CGG trinucleotide repeat length modulates neural plasticity and spatiotemporal processing in a mouse model of the fragile X premutation

Hippocampus

Volumn 22, Issue 12, 2012, Pages 2260-2275

  Hunsaker, Michael R ^a   Kim, Kyoungmi ^a   Willemsen, Rob ^b,c   Berman, Robert F ^a,c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b ERASMUS MEDICAL CENTER   (Netherlands)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

CGG KI mouse; Endophenotype; Fragile X permutation; Long term depression; Long term potentiation; Pattern separation; Spatial processing; Spatiotemporal hypergranularity; Temporal order

Indexed keywords

N METHYL DEXTRO ASPARTIC ACID RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BEHAVIOR; CELL VIABILITY; COGNITION; CONTROLLED STUDY; DEPRESSION; FRAGILE X PREMUTATION; GENE MUTATION; GENOMIC INSTABILITY; HIPPOCAMPUS; HISTOPATHOLOGY; MALE; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; TASK PERFORMANCE; TEMPORAL LOBE; TRINUCLEOTIDE REPEAT;

ANIMALS; BEHAVIOR, ANIMAL; CLUSTER ANALYSIS; DISEASE MODELS, ANIMAL; FRAGILE X MENTAL RETARDATION PROTEIN; FRAGILE X SYNDROME; GENOTYPE; HUMANS; LEARNING; MALE; MICE; MICE, TRANSGENIC; NEURONAL PLASTICITY; PATCH-CLAMP TECHNIQUES; SUPPORT VECTOR MACHINES; TRINUCLEOTIDE REPEATS;

EID: 84869866357     PISSN: 10509631     EISSN: 10981063     Source Type: Journal    
DOI: 10.1002/hipo.22043     Document Type: Article

References (51)

