Inactivation of Calcium-Binding Protein Genes Induces 160 Hz Oscillations in the Cerebellar Cortex of Alert Mice

Journal of Neuroscience

Volumn 24, Issue 2, 2004, Pages 434-441

  Cheron, Guy ^a,b   Gall, David ^b   Servais, Laurent ^a,b   Dan, Bernard ^a,b   Maex, Reinoud ^c   Schiffmann, Serge N ^b  

^a UNIVERSITY OF MONS   (Belgium)

^b UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

^c UNIVERSITY OF ANTWERP   (Belgium)

Author keywords

Calbindin; Calcium binding proteins; Calretinin; Cerebellum; Fast oscillations; Purkinje cells; Targeted gene inactivation

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR; CALBINDIN; CALCIUM BINDING PROTEIN; CALRETININ; N METHYL DEXTRO ASPARTIC ACID RECEPTOR;

ALERTNESS; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN DEVELOPMENT; CALCIUM TRANSPORT; CELL POPULATION; CELL SYNCHRONIZATION; CEREBELLUM CORTEX; CONTROLLED STUDY; GENE INACTIVATION; GENE INDUCTION; GENE MUTATION; GENE TARGETING; GRANULE CELL; HIGH FREQUENCY OSCILLATION; MOUSE; NERVE CELL; NERVE EXCITABILITY; NONHUMAN; OSCILLATION; PRIORITY JOURNAL; PURKINJE CELL; REINFORCEMENT;

ACTION POTENTIALS; ANIMALS; ATTENTION; CALCIUM-BINDING PROTEIN, VITAMIN D-DEPENDENT; CELL MEMBRANE; CEREBELLAR CORTEX; ELECTRIC CONDUCTIVITY; EVOKED POTENTIALS, MOTOR; FEMALE; MALE; MICE; MICE, KNOCKOUT; NERVE NET; PATCH-CLAMP TECHNIQUES; PERIODICITY; PURKINJE CELLS;

EID: 1642580557     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3197-03.2004     Document Type: Article

References (65)

