High resolution whole brain imaging of anatomical variation in XO, XX, and XY mice

NeuroImage

Volumn 83, Issue , 2013, Pages 962-968

  Raznahan, Armin ^a   Probst, Frank ^b   Palmert, Mark R ^c,d,e   Giedd, Jay N ^a   Lerch, Jason P ^c,e  

^a NATIONAL INSTITUTE OF MENTAL HEALTH   (United States)

^b BAYLOR COLLEGE OF MEDICINE   (United States)

^c HOSPITAL FOR SICK CHILDREN   (Canada)

^d UNIVERSITY OF TORONTO   (Canada)

^e UNIVERSITY OF TORONTO   (Canada)

Author keywords

Aneuploidy; Brain development; Sex chromosomes; Sex differences

Indexed keywords

SEX HORMONE;

ANATOMICAL VARIATION; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN DEVELOPMENT; BRAIN DISEASE; BRAIN RADIOGRAPHY; CHROMOSOME DISORDER; CHROMOSOME MOSAICISM; COGNITION; CONTROLLED STUDY; DEVELOPMENTAL DISORDER; EMOTION; FEMALE; GENE; GENETIC CONSERVATION; GONADAL DYSGENESIS; HORMONE ACTION; KARYOTYPING; MALE; MAMMAL; MEDIAL AMYGDALA; MONOSOMY X; MOUSE; NEUROANATOMY; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; NUCLEAR MAGNETIC RESONANCE SCANNER; OVARY DISEASE; PARIETAL CORTEX; PERIAQUEDUCTAL GRAY MATTER; PRIORITY JOURNAL; SEX DIFFERENCE; STRIA TERMINALIS; STRIATE CORTEX; X CHROMOSOME; X CHROMOSOME LINKED GENE; Y CHROMOSOME;

ANEUPLOIDY; BRAIN DEVELOPMENT; SEX CHROMOSOMES; SEX DIFFERENCES;

ANIMALS; BRAIN; DISEASE MODELS, ANIMAL; FEMALE; IMAGE PROCESSING, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; MALE; MICE; MICE, MUTANT STRAINS; SEX CHARACTERISTICS; TURNER SYNDROME;

EID: 84886380930     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2013.07.052     Document Type: Article

References (47)

