Developmental learning impairments in a rodent model of nodular heterotopia

Journal of Neurodevelopmental Disorders

Volumn 1, Issue 3, 2009, Pages 237-250

  Threlkeld, Steven W ^a,b   Hill, Courtney A ^c   Cleary, Caitlin E ^c   Truong, Dongnhu T ^c   Rosen, Glenn D ^d,e   Fitch, R Holly ^c  

^a BROWN UNIVERSITY   (United States)

^b WOMEN AND INFANTS HOSPITAL   (United States)

^c UNIVERSITY OF CONNECTICUT   (United States)

^d BETH ISRAEL DEACONESS MEDICAL CENTER   (United States)

^e HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Auditory processing; Hippocampal dysplasia; Methylazoxymethanol induced heterotopia; Neuronal migration; Spatial learning Non spatial learning; Startle response

Indexed keywords

EID: 79955782981     PISSN: 18661947     EISSN: 18661955     Source Type: Journal    
DOI: 10.1007/s11689-009-9026-7     Document Type: Article

References (61)

1. Chang B, Ly J, Appignani B, Bodell A, Apse K, Ravenscroft R, et al. Reading impairment in the neuronal migration disorder of periventricular nodular heterotopia. Neurology 2005;64(5):799-803.
2. Chang B, Katzir T, Liu T, Corriveau K, Barzillai M, Apse K, et al. A structural basis for reading fluency: white matter deficits in a genetic brain malformation. Neurology 2007;69(23):2146-54.
3. Guerreiro M, Hage S, Guimaraes C, Abramides D, Fernandes W, Pacheco P, et al. Developmental language disorder associated with polymicrogyria. Neurology 2002;59:245-50.
4. Galaburda A, Sherman G, Rosen G, Aboitiz F, Geschwind N. Developmental dyslexia: four consecutive patients with cortical abnormalities. Ann Neurol. 1985;18(2):222-33.
5. Hage S, Cendes F, Montenegro M, Abramides D, Guimaraes C, Guerreiro M. Specific Language Impairment: Linguistic and neurobiological aspects. Arq Neuropsiquiatr. 2006;64(2-A):173-80.
6. Oliveira EP, Hage SR, Guimaraes CA, Brandao-Almeida I, Lopes-Cendes I, Guerreiro CA, et al. Characterization of language and reading skills in familial polymicrogyria. Brain Dev. 2008;30 (4):254-60.
7. Galaburda A, Menard M, Rosen G. Evidence for aberrant auditory anatomy in developmental dyslexia. Proc Natl Acad Sci USA. 1994;91:8010-3.
8. Threlkeld SW, McClure MM, Rosen GD, Fitch RH. Developmental timeframes for induction of microgyria and rapid auditory processing deficits in the rat. Brain Res. 2006;1109(1):22-31.
9. Threlkeld SW, McClure MM, Bai J, Wang Y, LoTruco JJ, Rosen GD, et al. Developmetnal disruptions and behavioral impairments in rats following in utero RNAi of Dyx1c1. Brain Res Bull. 2007;71(5):508-14.
10. Kolb B, Gibb R. Brain plasticity and recovery from early cortical injury. Dev Psychobiol. 2007;49:107-18.
11. Leng A, Jongen-Relo AL, Pothuizen HHJ, Feldon J. Effects of prenatal methylazoxymethanol acetate (MAM) treatment in rats on water maze performance. Behav Brain Res. 2005;161:291-8.
12. Battaglia G, Pagliardini S, Saglietti L, Flaminio C, Di Luca M, Bassanini S, et al. Neurogenesis in cerebral heterotopia induced in rats by prenatal methylazoxymethanol treatment. Cereb Cortex. 2003;13:736-48.
13. Fitch RH, Tallal P, Brown C, Galaburda A, Rosen GD. Induced microgyria and auditory temporal processing in rats: a model for language impairment? Cereb Cortex. 1994;4(3):260-70.
14. Clark M, Rosen G, Tallal P, Fitch RH. Impaired processing of complex auditory stimuli in rats with indiced cerebrocortical microgyria: an animal model of developmental language disabilities. J Cogn Neurosci. 2000;12(5):828-39.
15. Peiffer A, McClure M, Threlkeld S, Rosen G, Fitch RH. Severity of focal microgyria and associated rapid auditory processing deficits. NeuroReport. 2004;15(12):1923-6.
16. Peiffer A, Rosen GD, Fitch RH. Sex differences in rapid auditory processing in ectopic BXSB/MpJ mice. NeuroReport. 2002;13 (17):2277-80.
17. Tallal P, Piercy M. Defects of non-verbal auditory perception in children with developmental aphasia. Nature 1973;241 (5390):468-9.
18. Choudhury N, Leppanen PH, Leevers H, Benasich A. Infant information processing and family history of specific language impairment: converging evidence for RAP deficits from two paradigms. Dev Sci. 2007;10(2):213-36.
