An allometric analysis of sex and sex chromosome dosage effects on subcortical anatomy in humans

Journal of Neuroscience

Volumn 36, Issue 8, 2016, Pages 2438-2448

  Reardon, Paul Kirkpatrick ^a   Clasen, Liv ^a   Giedd, Jay N ^b   Blumenthal, Jonathan ^a   Lerch, Jason P ^c   Chakravarty, M Mallar ^d,e   Raznahan, Armin ^a  

^a NATIONAL INSTITUTE OF MENTAL HEALTH   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF TORONTO   (Canada)

^d DOUGLAS MENTAL HEALTH UNIVERSITY INSTITUTE   (Canada)

^e MCGILL UNIVERSITY   (Canada)

Author keywords

Allometry; Aneuploidy; Morphometry; Sex; Subcortex

Indexed keywords

ADOLESCENT; ARTICLE; BRAIN ALLOMETRY; BRAIN SIZE; CEPHALOMETRY; CHILD; CORPUS STRIATUM; FEMALE; GENDER; GENE EXPRESSION REGULATION; GLOBUS PALLIDUS; HUMAN; KARYOTYPE; MAJOR CLINICAL STUDY; MALE; NEUROIMAGING; NORMAL HUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PHENOTYPE; PRIORITY JOURNAL; SEX CHROMOSOME ABERRATION; SEX CHROMOSOME DOSAGE; SUBCORTEX; THALAMUS; VENTRAL STRIATUM; ADULT; ANATOMY AND HISTOLOGY; ANEUPLOIDY; BRAIN; COHORT ANALYSIS; CROSS-SECTIONAL STUDY; GENE DOSAGE; PHYSIOLOGY; PRESCHOOL CHILD; SEX CHROMOSOME; SEXUAL DEVELOPMENT; YOUNG ADULT;

ADOLESCENT; ADULT; ANEUPLOIDY; BRAIN; CHILD; CHILD, PRESCHOOL; COHORT STUDIES; CORPUS STRIATUM; CROSS-SECTIONAL STUDIES; FEMALE; GENE DOSAGE; GLOBUS PALLIDUS; HUMANS; MALE; SEX CHARACTERISTICS; SEX CHROMOSOMES; THALAMUS; YOUNG ADULT;

EID: 84959421386     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3195-15.2016     Document Type: Article

References (46)

