Size does not always matter: Ts65Dn down syndrome mice show cerebellum-dependent motor learning deficits that cannot be rescued by postnatal SAG treatment

Journal of Neuroscience

Volumn 33, Issue 39, 2013, Pages 15408-15413

  Gutierrez Castellanos, Nicolas ^a   Winkelman, Beerend H J ^a   Tolosa Rodriguez, Leonardo ^a   Devenney, Benjamin ^b   Reeves, Roger H ^b   De Zeeuw, Chris I ^a,c  

^a NETHERLANDS INSTITUTE FOR NEUROSCIENCE   (Netherlands)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c ERASMUS MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

SMOOTHENED PROTEIN;

ACTION POTENTIAL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BEHAVIOR; BODY WEIGHT; CELL DENSITY; CEREBELLUM CORTEX; CONTROLLED STUDY; DOWN SYNDROME; EYE MOVEMENT; LEARNING DISORDER; MOUSE; NONHUMAN; OCULOMOTOR NERVE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PURKINJE CELL; SENSORIMOTOR FUNCTION; VESTIBULOOCULAR REFLEX; VISUAL STIMULATION;

ANIMALS; CEREBELLUM; CYCLOHEXYLAMINES; DISEASE MODELS, ANIMAL; DOWN SYNDROME; HEDGEHOG PROTEINS; LEARNING; MEMORY; MICE; PURKINJE CELLS; REFLEX, VESTIBULO-OCULAR; SYNAPSES; THIOPHENES;

EID: 84884579475     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2198-13.2013     Document Type: Article

References (31)