19. Hautus M, Setchell G, Waldie K, Kirk I. Age related improvements in auditory temporal resolution in reading-impaired children. Dyslexia 2003;9:37-45.
20. Bishop DV, McArthur GM. Immature cortical responses to auditory stimuli in specific language impairment: evidence from ERPs to rapid tone sequences. Dev Sci. 2004;7(4):11-8.
21. Gaab N, Gabrieli J, Deutsch G, Tallal P, Temple E. Neuroal correlates of rapid auditory processing are disrupted in children with developmental dyslexia and ameliorated with training: an fMRI study. Bestor Neurol Neurosci. 2007;25(3-4):295-310.
22. Cope N, Harold D, Hill G, Moskvina V, Stevenson J, Holmans P, et al. Strong evidence that KIAA0319 on chromosome 6p is a susceptibility gene for developmental dyslexia. Am J Hum Genet. 2005;76:581-91.
23. Shumacher J, Anthoni H, Dahdouh F, Konig IR, Hillmer AM, Kluck N, et al. Strong genetic evidence of DCDC2 as a susceptibility gene for dyslexia. Am J Hum Genet. 2006;78:52-62.
24. Taipale M, Kaminen N, Nopola-Hemmi J, Haltia T, Myllyluoma B, Lyytinen H, et al. A candidate gene for developmental dyslexia encodes a nuclear tetratricopeptide repeat domain protein dynamically regulated in brain. Proc Natl Acad Sci USA. 2003;100:11553-8.
25. Marino C, Citterio A, Giorda R, Facoetti A, Menozzi G, Vanzin L, et al. Association of short-term memory with a variant within DYX1C1 in developmental dyslexia. Genes Brain Behav. 2007;6 (7):640-6.
26. Wang Y, Paramasivam M, Thomas A, Bai J, Kaminen-Ahola N, Kere J, et al. DYX1C1 functions in neuronal miration in developing neocortex. Neuroscience 2006;143(2):515-22.
27. Burbridge TJ, Wang Y, Volz AJ, Peschansky VJ, Lisann L, Galaburda AM, et al. Postnatal analysis of the effect of embryonic knockdown and overexpression of candidate dyslexia susceptibility gene homolog Dcdc2 in the rat. Neuroscience 2008;152 (3):723-33.
28. Velayos-Baeza A, Toma C, Paracchini S, Monaco AP. The dyslexia-associated gene KIAA0319 encodes highly N-and Oglycosylated plasma membrane and secreted isoforms. Hum Mol Genet. 2008;17(6):859-71.
29. Rosen GD, Bai J, Yang Y, Fiondella CG, Threlkeld SW, LoTurco JJ, et al. Disruption of neuronal migration by RNAi of Dyx1c1 results in neocortical and hippocampal malformations. Cereb Cortex. 2007;17(11):2562-72.
30. Clark MG, Rosen GD, Tallal P, Fitch RH. Impaired processing of complex auditory stimuli in rats with induced cerebrocortical microgyria: an animal model of developmental language disabilities. J Cogn Neurosci. 2000;5:828-39.
31. McClure MM, Peiffer AM, Rosen GD, Fitch RH. Auditory processing deficits in rats with neonatal hypoxic-ischemic injury. Int J Dev Neurosci. 2005;23(4):351-62.
32. McClure MM, Threlkeld SW, Rosen GD, Fitch RH. Rapid auditory processing and leaning deficits in rats with P1 versus P7 neonatal hypoxic-ischemic injury. Behav Brain Res. 2006;172 (1):114-21.
33. Benasich A, Tallal P. Infant discrimination of rapid auditory cues predicts later language impairment. Behav Brain Re. 2002;136:31-49.
34. Noctor SC, Palmer SL, Hasling T, Juliano SL. Interference with the development of early generated neocortex results in disruption of radial glia and abnormal formation of neocortical layers. Cereb Cortex. 1999;9:121-36.
35. Garbossa D, Vercelli A. Experimentally-induced microencephaly: effects on cortical neurons. Brain Res Bull. 1998;60:329-38.
36. Sancini G, Franceschetti S, Battaglia G, Colacitti C, Di Luca M, Spreafico R, et al. Dysplastic neocortex and subcortical heterotopias in methylazoxymethanol-treated rats: and intracellular study of identified pyramidal neurons. Neurosci letters. 1998;246:181-5.
37. Bassanini S, Hallene K, Battaglia G, Finardi A, Santaguida S, Cipolla M, et al. Early cerebrovascular and parenchymal events following prenatal exposure to the putative neurotoxin methylazoxymethanol. Neurobiol Dis. 2007;26(2):481-95.
38. Fitch RH, Threlkeld SW, McClure MM, Peiffer AM. Use of a modified prepulse inhibition paradigm to assess complex auditory discrimination in rodents. Brain Res Bull. 2008;76 (1-2):1-7.