1. Adrian ED (1935) Discharge frequencies in the central and cerebellar cortex. J Physiol (Lond) 83:33P.
2. Airaksinen MS, Eilers J, Garaschuk O, Thoenen H, Konnerth A, Meyer M (1997) Ataxia and altered dendritic calcium signaling in mice carrying a targeted null mutation of the calbindin D28k gene. Proc Natl Acad Sci USA 94:1488-1493.
3. Baker SN, Kilner JM, Pinches EM, Lemon RN (1999) The role of synchrony and oscillations in the motor output. Exp Brain Res 128:109-117.
4. Barski JJ, Hartmann J, Rose CR, Hoebeek F, Morl K, Noll-Hussong M, De Zeeuw CI, Konnerth A, Meyer M (2003) Calbindin in cerebellar Purkinje cells is a critical determinant of the precision of motor coordination. J Neurosci 23:3469-3477.
5. Bartos M, Vida I, Frotscher M, Meyer A, Monyer H, Geiger JR, Jonas P (2002) Fast synaptic inhibition promotes synchronized gamma oscillations in hippocampal interneuron networks. Proc Natl Acad Sci USA 99:13222-13227.
6. Bower JM, Woolston DC (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.
7. Buzsáki G, Horváth Z, Urioste R, Hetke J, Wise K (1992) High-frequency network oscillation in the hippocampus. Science 256:1025-1027.
8. Carter AG, Regehr WG (2002) Quantal events shape cerebellar interneuron firing. Nat Neurosci 5:1309-1318.
9. Chavas J, Marty A (2003) Coexistence of excitatory and inhibitory GABA synapses in the cerebellar interneuron network. J Neurosci 23:2019-2031.
10. Chrobak JJ, Lorincz A, Buzsaki G (2000) Physiological patterns in the hippocampo-entorhinal cortex system. Hippocampus 10:457-465.
11. D'Angelo E, De Filippi G, Rossi P, Taglietti V (1995) Synaptic excitation of individual rat cerebellar granule cells in situ: evidence for the role of NMDA receptors. J Physiol (Lond) 484:397-413.
12. Dieudonné S, Dumoulin A (2000) Serotin-driven long-range inhibitory connections in the cerebellar cortex. J Neurosci 20:1837-1848.
13. Donoghue JP, Sanes JN, Hatsopoulos NG, Gaal G (1998) Neural discharge and local field potential oscillations in primate motor cortex during voluntary movements. J Neurophysiol 79:159-173.
14. Draguhn A, Traub RD, Schmitz D, Jefferys JGR (1998) Electrical coupling underlies high-frequency oscillations in the hippocampus in vitro. Nature 394:189-192.
15. Ebner TJ, Bloedel JR (1981) Temporal patterning in simple spike discharge of Purkinje cells and its relationship to climbing fiber activity. J Neurophysiol 45:933-947.
16. Eckhorn R, Thomas U (1993) A new method for the insertion of multiple microprobes into neural and muscular tissue, including fibre electrodes, fine wires, needles and microsensors. J Neurosci Methods 49:175-179.
17. Edmonds B, Reyes R, Schwaller B, Roberts WM (2000) Calretinin modifies presynaptic calcium signaling in frog saccular hair cells. Nat Neurosci 3:786-790.
18. Fetz EE, Chen D, Murthy VN, Matsumura M (2000) Synaptic interactions mediating synchrony and oscillations in primate sensorimotor cortex. J Physiol (Paris) 94:323-331.
19. Gall D, Roussel C, Susa I, D'Angelo E, Rossi P, Bearzatto B, Galas MC, Blum D, Schurmans S, Schiffmann SN (2003) Altered neuronal excitability in cerebellar granule cells of mice lacking calretinin. J Neurosci 23:9320-9327.
20. Goossens J, Daniel H, Rancillac A, van der Steen J, Oberdick J, Crepel F, De Zeeuw CI, Frens MA (2001) Expression of protein kinase C inhibitor blocks cerebellar long-term depression without affecting Purkinje cell excitability in alert mice. J Neurosci 21:5813-5823.
21. Gray CM, Koenig P, Engel AK, Singer W (1989) Stimulus-specific neuronal oscillations in cat visual cortex exhibit inter-columnar synchronization which reflects global stimulus properties. Nature 338:334-337.
22. Gruart A, Blazquez P, Delgado-Garcia JM (1995) Kinematics of spontaneous, reflex, and conditioned eyelid movements in the alert cat. J Neurophysiol 74:226-248.
23. Hartmann MJ, Bower JM (1998) Oscillatory activity in the cerebellar hemispheres of unrestrained rats. J Neurophysiol 80:1598-1604.
24. Horn R, Marty A (1988) Muscarinic activation of ionic currents measured by a new whole-cell recording method. J Gen Physiol 92:145-159.
25. Isope P, Dieudonné S, Barbour B (2002) Temporal organization of activity in the cerebellar cortex: a manifesto for synchrony. Ann NY Acad Sci 978:164-174.
26. Katz LC, Shatz CJ (1996) Synaptic activity and the construction of cortical circuits. Science 274:1133-1138.
27. Kondo S, Marty A (1998) Synaptic currents at individual connections among stellate cells in rat cerebellar slices. J Physiol (Lond) 509:221-232.
28. Lang EJ, Sugihara I, Llinas R (1996) GABAergic modulation of complex spike activity by the cerebellar nucleoolivary pathway in rat. J Neurophysiol 76:255-275.
29. Llano I, DiPolo R, Marty A (1994) Calcium-induced calcium release in cerebellar Purkinje cells. Neuron 12:663-673.
30. Llinás RR (1988) The intrinsic electrophysiological properties of mammalian neurons: insights into central nervous system function. Science 242:1654-1664.
31. Llinás RR, Sugimori M (1980) Electrophysiological properties of in vitro Purkinje cell somata in mammalian cerebellar slices. J Physiol (Lond) 305:171-195.
32. Maex R, De Schutter E (1998) Synchronization of Golgi and granule cell firing in a detailed network model of the cerebellar granule cell layer. J Neurophysiol 80:2521-2537.
33. Maex R, Vos B, De Schutter E (2000) Weak common parallel fibre synapses explain the loose synchrony observed between rat cerebellar Golgi cells. J Physiol (Lond) 523 1:175-192.
34. Mann-Metzer P, Yarom Y (1999) Electronic coupling interacts with intrinsic properties to generate synchronized activity in cerebellar networks of inhibitory interneurons. J Neurosci 19:3298-3306.
