Female CGG knock-in mice modeling the fragile X premutation are impaired on a skilled forelimb reaching task

Neurobiology of Learning and Memory

Volumn 97, Issue 2, 2012, Pages 229-234

  Diep, Amanda A ^a   Hunsaker, Michael R ^a,b   Kwock, Richard ^a   Kim, Kyoungmi ^a   Willemsen, Rob ^b,c   Berman, Robert F ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c ERASMUS MEDICAL CENTER   (Netherlands)

Author keywords

Fragile X premutation; Fragile X associated disorders; Motor function; Skilled reaching; Transgenic mice

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN DYSFUNCTION; CCG REPEAT; COGNITIVE DEFECT; CONTROLLED STUDY; DISEASE ASSOCIATION; DISEASE COURSE; DNA STRUCTURE; EXPERIMENTAL MODEL; FEMALE; FMR1 GENE; FORELIMB; FRAGILE X PREMUTATION; FRAGILE X SYNDROME; GENE MUTATION; GENE PRODUCT; GENOTYPE; HETEROZYGOTE; INFORMATION PROCESSING; LEARNING DISORDER; MOTOR DYSFUNCTION; MOTOR SYSTEM; MOUSE; NEUROPATHOLOGY; NONHUMAN; TASK PERFORMANCE; TRINUCLEOTIDE REPEAT; VISUAL IMPAIRMENT; VISUAL SYSTEM; WILD TYPE;

ANIMALS; BEHAVIOR, ANIMAL; FEMALE; FORELIMB; FRAGILE X MENTAL RETARDATION PROTEIN; GENE KNOCK-IN TECHNIQUES; MICE; MICE, TRANSGENIC; MOVEMENT; PSYCHOMOTOR PERFORMANCE; TRINUCLEOTIDE REPEAT EXPANSION;

EID: 84856771413     PISSN: 10747427     EISSN: 10959564     Source Type: Journal    
DOI: 10.1016/j.nlm.2011.12.006     Document Type: Article

References (52)