1. Arias-Vasquez A., Altink M.E., Rommelse N.N., Slaats-Willemse D.I., Buschgens C.J., Fliers E.A., Faraone S.V., Sergeant J.A., Oosterlaan J., Franke B., Buitelaar J.K. CDH13 is associated with working memory performance in attention deficit/hyperactivity disorder. Genes Brain Behav. 2011, 10:844-851.
2. Arnold A.P. Sex chromosomes and brain gender. Nat. Rev. Neurosci. 2004, 5:701-708.
3. Avants B.B., Epstein C.L., Grossman M., Gee J.C. Symmetric diffeomorphic image registration with cross-correlation: evaluating automated labeling of elderly and neurodegenerative brain. Med. Image Anal. 2008, 12:26-41.
4. Cahill L.S., Laliberte C.L., Ellegood J., Spring S., Gleave J.A., Eede M.C., Lerch J.P., Henkelman R.M. Preparation of fixed mouse brains for MRI. NeuroImage 2012, 60:933-939.
5. Cocquet J., Ellis P.J., Mahadevaiah S.K., Affara N.A., Vaiman D., Burgoyne P.S. A genetic basis for a postmeiotic x versus y chromosome intragenomic conflict in the mouse. PLoS Genet. 2012, 8:e1002900.
6. Davies W., Isles A., Smith R., Karunadasa D., Burrmann D., Humby T., Ojarikre O., Biggin C., Skuse D., Burgoyne P., Wilkinson L. Xlr3b is a new imprinted candidate for X-linked parent-of-origin effects on cognitive function in mice. Nat. Genet. 2005, 37:625-629.
7. Deckers J.F.M., van der Kroon P.H.W., Douglas L. Some characteristics of the X0 mouse (Mus musculus L.) II. Reproduction: fertility and gametic segregation. Genetica 1981, 57:3-11.
8. Dumont E.C. What is the bed nucleus of the stria terminalis?. Prog. Neuropsychopharmacol. Biol. Psychiatry 2009, 33:1289-1290.
9. Duvarci S., Bauer E.P., Pare D. The bed nucleus of the stria terminalis mediates inter-individual variations in anxiety and fear. J. Neurosci. 2009, 29:10357-10361.
10. Erickson G.F., Magoffin D.A., Dyer C.A., Hofeditz C. The ovarian androgen producing cells: a review of structure/function relationships. Endocr. Rev. 1985, 6:371-399.
11. Garagorri J.M., Rodriguez G., Lario-Elboj A.J., Olivares J.L., Lario-Munoz A., Orden I. Reference levels for 17-hydroxyprogesterone, 11-desoxycortisol, cortisol, testosterone, dehydroepiandrosterone sulfate and androstenedione in infants from birth to six months of age. Eur. J. Pediatr. 2008, 167:647-653.
12. Garces C., de Oya I., Lopez-Simon L., Cano B., Schoppen S., Gil A., de Oya M. Hormone levels in 12- to 15-year-old boys and girls in Spain and their relationship with anthropometric variables. Clin. Biochem. 2008, 41:621-624.
13. Genovese C.R., Lazar N.A., Nichols T. Thresholding of statistical maps in functional neuroimaging using the false discovery rate. NeuroImage 2002, 15:870-878.
14. Giedd J.N., Raznahan A., Mills K., Lenroot R.K. Review: magnetic resonance imaging of male/female differences in human adolescent brain anatomy. Biol. Sex Differ. 2012, 3:19.
15. Gregg C., Zhang J., Butler J.E., Haig D., Dulac C. Sex-specific parent-of-origin allelic expression in the mouse brain. Science 2010, 329:682-685.
16. Gregg C., Zhang J., Weissbourd B., Luo S., Schroth G.P., Haig D., Dulac C. High-resolution analysis of parent-of-origin allelic expression in the mouse brain. Science 2010, 329:643-648.
17. Hughes E.J., Bond J., Svrckova P., Makropoulos A., Ball G., Sharp D.J., Edwards A.D., Hajnal J.V., Counsell S.J. Regional changes in thalamic shape and volume with increasing age. NeuroImage 2012, 63:1134-1142.
18. Isles A.R., Davies W., Burrmann D., Burgoyne P.S., Wilkinson L.S. Effects on fear reactivity in XO mice are due to haploinsufficiency of a non-PAR X gene: implications for emotional function in Turner's syndrome. Hum. Mol. Genet. 2004, 13:1849-1855.
19. Kesler S.R. Turner syndrome. Child Adolesc. Psychiatr. Clin. N. Am. 2007, 16:709-722.
20. Lenz K.M., Nugent B.M., McCarthy M.M. Sexual differentiation of the rodent brain: dogma and beyond. Front. Neurosci. 2012, 6:26.
21. Lepage J.F., Mazaika P.K., Hong D.S., Raman M., Reiss A.L. Cortical brain morphology in young, estrogen-naive, and adolescent, estrogen-treated girls with Turner syndrome. Cereb. Cortex 2012.
22. Lerch J.P., Carroll J.B., Dorr A., Spring S., Evans A.C., Hayden M.R., Sled J.G., Henkelman R.M. Cortical thickness measured from MRI in the YAC128 mouse model of Huntington's disease. NeuroImage 2008, 41:243-251.
