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Sex, Age, and Cognitive Correlates of Asymmetries in Thickness of the Cortical Mantle Across the Life Span

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Sex, Age, and Cognitive Correlates of Asymmetries in Thickness of the Cortical Mantle Across the Life Span 6294 • The Journal of Neuroscience, April 30, 2014 • 34(18):6294–6302 Systems/Circuits Sex, Age, and Cognitive Correlates of Asymmetries in Thickness of the Cortical Mantle Across the Life Span Kerstin J. Plessen,1,2,3 Kenneth Hugdahl,4,5,6 Ravi Bansal,7,8 Xuejun Hao,7,8 and Bradley S. Peterson7,8 1Center for Child and Adolescent Mental Health, Capital Region Psychiatry, Denmark, 2Department of Clinical Medicine, Faculty of Health Sciences, University of Copenhagen, Denmark, 3Department of Clinical Medicine, Faculty of Medicine and Odontology, University of Bergen, Norway, 4Department of Biological and Medical Psychology, University of Bergen, Norway, 5Division of Psychiatry and the BMH-Centre, Haukeland University Hospital, Bergen, Norway, 6Department of Radiology, Haukeland University Hospital, Bergen, Norway, 7Center for Developmental Neuropsychiatry, Department of Psychiatry, Columbia University College of Physicians and Surgeons, New York, New York 10032, and 8New York State Psychiatric Institute, New York, New York 10032 We assessed the correlations of age, sex, and cognitive performance with measures of asymmetry in cortical thickness on high-resolution MRIs in 215 healthy human children and adults, 7–59 years of age. A left Ͼ right asymmetry in thickness of the cortical mantle was present throughout the entire lateral, dorsal, and mesial surfaces of the frontal lobe, extending into primary sensory, superior parietal, and anterior superior temporal cortices. A right Ͼ left asymmetry was present in the lateral, mesial, and dorsal surfaces of the posterior temporal, parietal, and occipital cortices, as well as in the entire inferior surface of the brain. An exaggerated left Ͼ right asymmetry was detected in females in anterior brain regions, and an exaggerated right Ͼ left asymmetry was detected in males in the orbitofrontal, inferior parietal, and inferior occipital cortices. Weaker moderating effects of sex were scattered along the mesial surface of the brain. Age significantly moderated asymmetry measures in the inferior sensorimotor, inferior parietal, posterior temporal, and inferior occipital cortices.Theageϫasymmetryinteractionderivedfromasteeperdeclineincorticalthicknesswithageintherighthemispherethaninthe left on the lateral surface, whereas it derived from a steeper decline with age in the left hemisphere than in the right on the mesial surface. Finally, measures of performance on working memory and vocabulary tasks improved with increasing magnitudes of normal asymme- tries in regions thought to support these cognitive capacities. Key words: asymmetry; cognitive performance; cortical thickness Introduction healthy adults. Studies using voxel-based morphometry have re- One of the most prominent anatomical features of the human ported a right Ͼ left asymmetry for gray matter extending from brain is its division into two distinct hemispheres, yet few prefrontal to temporoparietal regions (Watkins et al., 2001) and a studies have assessed morphological asymmetries and their left Ͼ right asymmetry in posterior brain regions (Good et al., development across the human life span (Hellige, 1990; Hug- 2001; Watkins et al., 2001; Takao et al., 2011). One MRI study dahl and Hirnstein, 2013). Important developmental pro- (Lyttelton et al., 2009) reported a leftward asymmetry in surface cesses are known to modify cortical architecture to thin the area for the planum temporale, Heschl’s gyrus, and supramar- cerebral cortex in support of more efficient information pro- ginal gyrus, and a rightward asymmetry in cortical thickness cessing and greater specialization of cognitive functions (Gog- along the mesial wall. tay et al., 2004; Tau and Peterson, 2010). Region of interest studies have reported larger occipital poles Differing imaging methodologies have yielded seemingly con- in the left and larger frontal poles in the right hemisphere, al- flicting findings in previous studies of anatomical asymmetries in though the other asymmetries in regional volumes have been less reliable (Raz et al., 1997, 2004). Deformation-based surface morphometry is another method Received Aug. 28, 2013; revised March 19, 2014; accepted March 25, 2014. Author contributions: K.J.P., K.H., and B.S.P. designed research; K.J.P., R.B., and B.S.P. performed research; R.B., to map patterns of asymmetries in the brain. One study in young X.H., and B.S.P. contributed unpublished reagents/analytic tools; K.J.P., R.B., X.H., and B.S.P. analyzed data; K.J.P., adults has revealed a significant leftward asymmetry in cortical K.H., R.B., and B.S.P. wrote the paper. thickness (CT) in precentral, middle frontal, anterior temporal, ThisworkwassupportedbytheResearchCouncilofNorway,theWesternNorwayHealthAuthority,andtheK.G. and superior parietal regions and a rightward asymmetry in pos- Jebsen Foundation grants to K.J.P. and K.H. and National Institute of Mental Health Grants MH36197, K02-74677, MH068318, and MH59139 to B.S.P. We thank Jun Liu, New York State Psychiatric Institute, New York and Morten teroinferior temporal and inferior frontal regions (Luders et al., Aagaard Petersen, Bispebjerg Hospital, Denmark for statistical expertise. 