Increased excitability and altered action potential waveform in cerebellar granule neurons of the Ts65Dn mouse model of Down syndrome

Brain Research

Volumn 1465, Issue , 2012, Pages 10-17

  Usowicz, Maria M ^a   Garden, Claire L P ^a,b  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

^b EDINBURGH NAPIER UNIVERSITY   (United Kingdom)

Author keywords

Cerebellum; Down syndrome; Granule cell; Hypoplasia

Indexed keywords

ACTION POTENTIAL; AFTERHYPERPOLARIZATION; ANIMAL CELL; ARTICLE; BRAIN DYSFUNCTION; BRAIN SIZE; CELL COUNT; CELL SURVIVAL; CEREBELLUM; CEREBELLUM CORTEX; CONTROLLED STUDY; DOWN SYNDROME; ELECTRIC POTENTIAL; GRANULE CELL; INTELLECTUAL IMPAIRMENT; INTERNEURON; MALE; MEMBRANE POTENTIAL; MOSSY FIBER; MOTOR COORDINATION; MOTOR DYSFUNCTION; MOUSE; NERVE CELL EXCITABILITY; NONHUMAN; PRIORITY JOURNAL; PURKINJE CELL; SENSORIMOTOR FUNCTION; SPEECH DISORDER; WAVEFORM;

ACTION POTENTIALS; ANIMALS; CEREBELLUM; DISEASE MODELS, ANIMAL; DOWN SYNDROME; FEMALE; MALE; MICE; MICE, INBRED C3H; MICE, INBRED C57BL; MICE, NEUROLOGIC MUTANTS; MOTOR SKILLS DISORDERS; NEURONS; ORGAN CULTURE TECHNIQUES; PATCH-CLAMP TECHNIQUES; UP-REGULATION;

EID: 84862878470     PISSN: 00068993     EISSN: 18726240     Source Type: Journal    
DOI: 10.1016/j.brainres.2012.05.027     Document Type: Article

References (51)

