Enhanced cortical and hippocampal neuronal excitability in mice deficient in the extracellular matrix glycoprotein tenascin-R

Molecular and Cellular Neuroscience

Volumn 25, Issue 3, 2004, Pages 515-523

  Gurevicius, K ^a   Gureviciene, I ^a   Valjakka, A ^a   Schachner, M ^b   Tanila, H ^a,c  

^a UNIVERSITY OF EASTERN FINLAND   (Finland)

^b UNIVERSITY OF HAMBURG   (Germany)

^c KUOPIO UNIVERSITY HOSPITAL   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOPROTEIN; TENASCIN R; UNCLASSIFIED DRUG;

AMPLITUDE MODULATION; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AUDITORY STIMULATION; AUDITORY THRESHOLD; BRAIN CORTEX; CONTROLLED STUDY; ELECTROENCEPHALOGRAM; EVOKED AUDITORY RESPONSE; FREQUENCY MODULATION; HIPPOCAMPUS; MALE; MOUSE; NERVE CELL EXCITABILITY; NONHUMAN; OSCILLATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; THETA RHYTHM; WILD TYPE;

ACOUSTIC STIMULATION; ANIMALS; CEREBRAL CORTEX; ELECTROENCEPHALOGRAPHY; EVOKED POTENTIALS, AUDITORY; HIPPOCAMPUS; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NEURONS; TENASCIN;

EID: 1642346263     PISSN: 10447431     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mcn.2003.12.001     Document Type: Article

References (38)