2006). A second study of CT in a large longitudinal study of The authors declare no competing financial interests. children and adolescents (Shaw et al., 2009) reported a promi- Correspondence should be addressed to Dr. Bradley S. Peterson, 1051 Riverside Drive, Unit 74, New York, NY, nent interaction of age with asymmetry, in which a left Ͼ right 10032. E-mail: [email protected]. Ͼ DOI:10.1523/JNEUROSCI.3692-13.2014 asymmetry in CT of the inferior frontal lobe and a right left Copyright © 2014 the authors 0270-6474/14/346294-09$15.00/0 asymmetry in thickness of posterior temporal and occipital re- Plessen et al. • Cortical Asymmetries Across the Life Span J. Neurosci., April 30, 2014 • 34(18):6294–6302 • 6295 participants and/or parents, as appropriate for age. We included 215 participants 7–59 years of age (mean 24.8 years, SD 14.2 years, median 21.7 years), 106 females (mean 25.6 years) and 109 males (mean 24.1 years). Ninety-seven participants were children (7–18 years of age) and 118 were adults (19–59 years of age). Handedness assignment was based on the hand the participants used for writing, which is known to correlate highly with more extensive hand-preference measures (Corey et al., 2001). In addition, we acquired a detailed assessment of handedness in the majority of participants (N ϭ 146) using the Edinburgh Handedness Inventory (Oldfield, 1971). A total of 200 par- ticipants were primarily right-handed, and 15 primarily left-handed. Cognitive measures. We explored the corre- lations of anatomical asymmetry with two cog- Figure1. Mapsofthemaineffectofasymmetry(Nϭ215).Thecolorbarindicatesthecolorcodingforpvaluesassociatedwith nitive measures in a subgroup of participants the main effect of asymmetry on CT. Warmer colors (red and yellow) represent positive correlations of cortical thickness with the to whom the tests were administered: (1) lefthemisphere,indicatingregionswherethecortexisthickerinthelefthemisphere;andcoolercolors(blueandpurple)represent working memory (N ϭ 130) was measured positive correlations of cortical thickness with the right hemisphere, indicating regions where the cortex is thicker in the right with Digit Span (DS; summing raw scores per- hemisphere. Correlations are visualized on the lateral, medial, superior, and inferior surfaces. These images show voxels that formed forward as an index of auditory atten- survived correction for multiple comparisons with GRF correction. Cortical regional boundaries indicate the following (Hao et al., tion and backward as an index of verbal 2011):Am,Amygdala;CG,cingulategyrus;Cu,cuneus;FuG,fusiformgyrus;GR,gyrusrectus;IFG,inferiorfrontalgyrus;IOG,inferior working memory capacities and converting to occipital gyrus; IPL, inferior parietal lobule; ITG, inferior temporal gyrus; LFOG, lateral fronto-orbital gyrus; LG, lingual gyrus; MFG, the age-corrected scaled scores) using identical middle frontal gyrus; MFOG, middle fronto-orbital gyrus; MOG, middle occipital gyrus; MTG, middle temporal gyrus; PreC, precu- procedures in the WAIS in adults or the “Num- neus; PoG, postcentral gyrus; PrG, precentral gyrus; SFG, superior frontal gyrus; SMG, supramarginal gyrus; SOG, superior occipital ber” subscale of the Children’s Memory Scale gyrus; SPG, superior parietal gyrus; STG, superior temporal gyrus. in children (both referred to here as the DS; and (2) verbal performance (N ϭ 100) was gions reversed following the transition from early childhood to measured with the Vocabulary test in either the WAIS in adults or WISC adolescence. in children, all within 4 weeks of the MRI scan. We selected these tests for We aimed to resolve some of the discrepant findings from correlation with our asymmetry measures because both DS (Henson et studies of children and adults by assessing the main effects of al., 2000) and Vocabulary (Warrington et al., 1986) are considered later- asymmetry on CT in a single, large sample of healthy children and alizing tasks, they have high reliability and age norms that yield compa- adult participants. We identified regions of anatomical asymmetry rable scaled scores across age groups (Canivez et al., 2005), and they were present across participants of all ages as well as interactions of acquired using identical procedures across the largest number of partic- ipants in our dataset. Unlike prior reports that have explored correlations asymmetry
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