrel monkey, Saimiri sciureus. Brain Res 128:374-378.
43. Schmitz D, Schuchmann S, Fisahn A, Draguhn A, Buhl EH, Petrasch-Parwez E, Dermietzel R, Heinemann U, Traub RD (2001) Axo-axonal coupling: a novel mechanism for ultrafast neuronal communication. Neuron 31:831-840.
44. Sharp AA, O'Neil MB, Abbott LF, Marder E (1993) Dynamic clamp: computer-generated conductances in real neurons. J Neurophysiol 69:992-995.
45. Sotelo C, Llinás RR (1972) Specialized membrane junctions between neurons in the vertebrate cerebellar cortex. J Cell Biol 53:271-289.
46. Sotelo C, Llinás R, Baker R (1974) Structural study of inferior olivary nucleus of the cat: morphological correlates of electrotonic coupling. J Neurophysiol 37:541-559.
47. Sotelo C, Gotow T, Wassef M (1986) Localization of glutamic-acid-decarboxylase-immunoreactive axon terminals in the inferior olive of the rat, with special emphasis on anatomical relations between GABAergic synapses and dendrodendritic gap junctions. J Comp Neurol 252:32-50.
48. Spruston N (2001) Axonal gap junctions send ripples through the hippocampus. Neuron 31:669-671.
49. Teubner B, Degen J, Sohl G, Guldenagel M, Bukauskas FF, Trexler EB, Verselis VK, De Zeeuw CI, Lee CG, Kozak CA, Petrasch-Parwez E, Dermietzel R, Willecke K (2000) Functional expression of the murine connexin 36 gene coding for a neuron-specific gap junctional protein. J Membr Biol 176:249-262.
50. Van Pelt J, Uylings HB, Verwer RW, Pentney RJ, Woldenberg MJ (1992) Tree asymmetry-a sensitive and practical measure for binary topological trees. Bull Math Biol 54:759-784.
51. Voogd J, Bigaré F (1980) Topographical distribution of olivary and corticonuclear fibers in the cerebellum. A review. In: The inferior olivary nucleus (Courville J, De Montigny C, Lamarre Y, eds), pp 207-235. New York: Raven.
52. Welsh JP, Lang EJ, Sugihara I, Llinás R (1995) Dynamic organization of motor control within the olivocerebellar system. Nature 374:453-457.
53. Yarom Y (1991) Rhythmogenesis in a hybrid system - interconnecting an olivary neuron to an analog network of coupled oscillators. Neuroscience 44:263-275.
54. Yarom Y, Cohen D (2002) The olivocerebellar system as a generator of temporal patterns. Ann NY Acad Sci 978:122-134.