1. Aimone JB, Deng W, Gage FH. 2011. Resolving new memories: A critical look at the dentate gyrus, adult neurogenesis, and pattern separation. Neuron 70: 589-596.
2. Bear MF, Huber KM, Warren ST. 2004. The mGluR theory of fragile × mental retardation. Trends Neurosci 27: 370-377.
3. Benjamini Y, Drai D, Elmer G, Kafkafi N, Golani I. 2001. Controlling the false discovery rate in behavior genetics research. Behav Brain Res 125(1-2): 279-284.
4. Berman RF, Murray KD, Arque G, Hunsaker MR, Wenzel HJ. 2012. Abnormal dendrite and spine morphology in primary visual cortex in the CGG knock-in mouse model of the fragile X premutation. Epilepsia 53(Suppl 1): 149-159.
5. Brouwer JR, Huizer K, Severijnen LA, Hukema RK, Berman RF, Oostra BA, Willemsen R. 2008. CGG-repeat length and neuropathological and molecular correlates in a mouse model for fragile X-associated tremor/ataxia syndrome. J Neurochem 107: 1671-1682.
6. Chen Y, Tassone F, Berman RF, Hagerman PJ, Hagerman RJ, Willemsen R, Pessah IN. 2010. Murine hippocampal neurons expressing Fmr1 gene premutations show early developmental deficits and late degeneration. Hum Mol Genet 19: 196-208.
7. Cornish KM, Kogan CS, Li L, Turk J, Jacquemont S, Hagerman RJ. 2009. Lifespan changes in working memory in fragile X premutation males. Brain Cogn 69(3): 551-558.
8. Cowell RA, Bussey TJ, Saksida LM. 2010. Components of recognition memory: Dissociable cognitive processes or just differences in representational complexity? Hippocampus 20: 1245-1262.
9. Diep AA, Hunsaker MR, Kwock R, Kim K, Willemsen R, Berman RF. 2012. Female CGG knock-in mice modeling the fragile X premutation are impaired on a skilled forelimb reaching task. Neurobiol Learn Mem 97: 229-234.
10. Entezam A, Biacsi R, Orrison B, Saha T, Hoffman GE, Grabczyk E, Nussbaum RL, Usdin K. 2007. Regional FMRP deficits and large repeat expansions into the full mutation range in a new Fragile X premutation mouse model. Gene 395(1-2): 125-134.
11. Faul F, Erdfelder E, Buchner A, Lang AG. 2009. Statistical power analyses using G*Power 3.1: tests for correlation and regression analyses. Behav Res Methods 41: 1149-1160.
12. Faul F, Erdfelder E, Lang AG, Buchner A. 2007. G*Power 3: A flexible statistical power analysis program for the social, behavioral, and biomedical sciences. Behav Res Methods 39: 175-191.
13. Goodrich-Hunsaker NJ, Hunsaker MR, Kesner RP. 2005. Dissociating the role of the parietal cortex and dorsal hippocampus for spatial information processing. Behav Neurosci 119: 1307-1315.
14. Goodrich-Hunsaker NJ, Wong LM, McLennan Y, Srivastava S, Tassone F, Harvey D, Rivera SM, Simon TJ. 2011a. Young adult female fragile X premutation carriers show age- and genetically-modulated cognitive impairments. Brain Cogn 75: 255-260.
15. Goodrich-Hunsaker NJ, Wong LM, McLennan Y, Tassone F, Harvey D, Rivera SM, Simon TJ. 2011b. Enhanced manual and oral motor reaction time in young adult female fragile X premutation carriers. J Int Neuropsychol Soc 17: 746-750.
16. Goodrich-Hunsaker NJ, Wong LM, McLennan Y, Tassone F, Harvey D, Rivera SM, Simon TJ. 2011c. Adult female fragile X premutation carriers exhibit age- and CGG repeat length-related impairments on an attentionally based enumeration task. Front Hum Neurosci 5: 63.
17. Gottesman II, Gould TD. 2003. The endophenotype concept in psychiatry: Etymology and strategic intentions. Am J Psychiatry 160: 636-645.
18. Hanson JE, Madison DV. 2011. Imbalanced pattern completion vs. separation in cognitive disease: Network simulations of synaptic pathologies predict a personalized therapeutics strategy. BMC Neurosci 11: 96.
19. Hessl D, Wang JM, Schneider A, Koldewyn K, Le L, Iwahashi C, Cheung K, Tassone F, Hagerman PJ, Rivera SM. 2011. Decreased fragile X mental retardation protein expression underlies amygdala dysfunction in carriers of the fragile X premutation. Biol Psychiatry 70: 859-865.
20. Hoem G, Raske CR, Garcia-Arocena D, Tassone F, Sanchez E, Ludwig AL, Iwahashi CK, Kumar M, Yang JE, Hagerman PJ. 2011. CGG-repeat length threshold for FMR1 RNA pathogenesis in a cellular model for FXTAS. Hum Mol Genet 20: 2161-2170.
21. Hunsaker MR. 2012. Comprehensive neurocognitive endophenotyping strategies for mouse models of genetic disorders. Prog Neurobiol 96: 220-241.
22. Hunsaker MR, Greco CM, Tassone F, Berman RF, Willemsen R, Hagerman RJ, Hagerman PJ. 2011a. Rare intranuclear inclusions in the brains of 3 older adult males with fragile x syndrome: implications for the spectrum of fragile x-associated disorders. J Neuropathol Exp Neurol 70: 462-469.
23. Hunsaker MR, Goodrich-Hunsaker NJ, Willemsen R, Berman RF. 2010. Temporal ordering deficits in female CGG KI mice heterozygous for the fragile X premutation. Behav Brain Res 213: 263-268.
24. Hunsaker MR, von Leden RE, Ta BT, Goodrich-Hunsaker NJ, Arque G, Kim K, Willemsen R, Berman RF. 2011b. Motor deficits on a ladder rung task in male and female adolescent and adult CGG knock-in mice. Behav Brain Res 222: 117-121.