1. Ad-Dab'bagh Y, Einarson D, Lyttelton O, Muehlboeck S, Mok K, Ivanov O, Vincent R, Lepage C, Lerch J, Fombonne E, Evans A (2006) The CIVET image-processing environment: a fully automated comprehensive pipeline for anatomical neuroimaging research. Proceedings of the 12th Annual Meeting of the Human Brain Mapping Organization. Florence, Italy.
2. Ahsan RL, Allom R, Gousias IS, Habib H, Turkheimer FE, Free S, Lemieux L, Myers R, Duncan JS, Brooks DJ, Koepp MJ, Hammers A (2007) Volumes, spatial extents and a probabilistic atlas of the human basal ganglia and thalamus. Neuroimage 38:261-270. CrossRef Medline
3. Bellott DW, Hughes JF, Skaletsky H, Brown LG, Pyntikova T, Cho TJ, Koutseva N, Zaghlul S, Graves T, Rock S, Kremitzki C, Fulton RS, Dugan S, Ding Y, Morton D, Khan Z, Lewis L, Buhay C, Wang Q, Watt J, et al. (2014) Mammalian Y chromosomes retain widely expressed dosagesensitive regulators. Nature 508:494-499. CrossRef Medline
4. Biegon A, Kim SW, Alexoff DL, Jayne M, Carter P, Hubbard B, King P, Logan J, Muench L, Pareto D, Schlyer D, Shea C, Telang F, Wang GJ, Xu Y, Fowler JS (2010) Unique distribution of aromatase in the human brain: in vivo studies with PET and [N-methyl-11C]vorozole. Synapse 64: 801-807. CrossRef Medline
5. Blumenthal JD, Baker EH, Lee NR, Wade B, Clasen LS, Lenroot RK, Giedd JN (2013) Brain morphological abnormalities in 49, XXXXY syndrome: a pediatric magnetic resonance imaging study. Neuroimage Clin 2: 197-203. CrossRef Medline
6. Bradshaw JL, Sheppard DM (2000) The neurodevelopmental frontostriatal disorders: evolutionary adaptiveness and anomalous lateralization. Brain Lang 73:297-320. CrossRef Medline
7. Brain Development Cooperative Group (2012) Total and regional brain volumes in a population-based normative sample from 4 to 18 years: the NIH MRI study of normal brain development. Cereb Cortex 22:1-12. CrossRef Medline
8. Bryant DM, Hoeft F, Lai S, Lackey J, Roeltgen D, Ross J, Reiss AL (2011) Neuroanatomical phenotype of Klinefelter syndrome in childhood: a voxel-based morphometry study. J Neurosci 31:6654-6660. CrossRef Medline
9. Bryant DM, Hoeft F, Lai S, Lackey J, Roeltgen D, Ross J, Reiss AL (2012) Sex chromosomes and the brain: a study of neuroanatomy in XYY syndrome: neuroanatomical variation in XYY syndrome. Dev Med Child Neurol 54:1149 -1156. CrossRef Medline
10. Cahill L (2006) Why sex matters for neuroscience. Nat Rev Neurosci 7: 477-484. CrossRef Medline
11. Chakravarty MM, Bertrand G, Hodge CP, Sadikot AF, Collins DL (2006) The creation of a brain atlas for image guided neurosurgery using serial histological data. Neuroimage 30:359 -376. CrossRef Medline
12. Chakravarty MM, Steadman P, van Eede MC, Calcott RD, Gu V, Shaw P, Raznahan A, Collins DL, Lerch JP (2013) Performing label-fusionbased segmentation using multiple automatically generated templates: MAGeT brain: label fusion segmentation using automatically generated templates. Hum Brain Mapp 34:2635-2654. CrossRef Medline
13. Choi EY, Yeo BT, Buckner RL (2012) The organization of the human striatum estimated by intrinsic functional connectivity. J Neurophysiol 108: 2242-2263. CrossRef Medline
14. Corre C, Friedel M, Vousden DA, Metcalf A, Spring S, Qiu LR, Lerch JP, Palmert MR (2014) Separate effects of sex hormones and sex chromosomes on brain structure and function revealed by high-resolution magnetic resonance imaging and spatial navigation assessment of the Four Core Genotype mouse model. Brain Struct Funct. Advance online publication. CrossRef Medline
15. Draganski B, Kherif F, Klöppel S, Cook PA, Alexander DC, Parker GJ, Deichmann R, Ashburner J, Frackowiak RS (2008) Evidence for segregated and integrative connectivity patterns in the human basal ganglia. J Neurosci 28:7143-7152. CrossRef Medline
16. Duvernoy HM (1999) The human brain. Vienna: Springer.
17. Escorial S, Román FJ, Martínez K, Burgaleta M, Karama S, Colom R (2015) Sex differences in neocortical structure and cognitive performance: a surface-based morphometry study. Neuroimage 104:355-365. CrossRef Medline
18. Finlay BL, Darlington RB (1995) Linked regularities in the development and evolution of mammalian brains. Science 268:1578 -1584. CrossRef Medline
19. Genovese CR, Lazar NA, Nichols T (2002) Thresholding of statistical maps in functional neuroimaging using the false discovery rate. Neuroimage 15:870-878. CrossRef Medline
20. Giedd JN, Raznahan A, Alexander-Bloch A, Schmitt E, Gogtay N, Rapoport JL (2015) Child psychiatry branch of the national institute of mental health longitudinal structural magnetic resonance imaging study of human brain development. Neuropsychopharmacology 40:43- 49. CrossRef Medline
21. Grahn JA, Parkinson JA, Owen AM (2008) The cognitive functions of the caudate nucleus. Prog Neurobiol 86:141-155. CrossRef Medline
22. Greene DJ, Laumann TO, Dubis JW, Ihnen SK, Neta M, Power JD, Pruett JR Jr, Black KJ, Schlaggar BL (2014) Developmental changes in the organization of functional connections between the basal ganglia and cerebral cortex. J Neurosci 34:5842-5854. CrossRef Medline
23. Hill J, Inder T, Neil J, Dierker D, Harwell J, Van Essen D (2010) Similar patterns of cortical expansion during human development and evolution. Proc Natl Acad Sci U S A 107:13135-13140. CrossRef Medline