39. Peiffer AM, Friedman JT, Rosen GD, Fitch RH. Impaired gap detection in juvenile microgyric rats. Brain Res Dev Brain Res. 2004;152(2):83-91.
40. Friedman JT, Peiffer AM, Clark MG, Benasich AA, Fitch RH. Age and experience-related improvements in gap detection in the rat. Brain Res Dev Brain Res. 2004;152(2):93-8.
41. D'Hooge R, De Deyn PP. Application of the Morris water maze in the study of learning and memory. Brain Res Brain Res Rev. 2001;36:60-90.
42. Stavenezer A, Hyde L, Bimonte H, Armstrong C, Denenberg V. Differential learning strategies in spatial and nonspatial versions of the Morris water maze in the C57BL/6J inbred mouse strain. Behav Brain Res. 2002;133(2):261-70.
43. Gundersen H, Jensen E. The efficiency of systematic sampling in stereology and its prediction. J Microsc. 1987;147:229-63.
44. Rosen GD, Harry JD. Brain volume estimation from serial section measurements: a comparison of methodologies. J Neurosci Methods. 1990;35(2):115-24.
45. Threlkeld SW, Hill CA, Rosen GD, Fitch RH. Early acoustic discrimination experience ameliorates auditory processing deficits in male rats with cortical developmental disruption. Int J Dev Neurosci. 2009;27(4):321-8.
46. Amenta F, Cavallotti C, De Rossi M, Bossoni G, Carpi C. Effect of acetyl-L-carnitine treatment on some behavioral, histochemical and histological parameters of methylazoxymethanol microencephalic rats. Int J Tissue React. 1986;8(6):513-26.
47. Archer T, Hiltunen AJ, Jarbe T, Kamkar M, Luthman J, Sundstrom E, et al. Hyperactivity and instrumental learning deficits in methylazoxymethanol-treated rat offspring. Neurotoxicol and Teratol. 1988;10:341-7.
48. Lee MH, Rabe A. Premature decline in Morris water maze performance of aging micrencephalic rats. Neurotoxicol Teratol. 1992;14(6):383-92.
49. Mohommed AK, Jonsson G, Sundstrom E, Minor BG, Soderberg U, Archer T. Selective attention and place navigation in rats treated prenatally with methylazoxymethanol. Brain Res. 1986;395(2):145-55.
50. Dillon GM, Qu X, Marcus JN, Dodart JC. Excitotoxic lesions restricted to the dorsal Cal field of the hippocampus impair spatial memory and extinction learning in C57BL/6 mice. Neurobiol Learn Mem. 2008;90(2):426-33.
51. Papp G, Witter MP, Treves A. The CA3 network as a memory store for spatial representations. Learning Mem. 2007;14(11):732-44.
52. Farmer ME, Klein RM. The evidence for a temporal processing deficit linked to dyslexia: a review. Psychon Bull Rev. 1995;2:460-93.
53. Walker KM, Hall SE, Klein RM, Phillips DP. Development of perceptual correlates of reading performance. Brain Res. 2006;1126(1):126-41.
54. Tallal P. Improving language and literacy is a matter of time. Nat Rev Neurosci. 2004;5(9):721-8.
55. Benasich A, Choudhury N, Friedman J, Bealpe-Bonilla T, Chojnowska C, Gou Z. The infant as a prelinguistic model for language learning impairments: predicting from eventrelated potentials to behavior. Neuropsychologia 2006;44(3): 396-411.
56. Temple E, Poldrack R, Protopapas A, Nagarajan S, Salz T, Tallal P, et al. Disruption of the neural response to rapid acoustic stimuli in dyslexia: evidence from functional MRI. PNAS 2000;97 (25):13907-12.
57. Smith S. Genes, language development, and language disorders. Mental retardation and developmental disabilities. Ment Retard Dev Disabil Res Rev. 2007;13:96-105.
58. Wijsman EM, Peterson D, Leutenegger AL, Thomson JB, Goddard KA, Hsu L, et al. Segregation analysis of phenotypic components of learning disabilities. I. Nonword memory and digit span. Am J Hum Genet. 2000;67(3):631-46.
59. Raskind WH, Hsu L, Berninger VW, Thomason JB, Wijsman EM. Familial aggregation of dyslexia phenotypes. Behav Genet. 2000;30(5):385-96.
60. Barkovich AJ, Jackson DE, Boyer RS. Band heterotopias: a newly recognized neuronal migration anomaly. Radiology 1989;171 (2):455-8.
61. Moro F, Pisano T, Bernardina BD, Polli R, Murgia A, Zoccante L, et al. Periventricular heterotopia in fragile X syndrome. Neurology 2006;67(4):713-5.