25. Hunsaker MR, Wenzel HJ, Willemsen R, Berman RF. 2009. Progressive spatial processing deficits in a mouse model of the fragile X premutation. Behav Neurosci 123: 1315-1324.
26. Hunter JE, Rohr JK, Sherman SL. 2010. Co-occurring diagnoses among FMR1 premutation allele carriers. Clin Genet 77: 374-381.
27. Hunter JE, Abramowitz A, Rusin M, Sherman SL. 2009. Is there evidence for neuropsychological and neurobehavioral phenotypes among adults without FXTAS who carry the FMR1 premutation? A review of current literature. Genet Med 11: 79-89.
28. Jin P, Zarnescu DC, Zhang F, Pearson CE, Lucchesi JC, Moses K, Warren ST. 2003. RNA-mediated neurodegeneration caused by the fragile X premutation rCGG repeats in Drosophila. Neuron 39: 739-747.
29. Johnson-Glenberg MC. 2008. Fragile X syndrome: Neural network models of sequencing and memory. Cogn Syst Res 9: 274-292.
30. Kéri S, Benedek G. 2010. The perception of biological and mechanical motion in female fragile X premutation carriers. Brain Cogn 72: 197-201.
31. Kéri S, Benedek G. 2009. Visual pathway deficit in female fragile X premutation carriers: A potential endophenotype. Brain Cogn 69: 291-295.
32. Kesner RP. 2007. A behavioral analysis of dentate gyrus function. Prog Brain Res 163: 567-576.
33. Kesner RP, Goodrich-Hunsaker NJ. 2010. Developing an animal model of human amnesia: The role of the hippocampus. Neuropsychologia 48: 2290-2302.
34. Kesner RP, Lee I, Gilbert P. 2004. A behavioral assessment of hippocampal function based on a subregional analysis. Rev Neurosci 15: 333-351.
35. Koldewyn K, Hessl D, Adams J, Tassone F, Hagerman PJ, Hagerman RJ, Rivera SM. 2008. Reduced hippocampal activation during recall is associated with elevated FMR1 mRNA and psychiatric symptoms in men with the fragile X Premutation. Brain Imaging Behav 2: 105-116.
36. McTighe SM, Cowell RA, Winters BD, Bussey TJ, Saksida LM. 2010. Paradoxical false memory for objects after brain damage. Science 330: 1408-1410.
37. Napoli E, Ross-Inta C, Wong S, Omanska-Klusek A, Barrow C, Iwahashi C, Garcia-Arocena D, Sakaguchi D, Berry-Kravis E, Hagerman R, Hagerman PJ, Giulivi C. 2011. Altered zinc transport disrupts mitochondrial protein processing/import in fragile X-associated tremor/ataxia syndrome. Hum Mol Genet 20: 3079-3092.
38. Qin M, Entezam A, Usdin K, Huang T, Liu ZH, Hoffman GE, Smith CB. 2011. A mouse model of the fragile X premutation: Effects on behavior, dendrite morphology, and regional rates of cerebral protein synthesis. Neurobiol Dis 42: 85-98.
39. R Development Core Team. 2011. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN3-900051-07-0, URL Available at: http://www.R-project.org/.
40. Raske C, Hagerman PJ. 2009. Molecular pathogenesis of fragile X-associated tremor/ataxia syndrome. J Investig Med 57: 825-829.
41. Rolls ET, Kesner RP. 2006. A computational theory of hippocampal function, and empirical tests of the theory. Prog Neurobiol 79: 1-48.
42. Ross-Inta C, Omanska-Klusek A, Wong S, Barrow C, Garcia-Arocena D, Iwahashi C, Berry-Kravis E, Hagerman RJ, Hagerman PJ, Giulivi C. 2010. Evidence of mitochondrial dysfunction in fragile X-associated tremor/ataxia syndrome. Biochem J 429: 545-552.
43. Saluto A, Brussino A, Tassone F, Arduino C, Cagnoli C, Pappi P, Hagerman P, Migone N, Brusco A. 2005. An enhanced polymerase chain reaction assay to detect pre- and full mutation alleles of the fragile X mental retardation 1 gene. J Mol Diagnosis 7: 605-612.
44. Simon TJ. 2008. A new account of the neurocognitive foundations of impairments in space, time and number processing in children with chromosome 22q11.2 deletion syndrome. Dev Disabil Res Rev 14: 52-58.
45. Simon TJ. 2011. Clues to the foundations of numerical cognitive impairments: Evidence from genetic disorders. Dev Neuropsychol 36: 788-805.
46. Tassone F, Hagerman RJ, Taylor AK, Gane LW, Godfrey TE, Hagerman PJ. 2000. Elevated levels of FMR1 mRNA in carrier males: a new mechanism of involvement in the fragile-X syndrome. Am J Hum Genet 66: 6-15.
47. Tassone F, Hagerman RJ, Taylor AK, Mills JB, Harris SW, Gane LW, Hagerman PJ. 2000. Clinical involvement and protein expression in individuals with the FMR1 premutation. Am J Med Genet 91: 144-152.
48. Tassone F, Pan R, Amiri K, Taylor AK, Hagerman PJ. 2008. A rapid polymerase chain reaction-based screening method for identification of all expanded alleles of the fragile X (FMR1) gene in newborn and high-risk populations. J Mol Diagn 10: 43-49.
49. van Dam D, Errijgers V, Kooy RF, Willemsen R, Mientjes E, Oostra BA, De Deyn PP. 2005. Cognitive decline, neuromotor and behavioural disturbances in a mouse model for fragile-X-associated tremor/ataxia syndrome (FXTAS). Behav Brain Res 162: 233-239.
50. Ward JHJr. 1963. Hierarchical grouping to optimize an objective function. J Am Stat Assoc 58: 236-244.
51. Yassa MA, Stark CE. 2011. Pattern separation in the hippocampus. Trends Neurosci 34: 515-525.