1. Ackermann, H., 2008. Cerebellar contributions to speech production and speech perception: psycholinguistic and neurobiological perspectives. Trends Neurosci. 31, 265-272.
2. Arenz, A., Bracey, E.F., Margrie, T.W., 2009. Sensory representations in cerebellar granule cells. Curr. Opin. Neurobiol. 19, 445-451.
3. Ault, B., Caviedes, P., Rapoport, S.I., 1989. Neurophysiological abnormalities in cultured dorsal root ganglion neurons from the trisomy-16 mouse fetus, a model for Down syndrome. Brain Res. 485, 165-170. (Pubitemid 19096293)
4. Aylward, E.H., Habbak, R., Warren, A.C., Pulsifer, M.B., Barta, P.E., Jerram, M., Pearlson, G.D., 1997. Cerebellar volume in adults with Down syndrome. Arch. Neurol. 54, 209-212. (Pubitemid 27078729)
5. Barnes, E.F., Roberts, J., Mirrett, P., Sideris, J., Misenheimer, J., 2006. A comparison of oral structure and oral-motor function in young males with fragile X syndrome and Down syndrome. J. Speech Lang. Hear. Res. 49, 903-917. (Pubitemid 350056563)
6. Baxter, L.L., Moran, T.H., Richtsmeier, J.T., Troncoso, J., Reeves, R.H., 2000. Discovery and genetic localization of Down syndrome cerebellar phenotypes using the Ts65Dn mouse. Hum. Mol. Genet. 9, 195-202. (Pubitemid 30052743)
7. Bean, B.P., 2007. The action potential in mammalian central neurons. Nat. Rev. Neurosci. 8, 451-465. (Pubitemid 46789230)
8. Best, T.K., Cramer, N.P., Chakrabarti, L., Haydar, T.F., Galdzicki, Z., 2011. Dysfunctional hippocampal inhibition in the Ts65Dn mouse model of Down syndrome. Exp. Neurol. 233, 749-757.
9. Brickley, S.G., Revilla, V., Cull-Candy, S.G., Wisden, W., Farrant, M., 2001. Adaptive regulation of neuronal excitability by a voltage-independent potassiumconductance. Nature 409, 88-92. (Pubitemid 32098630)
10. Brickley, S.G., Aller, M.I., Sandu, C., Veale, E.L., Alder, F.G., Sambi, H., Mathie, A., Wisden, W., 2007. TASK-3 two-pore domain potassium channels enable sustained high-frequency firing in cerebellar granule neurons. J. Neurosci. 27, 9329-9340. (Pubitemid 47358198)
11. Cathala, L., Brickley, S., Cull-Candy, S., Farrant, M., 2003. Maturation of EPSCs and intrinsic membrane properties enhances precision at a cerebellar synapse. J. Neurosci. 23, 6074-6085. (Pubitemid 36859445)
12. Caviedes, P., Ault, B., Rapoport, S.I., 1990. The role of altered sodium currents in action potential abnormalities of cultured dorsal root ganglion neurons from trisomy 21 (Down syndrome) human fetuses. Brain Res. 510, 229-236. (Pubitemid 20095497)
13. Caviedes, P., Caviedes, R., Rapoport, S.I., 2006. Altered calcium currents in cultured sensory neurons of normal and trisomy 16 mouse fetuses, an animal model for human trisomy 21 (Down syndrome). Biol. Res. 39, 471-481. (Pubitemid 44768768)
14. Cocchi, G., Gualdi, S., Bower, C., Halliday, J., Jonsson, B., Myrelid, A., Mastroiacovo, P., Amar, E., Bakker, M.K., Correa, A., Doray, B., Melve, K.K., Koshnood, B., Landau, D., Mutchinick, O.M., Pierini, A., Ritvanen, A., Ruddock, V., Scarano, G., Sibbald, B., Sipek, A., Tenconi, R., Tucker, D., Anneren, G., 2010. International trends of Down syndrome 1993-2004: births in relation to maternal age and terminations of pregnancies. Birth Defects Res. A Clin. Mol. Teratol. 88, 474-479.
15. Costa, A.C., Walsh, K., Davisson, M.T., 1999. Motor dysfunction in a mouse model for Down syndrome. Physiol. Behav. 68, 211-220. (Pubitemid 30009803)
16. 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. 484 (Pt 2), 397-413.
17. D'Angelo, E., De, F.G., Rossi, P., Taglietti, V., 1998. Ionic mechanism of electroresponsiveness in cerebellar granule cells implicates the action of a persistent sodium current. J. Neurophysiol. 80, 493-503. (Pubitemid 28387636)