24. Hong DS, Reiss AL (2014) Cognitive and neurological aspects of sex chromosome aneuploidies. Lancet Neurol 13:306 -318. CrossRef Medline
25. Hong DS, Hoeft F, Marzelli MJ, Lepage JF, Roeltgen D, Ross J, Reiss AL (2014) Influence of the X-chromosome on neuroanatomy: evidence from turner and Klinefelter syndromes. J Neurosci 34:3509 -3516. CrossRef Medline
26. Hughes JF, Rozen S (2012) Genomics and genetics of human and primate y chromosomes. Annu Rev Genomics Hum Genet 13:83-108. CrossRef Medline
27. Johnston MV (2001) Excitotoxicity in neonatal hypoxia. Ment Retard Dev Disabil Res Rev 7:229 -234. CrossRef Medline
28. Kim DJ, Park B, Park HJ (2013) Functional connectivity-based identification of subdivisions of the basal ganglia and thalamus using multilevel independent component analysis of resting state fMRI. Hum Brain Mapp 34:1371-1385. CrossRef Medline
29. Lee NR, Wallace GL, Adeyemi EI, Lopez KC, Blumenthal JD, Clasen LS, Giedd JN (2012) Dosage effects of X and Y chromosomes on language and social functioning in children with supernumerary sex chromosome aneuploidies: implications for idiopathic language impairment and autism spectrum disorders. J Child Psychol Psychiatry 53:1072-1081. CrossRef Medline
30. Lentini E, Kasahara M, Arver S, Savic I (2013) Sex differences in the human brain and the impact of sex chromosomes and sex hormones. Cereb Cortex 23:2322-2336. CrossRef Medline
31. Meltzer H, Gatward R, Goodman R, Ford T (2003) The mental health of children and adolescents in Great Britain: summary report. Int Rev Psychiatry 15:185-187. CrossRef Medline
32. Ostby Y, Tamnes CK, Fjell AM, Westlye LT, Due-Tønnessen P, Walhovd KB (2009) Heterogeneity in subcortical brain development: a structural magnetic resonance imaging study of brain maturation from 8 to 30 years. J Neurosci 29:11772-11782. CrossRef Medline
33. Otto SP, Pannell JR, Peichel CL, Ashman TL, Charlesworth D, Chippindale AK, Delph LF, Guerrero RF, Scarpino SV, McAllister BF (2011) About PAR: the distinct evolutionary dynamics of the pseudoautosomal region. Trends Genet 27:358 -367. CrossRef Medline
34. Raznahan A, Lee Y, Stidd R, Long R, Greenstein D, Clasen L, Addington A, Gogtay N, Rapoport JL, Giedd JN (2010) Longitudinally mapping the influence of sex and androgen signaling on the dynamics of human cortical maturation in adolescence. Proc Natl Acad Sci U S A 107: 16988 -16993. CrossRef Medline
35. Raznahan A, Shaw PW, Lerch JP, Clasen LS, Greenstein D, Berman R, Pipitone J, Chakravarty MM, Giedd JN (2014) Longitudinal fourdimensional mapping of subcortical anatomy in human development. Proc Natl Acad Sci U S A 111:1592-1597. CrossRef Medline
36. Raznahan A, Lue Y, Probst F, Greenstein D, Giedd J, Wang C, Lerch J, Swerdloff R (2015) Triangulating the sexually dimorphic brain through highresolution neuroimaging of murine sex chromosome aneuploidies. Brain Struct Funct 220:3581-3593. CrossRef Medline
37. Raznahan A, Lee NR, Greenstein D, Wallace GL, Blumenthal JD, Clasen LS, Giedd JN (2016) Globally divergent but locally convergent X- and Y-chromosome influences on cortical development. Cereb Cortex 26: 70-79. CrossRef Medline
38. Rijpkema M, Everaerd D, van der Pol C, Franke B, Tendolkar I, Fernández G (2012) Normal sexual dimorphism in the human basal ganglia. Hum Brain Mapp 33:1246 -1252. CrossRef Medline
39. Roalf DR, Gur RE, Ruparel K, Calkins ME, Satterthwaite TD, Bilker WB, Hakonarson H, Harris LJ, Gur RC (2014) Within-individual variability in neurocognitive performance: age- and sex-related differences in children and youths from ages 8 to 21. Neuropsychology 28:506 -518. CrossRef Medline
40. Rutter M, Caspi A, Moffitt TE (2003) Using sex differences in psychopathology to study causal mechanisms: unifying issues and research strategies [Review]. J Child Psychol Psychiatry 44:1092-1115. CrossRef Medline
41. Sheltzer JM, Torres EM, Dunham MJ, Amon A (2012) Transcriptional consequences of aneuploidy. Proc Natl Acad Sci U S A 109:12644 -12649. CrossRef Medline
42. Sowell ER, Trauner DA, Gamst A, Jernigan TL (2002) Development of cortical and subcortical brain structures in childhood and adolescence: a structural MRI study. Dev Med Child Neurol 44:4 -16. CrossRef Medline
43. Tartaglia N, Davis S, Hench A, Nimishakavi S, Beauregard R, Reynolds A, Fenton L, Albrecht L, Ross J, Visootsak J, Hansen R, Hagerman R (2008) A new look at XXYY syndrome: medical and psychological features. Am J Med Genet A 146A:1509 -1522. CrossRef Medline
44. Toro R, Chupin M, Garnero L, Leonard G, Perron M, Pike B, Pitiot A, Richer L, Veillette S, Pausova Z, Paus T (2009) Brain volumes and Val66Met polymorphism of the BDNF gene: local or global effects? Brain Struct Funct 213:501-509. CrossRef Medline
45. Voorn P, Vanderschuren LJ, Groenewegen HJ, Robbins TW, Pennartz CM (2004) Putting a spin on the dorsal-ventral divide of the striatum. Trends Neurosci 27:468-474. CrossRef Medline
46. Wierenga L, Langen M, Ambrosino S, van Dijk S, Oranje B, Durston S (2014) Typical development of basal ganglia, hippocampus, amygdala and cerebellum from age 7 to 24. Neuroimage 96:67-72. CrossRef Medline