1. Adams J.S., Adams P.E., Nguyen D., Brunberg J.A., Tassone F., Zhang W., et al. Volumetric brain changes in females with fragile X-associated tremor/ataxia syndrome (FXTAS). Neurology 2007, 69:851-859.
2. Barneoud P., Descombris E., Aubin N., Abrous D.N. Evaluation of simple and complex sensorimotor behaviours in rats with a partial lesion of the dopaminergic nigrostriatal system. European Journal of Neuroscience 2000, 12:322-336.
3. Bays P.M., Singh-Curry V., Gorgoraptis N., Driver J., Husain M. Integration of goal- and stimulus-created visual signals revealed by damage to human parietal cortex. Journal of Neuroscience 2010, 30:5968-5978.
4. Beloozerova I.N., Sirota M.G. Integration of motor and visual information in the parietal area 5 during locomotion. Journal of Neurophysiology 2003, 90:961-971.
5. Benjamini Y., Drai D., Elmer G., Kafkafi N., Golani I. Controlling the false discovery rate in behavior genetics research. Behavioural Brain Research 2001, 125:279-284.
6. Berman R.F., Willemsen R. Mouse models of fragile X-associated tremor ataxia. Journal of Investigative Medicine 2009, 57:837-841.
7. Bernier P.-M., Grafton S.T. Human posterior parietal cortex flexibly determines reference frames for reaching based on sensory context. Neuron 2010, 68:776-788.
8. Beurze S.M., Toni I., Pisella L., Medendorp W.P. Reference frames for reach planning in human parietofrontal cortex. Journal of Neurophysiology 2010, 104:1736-1745.
9. Brouwer J.R., Huizer K., Severijnen L.A., Hukema R.K., Berman R.F., Oostra B.A., et al. CGG-repeat length and neuropathological and molecular correlates in a mouse model for fragile X-associated tremor/ataxia syndrome. Journal of Neurochemistry 2008, 107:176-183.
10. Buitrago M.M., Ringer T., Schulz J.B., Dichgans J., Luft A.R. Characterization of motor skill and instrumental learning time scales in a skilled reaching task in rat. Behavioural Brain Research 2004, 155:249-256.
11. Ceravolo R., Antonini A., Volterrani D., Rossi C., Goldwurm S., Di Maria E., et al. Dopamine transporter imaging study in parkinsonism occurring in fragile X premutation carriers. Neurology 2005, 65:1971-1973.
12. Clower D.M., Dum R.P., Strick P.L. Basal ganglia and cerebellar inputs to 'AIP'. Cerebral Cortex 2005, 15:913-920.
13. Clower D.M., West R.A., Lynch J.C., Strick P.L. The inferior parietal lobule is the target of output from the superior colliculus, hippocampus, and cerebellum. Journal of Neuroscience 2001, 21:6283-6291.
14. Cunningham C.L., Martinez-Cerdeno V., Navarro-Porras E., Prakash A.N., Angelastro J.M., Willemsen R., et al. Premutation CGG-repeat expansion of the FMR1 gene impairs mouse neocortical development. Human Molecular Genetics 2011, 20:64-79.
15. Faraji J., Metz G.A. Sequential bilateral lesions have additive effects on single skilled limb use in rats. Behavioural Brain Research 2007, 177:195-204.
16. Farr T.D., Whishaw I.Q. Quantitative and qualitative impairments in skilled reaching in the mouse (Mus musculus) after a focal motor cortex stroke. Stroke 2002, 33:1869-1875.
17. Gallistel C.R., Fairhurst S., Balsam P. The learning curve: Implications of a quantitative analysis. Proceedings of the National Academy of Sciences, USA 2004, 101:13124-13131.
18. Galvan A., Floran B., Erlij D., Aceves J. Intrapallidal dopamine restores motor deficits induced by 6-hydroxydopamine in the rat. Journal of Neural Transmission 2001, 108:153-166.
19. Garcia-Arocena D., Hagerman P. Advances in understanding the molecular basis of FXTAS. Human Molecular Genetics 2010, 19:83-89.
20. Goodale M.A., Foreman N.P., Milner A.D. Visual orientation in the rat: A double dissociation of deficits following cortical and collicular lesions. Experimental Brain Research 1978, 31:445-457.
21. Goodrich-Hunsaker N.J., Wong L.M., McLennan Y., Srivastava S., Tassone F., Harvey D., Simon T.J. Young adult female fragile X premutation carriers show age- and genetically-modulated cognitive impairments. Brain and Cognition 2011, 75:255-260.
22. Goodrich-Hunsaker N.J., Wong L.M., McLennan Y., Srivastava S., Tassone F., Harvey D., Simon T.J. Enhanced manual and oral motor reaction time in young adult female fragile X premutation carriers. Journal of the International Neuropsychiatric Society 2011, 21:1-5.
23. Goodrich-Hunsaker N.J., Wong L.M., McLennan Y., Tassone F., Harvey D., Simon T.J. Adult female fragile X premutation carriers exhibit age- and CGG repeat length-related impairments on an attentionally based enumeration task. Frontiers in Human Neuroscience 2011, 5:63.
24. Hagerman P.J. The fragile X prevalence paradox. Journal of Medical Genetics 2008, 45:498-499.
25. Hall D.A., Berry-Kravis E., Hagerman R.J., Hagerman P.J., Rice C.D., Leehey M.A. Symptomatic treatment in the fragile X-associated tremor/ataxia syndrome. Movement Disorders 2006, 21:1741-1744.
26. Hermer-Vazquez L., Hermer-Vazquez R., Chapin J.K. The reach-to-grasp-food task for rats: a rare case of modularity in animal behavior?. Behavioural Brain Research 2007, 177:322-328.
27. Hikosaka O., Nakamura K., Sakai K., Nakahara H. Central mechanisms of motor skill learning. Current Opinion in Neurobiology 2002, 12:217-222.