1. Aylward EH, Habbak R, Warren AC, Pulsifer MB, Barta PE, Jerram M, Pearlson GD (1997) Cerebellar volume in adults with Down syndrome. Arch Neurol 54:209-212. CrossRef Medline
2. Baxter LL, Moran TH, Richtsmeier JT, Troncoso J, Reeves RH (2000) Discovery and genetic localization of Down syndrome cerebellar phenotypes using the Ts65Dn mouse. Hum Mol Genet 9:195-202. CrossRef Medline
3. Burguière E, Arleo A, Hojjati MR, Elgersma Y, De Zeeuw CI, Berthoz A, Rondi-Reig L (2005) Spatial navigation impairment in mice lacking cerebellar LTD: a motor adaptation deficit? Nat Neurosci 8:1292-1294. CrossRef Medline
4. Chen JK, Taipale J, Young KE, Maiti T, Beachy PA (2002) Small molecule modulation of smoothened activity. Proc Natl Acad Sci U S A 99:14071-14076. CrossRef Medline
5. Costa AC (2011) An assessment of the vestibulo-ocular reflex (VOR) in persons with Down syndrome. Exp Brain Res 214:199-213. CrossRef Medline
6. Costa AC, Walsh K, Davisson MT (1999) Motor dysfunction in a mouse model for Down syndrome. Physiol Behav 68:211-220. CrossRef Medline
7. Costa AC, Stasko MR, Schmidt C, Davisson MT (2010) Behavioral validation of the Ts65Dn mouse model for Down syndrome of a genetic background free of the retinal degeneration mutation Pde6b(rd1). Behav Brain Res 206:52-62. CrossRef Medline
8. Currier DG, Polk RC, Reeves RH (2012) A Sonic hedgehog (Shh) response deficit in trisomic cells may be a common denominator for multiple features of Down syndrome. Prog Brain Res 197:223-236. CrossRef Medline
9. Dahmane N, Ruiz i Altaba A (1999) Sonic hedgehog regulates the growth and patterning of the cerebellum. Development 126:3089-3100. Medline
10. Das I, Park JM, Shin JH, Jeon SK, Lorenzi H, Linden DJ, Worley PF, Reeves RH (2013) Hedgehog agonist therapy corrects structural and cognitive deficits in a Down syndrome mouse model. Sci Translational Med 5:201ra120. CrossRef.
11. de Jeu M, De Zeeuw CI (2012) Video-oculography in mice. J Vis Exp 65; e3971. CrossRef Medline
12. Di Filippo FM, Tozzi A, Ghiglieri V, Picconi B, Costa C, Cipriani S, Tantucci M, Belcastro V, Calabresi P (2010) Impaired plasticity at specific subset of striatal synapses in the Ts65Dn mouse model of Down syndrome. Biol Psychiatry 67:666-671. CrossRef Medline
13. Epstein C (1986) The consequences of chromosome imbalance: principles, mechanisms, and models. Cambridge: Cambridge UP.
14. Galliano E, Gao Z, Schonewille M, Todorov B, Simons E, Pop AS, D'Angelo E, van den Maagdenberg AM, Hoebeek FE, De Zeeuw CI (2013) Silencing the majority of cerebellar granule cells uncovers their essential role in motor learning and consolidation. Cell Reports 3:1239-1251. CrossRef Medline
15. Gao Z, van Beugen BJ, De Zeeuw CI (2012) Distributed synergistic plasticity and cerebellar learning. Nat Rev Neurosci 13:619-635. CrossRef Medline
16. Gutierrez-Castellanos N, Winkelman BH, Tolosa-Rodriguez L, De Gruijl JR, De Zeeuw CI (2013) Impact of aging on long-term ocular reflex adaptation. Neurobiol Aging pii: S0197-4580(13)00267-4. CrossRef Medline
17. Hyde LA, Crnic LS, Pollock A, Bickford PC (2001) Motor learning in Ts65Dn mice, a model for Down syndrome. Dev Psychobiol 38:33-45. CrossRef Medline
18. Kaminski HJ, Richmonds CR (2002) Extraocular muscle fatigue. Ann N Y Acad Sci 956:397-398. CrossRef Medline
19. Kleschevnikov AM, Belichenko PV, Gall J, George L, Nosheny R, Maloney MT, Salehi A, Mobley WC (2012) Increased efficiency of the GABAA and GABAB receptor-mediated neurotransmission in the Ts65Dn mouse model of Down syndrome. Neurobiol Dis 45:683-691. CrossRef Medline
20. Martínez-Cué C, Martínez P, Rueda N, Vidal R, García S, Vidal V, Corrales A, Montero JA, Pazosá, Flórez J, Gasser R, Thomas AW, Honer M, Knoflach F, Trejo JL, Wettstein JG, Hernández MC (2013) Reducing GABAA α5 receptor-mediated inhibition rescues functional and neuromorphological deficits in a mouse model of down syndrome. J Neurosci 33:3953-3966. CrossRef Medline
21. Olson LE, Roper RJ, Baxter LL, Carlson EJ, Epstein CJ, Reeves RH (2004) Down syndrome mouse models Ts65Dn, Ts1Cje, and Ms1Cje/Ts65Dn exhibit variable severity of cerebellar phenotypes. Dev Dyn 230:581-589. CrossRef Medline
22. Pereira PL, Magnol L, Sahún I, Brault V, Duchon A, Prandini P, Gruart A, Bizot JC, Chadefaux-Vekemans B, Deutsch S, Trovero F, Delgado-García JM, Antonarakis SE, Dierssen M, Herault Y (2009) A new mouse model for the trisomy of the Abcg1-U2af1 region reveals the complexity of the combinatorial genetic code of down syndrome. Hum Mol Genet 18: 4756-4769. CrossRef Medline
23. Reeves RH, Irving NG, Moran TH, Wohn A, Kitt C, Sisodia SS, Schmidt C, Bronson RT, Davisson MT (1995) A mouse model for Down syndrome exhibits learning and behaviour deficits. Nat Genet 11:177-184. CrossRef Medline
24. Reinholdt LG, Ding Y, Gilbert GT, Czechanski A, Solzak JP, Roper RJ, Johnson MT, Donahue LR, Lutz C, Davisson MT (2011) Molecular characterization of the translocation breakpoints in the Down syndrome mouse model Ts65Dn. Mamm Genome 22:685-691. CrossRef Medline
25. Roper RJ, Baxter LL, Saran NG, Klinedinst DK, Beachy PA, Reeves RH (2006) Defective cerebellar response to mitogenic hedgehog signaling in Down syndrome mice. Proc Natl Acad Sci U S A 103:1452-1456. CrossRef Medline
26. Seja P, Schonewille M, Spitzmaul G, Badura A, Klein I, Rudhard Y, Wisden W, Hübner CA, De Zeeuw CI, Jentsch TJ (2012) Raising cytosolic Cl- in cerebellar granule cells affects their excitability and vestibulo-ocular learning. EMBO J 31:1217-1230. CrossRef Medline
27. Stahl JS, van Alphen AM, De Zeeuw CI (2000) A comparison of video and magnetic search coil recordings of mouse eye movements. J Neurosci Methods 99:101-110. CrossRef Medline
28. Usowicz MM, Garden CL (2012) Increased excitability and altered action potential waveform in cerebellar granule neurons of the Ts65Dn mouse model of Down syndrome. Brain Res 1465:10-17. CrossRef Medline
29. van Alphen AM, Stahl JS, De Zeeuw CI (2001) The dynamic characteristics of the mouse horizontal vestibulo-ocular and optokinetic response. Brain Res 890:296-305. CrossRef Medline
30. Wallace VA (1999) Purkinje-cell-derived Sonic hedgehog regulates granule neuron precursor cell proliferation in the developing mouse cerebellum. Curr Biol 9:445-448. CrossRef Medline
31. Wechsler-Reya RJ, Scott MP (1999) Control of neuronal precursor proliferation in the cerebellum by Sonic hedgehog. Neuron 22:103-114. CrossRef Medline