Research progress on genetic effects of the asymmetry of human brain structure revealed by magnetic resonance imaging_Journal of Biomedical Engineering

Authors：

WEI Long ¹ , YANG Yifeng ² , HU Ying ² ,  NIE Shengdong ²

1. School of Computer Science and Technology, Shandong Jianzhu University, Jinan 250101, P.R.China;
2. Institute of Medical Imaging Engineering, University of Shanghai for Science and Technology, Shanghai 200093, P.R.China;

Corresponding author：

Keywords：

magnetic resonance imaging; asymmetry; heritability; genetic correlation; twin study

DOI：

10.7507/1001-5515.201912035

Video：

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Hemispheric asymmetry is a fundamental organizing principle of the human brain. Answering the genetic effects of the asymmetry is a prerequisite for elucidating developmental mechanisms of brain asymmetries. Multi-modal magnetic resonance imaging (MRI) has provided an important tool for comprehensively interpreting human brain asymmetry and its genetic mechanism. By combining MRI data, individual differences in brain structural asymmetry have been investigated with quantitative genetic brain mapping using gene-heritability. Twins provide a useful natural model for studying the effects of genetics and environment on the brain. Studies based on MRI have found that the asymmetry of human brain structure has a genetic basis. From the perspective of quantitative genetic analysis, this article reviews recent findings on the genetic effects of asymmetry and genetic covariance between hemispheres from three aspects: the asymmetry of heritability, the heritability of asymmetry and the genetic correlation. At last, the article shows the limitations and future research directions in this field. The purpose of this systematic review is to quickly guide researchers to understand the origins and genetic mechanism of interhemispheric differences, and provide a genetic basis for further understanding and exploring individual differences in laterized cognitive behavior.

Citation： WEI Long, YANG Yifeng, HU Ying, NIE Shengdong. Research progress on genetic effects of the asymmetry of human brain structure revealed by magnetic resonance imaging. Journal of Biomedical Engineering, 2020, 37(6): 1089-1094. doi: 10.7507/1001-5515.201912035 Copy