35. Mauk MD, Medina JF, Nores WL, Ohyama T (2000) Cerebellar function: coordination, learning or timing? Curr Biol 10:522-525.
36. McCormick DA (1999) Spontaneous activity: signal or noise? Science 23:541-543.
37. Medina JF, Garcia KS, Nores WL, Taylor NM, Mauk MD (2000) Timing mechanisms in the cerebellum: testing predictions of a large-scale computer simulation. J Neurosci 20:5516-5525.
38. Meier C, Petrasch-Parwez E, Habbes HW, Teubner B, Guldenagel M, Degen J, Sohl G, Willecke K, Dermietzel R (2002) Immunohistochemical detection of the neuronal connexin36 in the mouse central nervous system in comparison to connexin36-deficient tissues. Histochem Cell Biol 117:461-471.
39. Moortgat KT, Bullock TH, Sejnowski TJ (2000) Gap junction effects on precision and frequency of a model pacemaker network. J Neurophysiol 83:984-997.
40. Murthy VN, Fetz EE (1996) Oscillatory activity in sensorimotor cortex of awake monkeys: synchronization of local field potentials and relation to behavior. J Neurophysiol 76:3949-3967.
41. Odermatt B, Wellershaus K, Wallraff A, Seifert G, Degen J, Euwens C, Fuss B, Bussow H, Schilling K, Steinhauser C, Willecke K (2003) Connexin 47 (Cx47)-deficient mice with enhanced green fluorescent protein reporter gene reveal predominant oligodendrocytic expression of Cx47 and display vacuolized myelin in the CNS. J Neurosci 23:4549-4559.
42. Ohara S, Ikeda A, Kunieda T, Yazawa S, Baba K, Nagamine T, Taki W, Hashimoto N, Mihara T, Shibasaki H (2000) Movement-related change of electrocorticographic activity in human supplementary motor area proper. Brain 123:1203-1215.
43. Pellerin JP, Lamarre Y (1997) Local field potential oscillations in primate cerebellar cortex during voluntary movement. J Neurophysiol 78:3502-3507.
44. Pfurtscheller G, Graimann B, Huggins JE, Levine SP, Schuh LA (2003) Spatiotemporal patterns of beta desynchronization and gamma synchronization in corticographic data during self-paced movement. Clin Neurophysiol 114:1226-1236.
45. Puia G, Costa E, Vicini S (1994) Functional diversity of GABA-activated Cl-currents in Purkinje versus granule neurons in rat cerebellar slices. Neuron 12:117-126.
46. Résibois A, Rogers JH (1992) Calretinin in rat brain: an immunohistochemical study. Neuroscience 46:101-134.
47. Schiffmann SN, Cheron G, Lohof A, d'Alcantara P, Meyer M, Parmentier M, Schurmans S (1999) Impaired motor coordination and Purkinje cell excitability in mice lacking calretinin. Proc Natl Acad Sci USA 96:5257-5262.
48. 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.
49. Schwarz C, Welsh JP (2001) Dynamic modulation of mossy fiber system throughput by inferior olive synchrony: a multielectrode study of cerebellar cortex activated by motor cortex. J Neurophysiol 86:2489-2504.
50. Simburger E, Stang A, Kremer M, Dermietzel R (1997) Expression of connexin43 mRNA in adult rodent brain. Histochem Cell Biol 107:127-137.
51. Singer W (1993) Synchronization of cortical activity and its putative role in information processing and learning. Annu Rev Physiol 55:349-374.
52. Singer W (1999) Neuronal synchrony: a versatile code for the definition of relations. Neuron 24:31-65.
53. Sotelo C, Llinas R (1972) Specialized membrane junctions between neurons in the vertebrate cerebellar cortex. J Cell Biol 53:271-289.
54. Steriade M, Amzica F, Neckelmann D, Timofeev I (1998) Spike-wave complexes and fast components of cortically generated seizures. II. Extra- and intracellular patterns. J Neurophysiol 80:1456-1479.
55. Sugihara I, Lang EJ, Llinas R (1995) Serotonin modulation of inferior olivary oscillations and synchronicity: a multiple-electrode study in the rat cerebellum. Eur J Neurosci 7:521-534.
56. 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.
57. Teubner B, Odermatt B, Guldenagel M, Sohl G, Degen J, Bukauskas F, Kronengold J, Verselis VK, Jung YT, Kozak CA, Schilling K, Willecke K (2001) Functional expression of the new gap junction gene connexin47 transcribed in mouse brain and spinal cord neurons. J Neurosci 21:1117-1126.
58. Timofeev I, Steriade M (1997) Fast (mainly 30-100 Hz) oscillations in the cat cerebellothalamic pathway and their synchronization with cortical potentials. J Physiol (Lond) 504:153-168.
59. Traub RD, Bibbig A (2000) A model of high-frequency ripples in the hippocampus based on synaptic coupling plus axon-axon gap junctions between pyramidal neurons. J Neurosci 20:2086-2093.
60. Traub RD, Schmitz D, Jefferys JG, Draguhn A (1999) High-frequency population oscillations are predicted to occur in hippocampal pyramidal neuronal networks interconnected by axoaxonal gap junctions. Neuroscience 92:407-426.
61. Traub RD, Draguhn A, Whittington MA, Baldeweg T, Bibbig A, Bumhl EH, Schmitz D (2002) Axonal gap junctions between principal neurons: a novel source of network oscillations, and perhaps epileptogenesis. Rev Neurosci 13:1-30.
62. Vecellio M, Schwaller B, Meyer M, Hunziker W, Celio MR (2000) Alterations in Purkinje cell spines of calbindin D-28 k and parvalbumin knockout mice. Eur J Neurosci 12:945-954.
63. Vos BP, Volny-Luraghi A, De Schutter E (1999) Cerebellar Golgi cells in the rat: receptive fields and timing of responses to facial stimulation. Eur J Neurosci 11:2621-2634.
64. Welsh JP, Lang EJ, Suglhara I, Llinás RR (1995) Dynamic organization of motor control within the olivocerebellar system. Nature 374:453-457.
65. Ylinen A, Bragin A, Nadasdy Z, Jando G, Szabo I, Sik A, Buzsaki G (1995) Sharp wave-associated high-frequency oscillation (200 Hz) in the intact hippocampus: network and intracellular mechanisms. J Neurosci 15:30-46.