1. Andersen P., Eccles J., Loyning T. Pathway of post-synaptic inhibition in the hippocampus. J. Neurophysiol. 27:1964;608-619.
2. Bartsch U. The extracellular matrix molecule tenascin-C: expression in vivo and functional characterization in vitro. Prog. Neurobiol. 49:1996;145-168.
3. Bartsch U., Pesheva P., Raff M., Schachner M. Expression of janusin (J1-160/180) in the retina and optic nerve of the developing and adult mouse. Glia. 9:1993;57-69.
4. Bickford-Wimer P.C., Nagamoto H., Johnson R., Adler L.E., Egan M., Rose G.M., Freedman R. Auditory sensory gating in hippocampal neurons: a model system in the rat. Biol. Psychiatry. 27:1990;183-192.
5. Bragin A., Jando G., Nadasdy Z., Hetke J., Wise K., Buzsaki G. Gamma (40-100 Hz) oscillation in the hippocampus of the behaving rat. J. Neurosci. 15:1995;47-60.
6. Brenneke F., Bukalo O., Schmidt S., Schachner M., Lie A.A., Dityatev A. Mice deficient for the extracellular matrix glycoprotein tenascin-R show increased polyspiking and seizure-associated structural alternations. Neuroscience. 2004;. (in press).
7. Brückner G., Grosche J., Schmidt S., Hartig W., Margolis R.U., Delpech B., Seidenbecher C.I., Czaniera R., Schachner M. Postnatal development of perineuronal nets in wild-type mice and in a mutant deficient in tenascin-R. J. Comp. Neurol. 428:2000;616-629.
8. Buhl D.L., Harris K.D., Hormuzdi S.G., Monyer H., Buzsaki G. Selective impairment of hippocampal gamma oscillations in connexin-36 knock-out mouse in vivo. J. Neurosci. 23:2003;1013-1018.
9. Buzsaki G. Hippocampal sharp waves: their origin and significance. Brain Res. 398:1986;242-252.
10. Buzsaki G. Theta oscillations in the hippocampus. Neuron. 33:2002;325-340.
11. Buzsaki G., Horvath Z., Urioste R., Hetke J., Wise K. High-frequency network oscillation in the hippocampus. Science. 256:1992;1025-1027.
12. Buzsaki G., Buhl D.L., Harris K.D., Csicsvari J., Czh B., Morozov A. Hippocampal network patterns of activity in the mouse. Neuroscience. 116:2003;201-211.
13. Draguhn A., Traub R.D., Schmitz D., Jefferys J.G. Electrical coupling underlies high-frequency oscillations in the hippocampus in vitro. Nature. 394:1998;189-192.
14. Faissner A. The tenascin gene family in axon growth and guidance. Cell Tissue Res. 290:1997;331-341.
15. Freitag S., Schachner M., Morellini F. Behavioral alterations in mice deficient for the extracellular matrix glycoprotein tenascin-R. Behav. Brain Res. 145:2003;189-207.
16. Fukuda T., Kosaka T. Gap junctions linking the dendritic network of GABAergic interneurons in the hippocampus. J. Neurosci. 20:2000;1519-1528.
17. Hershman K.M., Freedman R., Bickford P.C. GABAB antagonists diminish the inhibitory gating of auditory response in the rat hippocampus. Neurosci. Lett. 190:1995;133-136.
18. Kramis R., Vanderwolf C.H., Bland B.H. Two types of hippocampal rhythmical slow activity in both the rabbit and the rat: relations to behavior and effects of atropine, diethyl ether, urethane, and pentobarbital. Exp. Neurol. 49:1975;58-85.
19. LeBeau F.E., Towers S.K., Traub R.D., Whittington M.A., Buhl E.H. Fast network oscillations induced by potassium transients in the rat hippocampus in vitro. J. Physiol. 542:2002;167-179.
20. Lee M.G., Chrobak J.J., Sik A., Wiley R.G., Buzsaki G. Hippocampal theta activity following selective lesion of the septal cholinergic system. Neuroscience. 62:1994;1033-1047.
21. Leranth C., Carpi D., Buzsaki G., Kiss J. The entorhino-septo- supramammillary nucleus connection in the rat: morphological basis of a feedback mechanism regulating hippocampal theta rhythm. Neuroscience. 88:1999;701-718.
22. McNaughton N., Logan B., Panickar K.S., Kirk I.J., Pan W.X., Brown N.T., Heenan A. Contribution of synapses in the medial supramammillary nucleus to the frequency of hippocampal theta rhythm in freely moving rats. Hippocampus. 5:1995;534-545.
23. Nikonenko A., Schmidt S., Skibo G., Bruckner G., Schachner M. Tenascin-R-deficient mice show structural alterations of symmetric perisomatic synapses in the CA1 region of the hippocampus. J. Comp. Neurol. 456:2003;338-349.
24. Penttonen M., Kamondi A., Acsady L., Buzsaki G. Gamma frequency oscillation in the hippocampus of the rat: intracellular analysis in vivo. Eur. J. Neurosci. 10:1998;718-728.
25. Saghatelyan A.K., Gorissen S., Albert M., Hertlein B., Schachner M., Dityatev A. The extracellular matrix molecule tenascin-R and its HNK-1 carbohydrate modulate perisomatic inhibition and long-term potentiation in the CA1 region of the hippocampus. Eur. J. Neurosci. 12:2000;3331-3342.
26. Saghatelyan A.K., Dityatev A., Schmidt S., Schuster T., Bartsch U., Schachner M. Reduced perisomatic inhibition, increased excitatory transmission, and impaired long-term potentiation in mice deficient for the extracellular matrix glycoprotein tenascin-R. Mol. Cell. Neurosci. 17:2001;226-240.
27. Saghatelyan A.K., Snapyan M., Gorissen S., Meigel I., Mosbacher J., Kaupmann K., Bettler B., Kornilov A.V., Nifantiev N.E., Sakanyan V., Schachner M., Dityatev A. Recognition molecule associated carbohydrate inhibits postsynaptic GABA(B) receptors: a mechanism for homeostatic regulation of GABA release in perisomatic synapses. Mol. Cell. Neurosci. 24:2003;271-282.
28. Schachner M., Taylor J., Bartsch U., Pesheva P. The perplexing multifunctionality of janusin, a tenascin-related molecule. Perspect. Dev. Neurobiol. 2:1994;33-41.
29. Srinivasan J., Schachner M., Catterall W.A. Interaction of voltage-gated sodium channels with the extracellular matrix molecules tenascin-C and tenascin-R. Proc. Natl. Acad. Sci. U. S. A. 95:1998;15753-15757.
30. Traub R.D., Whittington M.A., Colling S.B., Buzsaki G., Jefferys J.G. Analysis of gamma rhythms in the rat hippocampus in vitro and in vivo. J. Physiol. 493(Pt 2):1996;471-484.
31. Wang X.J., Buzsaki G. Gamma oscillation by synaptic inhibition in a hippocampal interneuronal network model. J. Neurosci. 16:1996;6402-6413.
32. Weber P., Bartsch U., Rasband M.N., Czaniera R., Lang Y., Bluethmann H., Margolis R.U., Levinson S.R., Shrager P., Montag D., Schachner M. Mice deficient for tenascin-R display alterations of the extracellular matrix and decreased axonal conduction velocities in the CNS. J. Neurosci. 19:1999;4245-4262.
33. Wintergerst E.S., Fuss B., Bartsch U. Localization of janusin mRNA in the central nervous system of the developing and adult mouse. Eur. J. Neurosci. 5:1993;299-310.
34. Wintergerst E.S., Rathjen F.G., Schwaller B., Eggli P., Celio M.R. Tenascin-R associates extracellularly with parvalbumin immunoreactive neurones but is synthesised by another neuronal population in the adult rat cerebral cortex. J. Neurocytol. 30:2001;293-301.
35. Vreugdenhil M., Jefferys J.G., Celio M.R., Schwaller B. Parvalbumin-deficiency facilitates repetitive IPSCs and gamma oscillations in the hippocampus. J. Neurophysiol. 89:2003;1414-1422.
36. Xiao Z.C., Ragsdale D.S., Malhotra J.D., Mattei L.N., Braun P.E., Schachner M., Isom L.L. Tenascin-R is a functional modulator of sodium channel beta subunits. J. Biol. Chem. 274:1999;26511-26517.
37. Ylinen A., Bragin A., Nadasdy Z., Jando G., Szabo I., Sik A., Buzsaki G. Sharp wave-associated high-frequency oscillation (200 Hz) in the intact hippocampus: network and intracellular mechanisms. J. Neurosci. 15:1995;30-46.
38. Zarrindast M., Rostami P., Sadeghi-Hariri M. GABA(A) but not GABA(B) receptor stimulation induces antianxiety profile in rats. Pharmacol. Biochem. Behav. 69:2001;9-15.