18. Dierssen, M., Herault, Y., Estivill, X., 2009. Aneuploidy: from a physiological mechanism of variance to Down syndrome. Physiol. Rev. 89, 887-920.
19. Escorihuela, R.M., Fernandez-Teruel, A., Vallina, I.F., Baamonde, C., Lumbreras, M.A., Dierssen, M., Tobena, A., Florez, J., 1995. A behavioral assessment of Ts65Dn mice: a putative Down syndrome model*1. Neurosci. Lett. 199, 143-146.
20. Frith, U., Frith, C.D., 1974. Specific motor disabilities in Down's syndrome. J. Child Psychol. Psychiatry 15, 293-301.
21. Gabbiani, F., Midtgaard, J., Knopfel, T., 1994. Synaptic integration in a model of cerebellar granule cells. J. Neurophysiol. 72, 999-1009. (Pubitemid 24273598)
22. Galante, M., Jani, H., Vanes, L., Daniel, H., Fisher, E.M.C., Tybulewicz, V.L.J., Bliss, T.V.P., Morice, E., 2009. Impairments in motor coordination without major changes in cerebellar plasticity in the Tc1 mouse model of Down syndrome. Hum. Mol. Genet. 18, 1449-1463.
23. Galdzicki, Z., Coan, E., Rapoport, S.I., 1993. Cultured hippocampal neurons from trisomy 16 mouse, a model for Down's syndrome, have an abnormal action potential due to a reduced inward sodium current. Brain Res. 604, 69-78. (Pubitemid 23080099)
24. Galdzicki, Z., Coan, E.J., Rapoport, S.I., Stoll, J., 1998. Increased expression of voltage-activated calcium channels in cultured hippocampal neurons from mouse trisomy 16, a model for Down syndrome. Mol. Brain Res. 56, 200-206. (Pubitemid 28271677)
25. Hamann, M., Rossi, D.J., Attwell, D., 2002. Tonic and spillover inhibition of granule cells control information flow through cerebellar cortex. Neuron 33, 625-633. (Pubitemid 34188437)
26. Hanson, J.E., Blank, M., Valenzuela, R.A., Garner, C.C., Madison, D.V., 2007. The functional nature of synaptic circuitry is altered in area CA3 of the hippocampus in a mouse model of Down's syndrome. J. Physiol (Lond.) 579, 53-67.
27. Harashima, C., Jacobowitz, D., Stoffel, M., Chakrabarti, L., Haydar, T., Siarey, R., Galdzicki, Z., 2006. Elevated expression of the G-protein-activated inwardly rectifying potassium channel 2 (GIRK2) in cerebellar unipolar brush cells of a Down syndrome mouse model. Cell. Mol. Neurobiol. 1-16.
28. Haydar, T.F., Reeves, R.H., 2011. Trisomy 21 and early brain development. Trends Neurosci. 35, 81-91.
29. Henderson, S.E., Morris, J., Frith, U., 1981. The motor deficit in Down's syndrome children: a problem of timing? J. Child Psychol. Psychiatry 22, 233-245. (Pubitemid 11127773)
30. Hyde, L.A., Crnic, L.S., Pollock, A., Bickford, P.C., 2001. Motor learning in Ts65Dn mice, a model for Down syndrome. Dev. Psychobiol. 38, 33-45. (Pubitemid 32037354)
31. Jernigan, T.L., Bellugi, U., 1990. Anomalous brain morphology on magnetic resonance images in Williams syndrome and Down syndrome. Arch. Neurol. 47, 529-533. (Pubitemid 20155841)
32. Klein, S.L., Kriegsfeld, L.J., Hairston, J.E., Rau, V., Nelson, R.J., Yarowsky, P.J., 1996. Characterization of sensorimotor performance, reproductive and aggressive behaviors in segmental trisomic 16 (Ts65Dn) mice. Physiol. Behav. 60, 1159-1164. (Pubitemid 26336736)
33. Kleschevnikov, A.M., Belichenko, P.V., Gall, J., George, L., Nosheny, R., Maloney, M.T., Salehi, A., Mobley, W.C., 2012. Increased efficiency of the GABAA and GABAB receptor-mediated neurotransmission in the Ts65Dn mouse model of Down syndrome. Neurobiol. Dis. 45, 683-691.
34. Laffaire, J., Rivals, I., Dauphinot, L., Pasteau, F., Wehrle, R., Larrat, B., Vitalis, T., Moldrich, R.X., Rossier, J., Sinkus, R., Herault, Y., Dusart, I., Potier, M.C., 2009. Gene expression signature of cerebellar hypoplasia in a mouse model of Down syndrome during postnatal development. BMC Genomics 10, 138.