28. Hunsaker M.R., Goodrich-Hunsaker N.J., Willemsen R., Berman R.F. Temporal ordering deficits in female CGG KI mice heterozygous for the fragile X premutation. Behavioural Brain Research 2010, 213:263-268.
29. Hunsaker M.R., von Leden R.E., Ta B.T., Goodrich-Hunsaker N.J., Arque G., Kim K.M., et al. Motor deficits on a ladder rung task in male and female adolescent CGG knock-in mice. Behavioural Brain Research 2011, 222:117-121.
30. Hunsaker M.R., Wenzel H.J., Willemsen R., Berman R.F. Progressive spatial processing deficits in a mouse model of the fragile X premutation. Behavioral Neuroscience 2009, 123:1315-1324.
31. Jeyasingham R.A., Baird A.L., Meldrum A., Dunnett S.B. Differential effects of unilateral striatal and nigrostriatal lesions on grip strength, skilled paw reaching and drug-induced rotation in the rat. Brain Research Bulletin 2001, 55:541-548.
32. Keri S., Benedek G. Visual pathway deficit in female fragile X premutation carriers: A potential endophenotype. Brain and Cognition 2009, 69:291-295.
33. Keri S., Benedek G. The perception of biological and mechanical motion in female fragile X premutation carriers. Brain and Cognition 2010, 72:197-201.
34. Kolb B., Gibb R. Tactile stimulation after frontal or parietal cortical injury in infant rats facilitates functional recovery and produces synaptic changes in adjacent cortex. Behavioural Brain Research 2010, 214:115-120.
35. Lachiewicz A.M., Dawson D.V., Spiridigliozzi G.A., McConkie-Rosell A. Arithmetic difficulties in females with the fragile X premutation. American Journal of Medical Genetics A 2006, 140:665-672.
36. MacKinnon D.A., Gross C.G., Bender D.B. A visual deficit after superior colliculus lesions in monkeys. Acta Neurobiologiae Experimentalis 1976, 36:169-180.
37. Melvin K.G., Doan J., Pellis S.M., Brown L., Whishaw I.Q., Suchowersky O. Pallidal deep brain stimulation and L-dopa do not improve qualitative aspects of skilled reaching in Parkinson's disease. Behavioural Brain Research 2005, 160:188-194.
38. Meredith M.A., Stein B.E. Visual, auditory, and somatosensory convergence on cells in superior colliculus results in multisensory integration. Journal of Neurophysiology 1986, 56:640-662.
39. Mutha P.K., Sainburg R.L., Haaland K.Y. Coordination deficits in ideomotor apraxia during visually targeted reaching reflect impaired visuomotor transformations. Neuropsychologia 2010, 48:3855-3867.
40. Narcisa, V., Aguilar, D., Nguyen, D. V., Campos, L., Brodovsky, J., White, S., Hagerman, R. J. (2011). A quantitative assessment of tremor and ataxia in female FMR1 premutation carriers using CATSYS. Current Gerontology and Genomics Research doi:. doi:10.1155/2011/484713.
41. R Development Core Team (2011). R: A language and environment for statistical computing. R foundation for statistical computing. Vienna, Austria. http://www.R-project.org/.
42. Redish A.D., Touretzky D.S. The reaching task: Evidence for vector arithmetic in the motor system?. Biological Cybernetics 1994, 71:307-317.
43. Scaglione C., Ginestroni A., Vella A., Dotti M.T., Nave R.D., Rizzo G., et al. MRI and SPECT of midbrain and striatal degeneration in fragile X-associated tremor/ataxia syndrome. Journal of Neurology 2008, 255:144-146.
44. Simon T.J. A new account of the neurocognitive foundations of impairments in space, time and number processing in children with chromosome 22q11.2 deletion syndrome. Developmental Disabilities Research Reviews 2008, 14:52-58.
45. Sprague J.M., Meikle T.H. The role of the superior colliculus in visually guided behavior. Experimental Neurology 1965, 11:115-146.
46. Tennant K.A., Jones T.A. Sensorimotor behavioral effects of endothelin-1 induced small cortical infarcts in C57BL/6 mice. Journal of Neuroscience Methods 2009, 181:18-26.
47. van Dam D., Errijgers V., Kooy R.F., Willemsen R., Mientjes E., Oostra B.A., et al. Cognitive decline, neuromotor and behavioural disturbances in a mouse model for fragile-X-associated tremor/ataxia syndrome (FXTAS). Behavioural Brain Research 2005, 162:233-239.
48. Vergara-Aragon P., Gonzalez C.L., Whishaw I.Q. A novel skilled-reaching impairment in paw supination on the "good" side of the hemi-Parkinson rat improved with rehabilitation. Journal of Neuroscience 2003, 23:579-586.
49. Wang H., Wu L.J., Kim S.S., Lee F.J., Gong B., Toyoda H., et al. FMRP acts as a key messenger for dopamine modulation in the forebrain. Neuron 2008, 59:634-647.
50. Wenzel H.J., Hunsaker M.R., Greco C.M., Willemsen R., Berman R.F. Ubiquitin-positive intranuclear inclusions in neuronal and glial cells in a mouse model of the fragile X premutation. Brain Research 2010, 1318:155-166.
51. Whishaw I.Q., Zeeb F., Erickson C., McDonald R.J. Neurotoxic lesions of the caudate-putamen on a reaching for food task in the rat: Acute sensorimotor neglect and chronic qualitative motor impairment follow lateral lesions and improved success follows medial lesions. Neuroscience 2007, 146:86-97.
52. Willemsen R., Hoogeveen-Westerveld M., Reis S., Holstege J., Severijnen L.A., Nieuwenhuizen I.M., et al. The FMR1 CGG repeat mouse displays ubiquitin-positive intranuclear neuronal inclusions; implications for the cerebellar tremor/ataxia syndrome. Human Molecular Genetics 2003, 12:949-959.