23. Lerch J.P., Sled J.G., Henkelman R.M. MRI phenotyping of genetically altered mice. Methods Mol. Biol. 2011, 711:349-361.
24. Linnman C., Moulton E.A., Barmettler G., Becerra L., Borsook D. Neuroimaging of the periaqueductal gray: state of the field. NeuroImage 2012, 60:505-522.
25. Lopes A.M., Burgoyne P.S., Ojarikre A., Bauer J., Sargent C.A., Amorim A., Affara N.A. Transcriptional changes in response to X chromosome dosage in the mouse: implications for X inactivation and the molecular basis of Turner syndrome. BMC Genomics 2010, 11:82.
26. Lyon M.F. Gene action in the X-chromosome of the mouse (Mus musculus L.). Nature 1961, 190:372-373.
27. Marzelli M.J., Hoeft F., Hong D.S., Reiss A.L. Neuroanatomical spatial patterns in Turner syndrome. NeuroImage 2011, 55:439-447.
28. McCarthy M.M., Arnold A.P., Ball G.F., Blaustein J.D., De Vries G.J. Sex differences in the brain: the not so inconvenient truth. J. Neurosci. 2012, 32:2241-2247.
29. Morris J.A., Jordan C.L., Breedlove S.M. Sexual differentiation of the vertebrate nervous system. Nat. Neurosci. 2004, 7:1034-1039.
30. Otto S.P., Pannell J.R., Peichel C.L., Ashman T.L., Charlesworth D., Chippindale A.K., Delph L.F., Guerrero R.F., Scarpino S.V., McAllister B.F. About PAR: the distinct evolutionary dynamics of the pseudoautosomal region. Trends Genet. 2011, 27:358-367.
31. Palaszynski K.M., Smith D.L., Kamrava S., Burgoyne P.S., Arnold A.P., Voskuhl R.R. A yin-yang effect between sex chromosome complement and sex hormones on the immune response. Endocrinology 2005, 146:3280-3285.
32. Phoenix C.H., Goy R.W., Gerall A.A., Young W.C. Organizing action of prenatally administered testosterone propionate on the tissues mediating mating behavior in the female guinea pig. Endocrinology 1959, 65:369-382.
33. Probst F.J., Cooper M.L., Cheung S.W., Justice M.J. Genotype, phenotype, and karyotype correlation in the XO mouse model of Turner syndrome. J. Hered. 2008, 99:512-517.
34. R Core Team R: A language and environment for statistical computing 2013, R Foundation for Statistical Computing, Vienna, Austria, (ISBN 3-900051-07-0, URL:http://www.R-project.org/).
35. Raznahan A., Cutter W., Lalonde F., Robertson D., Daly E., Conway G.S., Skuse D.H., Ross J., Lerch J.P., Giedd J.N., Murphy D.D. Cortical anatomy in human X monosomy. NeuroImage 2010, 49:2915-2923.
36. Shah N.M., Pisapia D.J., Maniatis S., Mendelsohn M.M., Nemes A., Axel R. Visualizing sexual dimorphism in the brain. Neuron 2004, 43:313-319.
37. Silveira M.C., Sandner G., Graeff F.G. Induction of Fos immunoreactivity in the brain by exposure to the elevated plus-maze. Behav. Brain Res. 1993, 56:115-118.
38. Skuse D.H., James R.S., Bishop D.V., Coppin B., Dalton P., Aamodt-Leeper G., Bacarese-Hamilton M., Creswell C., McGurk R., Jacobs P.A. Evidence from Turner's syndrome of an imprinted X-linked locus affecting cognitive function. Nature 1997, 387:705-708.
39. Sybert V.P., McCauley E. Turner's syndrome. N. Engl. J. Med. 2004, 351:1227-1238.
40. Trolle C., Hjerrild B., Cleemann L., Mortensen K.H., Gravholt C.H. Sex hormone replacement in Turner syndrome. Endocrine 2012, 41:200-219.
41. Wallace G.L., Robustelli B., Dankner N., Kenworthy L., Giedd J.N., Martin A. Increased gyrification, but comparable surface area in adolescents with autism spectrum disorders. Brain 2013, 136:1956-1967.
42. Wickham H. ggplot2: elegant graphics for data analysis 2009, Springer, New York.
43. Wolff D.J., Van Dyke D.L., Powell C.M., Working Group of the, A.L.Q.A.C. Laboratory guideline for Turner syndrome. Genet. Med. 2010, 12:52-55.
44. Xu J., Burgoyne P.S., Arnold A.P. Sex differences in sex chromosome gene expression in mouse brain. Hum. Mol. Genet. 2002, 11:1409-1419.
45. Yamagata B., Barnea-Goraly N., Marzelli M.J., Park Y., Hong D.S., Mimura M., Reiss A.L. White matter aberrations in prepubertal estrogen-naive girls with monosomic Turner syndrome. Cereb. Cortex 2012, 22:2761-2768.
46. Yang F., Babak T., Shendure J., Disteche C.M. Global survey of escape from X inactivation by RNA-sequencing in mouse. Genome Res. 2010, 20:614-622.
47. Zuloaga D.G., Puts D.A., Jordan C.L., Breedlove S.M. The role of androgen receptors in the masculinization of brain and behavior: what we've learned from the testicular feminization mutation. Horm. Behav. 2008, 53:613-626.