35. Lana-Elola, E., Watson-Scales, S.D., Fisher, E.M., Tybulewicz, V.L., 2011. Down syndrome: searching for the genetic culprits. Dis. Model. Mech. 4, 586-595.
36. Liu, D.P., Schmidt, C., Billings, T., Davisson, M.T., 2003. Quantitative PCR genotyping assay for the Ts65Dn mouse model of Down syndrome. Biotechniques 35, 1170-1174 1176, 1178.
37. Mitra, A., Blank, M., Madison, D.V., 2012. Developmentally altered inhibition in Ts65Dn, a mouse model of Down syndrome. Brain Res. 1440, 1-8.
38. Moldrich, R.X., Dauphinot, L., Laffaire, J., Rossier, J., Potier, M.C., 2007. Down syndrome gene dosage imbalance on cerebellum development. Prog. Neurobiol. 82, 87-94. (Pubitemid 46829600)
39. Necchi, D., Lomoio, S., Scherini, E., 2008. Axonal abnormalities in cerebellar Purkinje cells of the Ts65Dn mouse. Brain Res. 1238, 181-188.
40. O'Doherty, A., Ruf, S., Mulligan, C., Hildreth, V., Errington, M.L., Cooke, S., Sesay, A., Modino, S., Vanes, L., Hernandez, D., Linehan, J.M., Sharpe, P.T., Brandner, S., Bliss, T.V.P., Henderson, D.J., Nizetic, D., Tybulewicz, V.L.J., Fisher, E.M.C., 2005. An aneuploid mouse strain carrying human chromosome 21 with Down syndrome phenotypes. Science 309, 2033-2037.
41. O'Nuallain, S., Flanagan, O., Raffat, I., Avalos, G., Dineen, B., 2007. The prevalence of Down syndrome in County Galway. Ir. Med. J. 100, 329-331.
42. Parker, S.E., Mai, C.T., Canfield, M.A., Rickard, R., Wang, Y., Meyer, R.E., Anderson, P., Mason, C.A., Collins, J.S., Kirby, R.S., Correa, A., 2010. Updated national birth prevalence estimates for selected birth defects in the United States, 2004-2006. Birth Defects Res. A Clin. Mol. Teratol. 88, 1008-1016.
43. Pinter, J.D., Eliez, S., Schmitt, J.E., Capone, G.T., Reiss, A.L., 2001. Neuroanatomy of Down's syndrome: a high-resolution MRI study. Am. J. Psychiatry 158, 1659-1665. (Pubitemid 32923659)
44. Pugh, J.R., Jahr, C.E., 2011. Axonal GABAA receptors increase cerebellar granule cell excitability and synaptic activity. J. Neurosci. 31, 565-574.
45. Raz, N., Torres, I.J., Briggs, S.D., Spencer, W.D., Thornton, A.E., Loken, W.J., Gunning, F.M., McQuain, J.D., Driesen, N.R., Acker, J.D., 1995. Selective neuroanatomic abnormalities in Down's syndrome and their cognitive correlates: evidence from MRI morphometry. Neurology 45, 356-366.
46. Reeves, R.H., Irving, N.G., Moran, T.H., Wohn, A., Kitt, C., Sisodia, S.S., Schmidt, C., Bronson, R.T., Davisson, M.T., 1995. A mouse model for Down syndrome exhibits learning and behaviour deficits. Nat. Genet. 11, 177-184.
47. Roper, R.J., Baxter, L.L., Saran, N.G., Klinedinst, D.K., Beachy, P.A., Reeves, R.H., 2006. Defective cerebellar response to mitogenic Hedgehog signaling in Down's syndrome mice. Proc. Natl. Acad. Sci. U. S. A. 103, 1452-1456. (Pubitemid 43191186)
48. Saarinen, A., Linne, M.L., Yli-Harja, O., 2008. Stochastic differential equation model for cerebellar granule cell excitability. PLoS Comput. Biol. 4, e1000004.
49. Spano, M., Mercuri, E., Rando, T., Panto, T., Gagliano, A., Henderson, S., Guzzetta, F., 1999. Motor and perceptual-motor competence in children with Down syndrome: variation in performance with age. Eur. J. Paediatr. Neurol. 3, 7-13.
50. Truett, G.E., Heeger, P., Mynatt, R.L., Truett, A.A., Walker, J.A., Warman, M.L., 2000. Preparation of PCR-quality mouse genomic DNA with hot sodium hydroxide and tris (HotSHOT). Biotechniques 29, 52-54. (Pubitemid 30439416)
51. Turner, C.A., Presti, M.F., Newman, H.A., Bugenhagen, P., Crnic, L., Lewis, M.H., 2001. Spontaneous stereotypy in an animal model of Down syndrome: Ts65Dn mice. Behav. Genet. 31, 393-400. (Pubitemid 33043139)