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8.	Xiang L A-O, Crow T, Roberts N. Automatic analysis of cross-sectional cerebral asymmetry on 3D in vivo MRI scans of human and chimpanzee. J Neurosci Res, 2019, 97(6): 673-682.
9.	Toga A W, Thompson P M. Mapping brain asymmetry. Nat Rev Neurosci, 2003, 4(1): 37-48.
10.	Güntürkün O, Ocklenburg S. Ontogenesis of lateralization. Neuron, 2017, 94(2): 249-263.
11.	Wiberg A, Ng M, Al Omran Y, et al. Handedness, language areas and neuropsychiatric diseases: insights from brain imaging and genetics. Brain, 2019, 142(10): 2938-2947.
12.	de Kovel C G F, Lisgo S, Karlebach G, et al. Left-Right asymmetry of maturation rates in human embryonic neural development. Biol Psychiatry, 2017, 82(3): 204-212.
13.	de Kovel C G F, Lisgo S N, Fisher S E, et al. Subtle left-right asymmetry of gene expression profiles in embryonic and foetal human brains. Sci Rep, 2018, 8(1): 12606.
14.	Ocklenburg S, Schmitz J, Moinfar Z, et al. Epigenetic regulation of lateralized fetal spinal gene expression underlies hemispheric asymmetries. eLife, 2017: e22784.
15.	Muntané G, Santpere G, Verendeev A, et al. Interhemispheric gene expression differences in the cerebral cortex of humans and macaque monkeys. Brain Struct Funct, 2017, 222(7): 3241-3254.
16.	王雪雯, 傅一笑, 唐金香, 等. 双生子研究方法在精神障碍研究中的应用与进展. 四川精神卫生, 2019, 32(2): 181-184.
17.	Blokland G A, de Zubicaray G I, Mcmahon K L, et al. Genetic and environmental influences on neuroimaging phenotypes: a meta-analytical perspective on twin imaging studies. Twin Res Hum Genet, 2012, 15(3): 351-371.
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19.	Thompson P M, Ge T, Glahn D C, et al. Genetics of the connectome. Neuroimage, 2013, 80: 475-488.
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21.	马兴顺, 贺越, 李晓, 等. 遗传和环境因素对青少年脑灰质容积和皮层厚度影响的双生子研究. 中国神经精神疾病杂志, 2018, 44(6): 354-359.
22.	Gao W, Grewen K, Knickmeyer R C, et al. A review on neuroimaging studies of genetic and environmental influences on early brain development. Neuroimage, 2019, 185: 802-812.
23.	Ge T, Chen C Y, Vettermann R, et al. The shared genetic basis of human fluid intelligence and brain morphology. Cereb Cortex, 2018, 29(8): 3471-3481.
24.	Elliott L T, Sharp K, Alfaro-Almagro F, et al. Genome-wide association studies of brain imaging phenotypes in UK Biobank. Nature, 2018, 562(7726): 210-216.
25.	Eyler L T, Vuoksimaa E, Panizzon M S, et al. Conceptual and data-based investigation of genetic influences and brain asymmetry: a twin study of multiple structural phenotypes. J Cogn Neurosci, 2014, 26(5): 1100-1117.
26.	Liu S, Li A, Zhu M, et al. Genetic influences on cortical myelination in the human brain. Genes Brain Behav, 2019, 18(4): e12537.
27.	Wen W, Thalamuthu A, Mather K A, et al. Distinct genetic influences on cortical and subcortical brain structures. Scientific Reports, 2016, 6: 32760.
28.	Zhao B, Ibrahim J G, Li Y, et al. Heritability of regional brain volumes in large-scale neuroimaging and genetic studies. Cereb Cortex, 2019, 29(7): 2904-2914.
29.	Geschwind D H, Miller B L, Decarli C, et al. Heritability of lobar brain volumes in twins supports genetic models of cerebral laterality and handedness. Proc Natl Acad Sci U S A, 2002, 99(5): 3176-3181.
30.	Yoon U, Fahim C, Perusse D, et al. Lateralized genetic and environmental influences on human brain morphology of 8-year-old twins. Neuroimage, 2010, 53(3): 1117-1125.
31.	Yoon U, Perusse D, Evans A C. Mapping genetic and environmental influences on cortical surface area of pediatric twins. Neuroscience, 2012, 220: 169-178.
32.	van der Lee S J, Roshchupkin G V, Adams H H, et al. Gray matter heritability in family-based and population-based studies using voxel-based morphometry. Hum Brain Mapp, 2017, 38(5): 2408-2423.
33.	Yoon U, Perusse D, Lee J M, et al. Genetic and environmental influences on structural variability of the brain in pediatric twin: deformation based morphometry. Neurosci Lett, 2011, 493(1/2): 8-13.
34.	Lebel C, Deoni S. The development of brain white matter microstructure. Neuroimage, 2018, 182(1): 207-218.
35.	Guadalupe T, Mathias S R, Vanerp T, et al. Human subcortical brain asymmetries in 15, 847 people worldwide reveal effects of age and sex. Brain Imaging Behav, 2017, 11(5): 1497-1514.
36.	Parma V, Brasselet R, Zoia S, et al. The origin of human handedness and its role in pre-birth motor control. Sci Rep, 2017, 7(1): 16804.
37.	Young G. Causality and Development. Berlin, Germany: Springer, Cham, 2019.
38.	Barzilay E, Bar-Yosef O, Dorembus S, et al. Fetal brain anomalies associated with ventriculomegaly or asymmetry: an MRI-based study. AJNR Am J Neuroradiol, 2017, 38(2): 371-375.
39.	Andescavage N N, Du Plessis A, Mccarter R, et al. Complex trajectories of brain development in the healthy human fetus. Cereb Cortex, 2017, 27(11): 5274-5283.
40.	Jahanshad N, Lee A D, Barysheva M, et al. Genetic influences on brain asymmetry: a DTI study of 374 twins and siblings. Neuroimage, 2010, 52(2): 455-469.
41.	Budisavljevic S, Dell'acqua F, Rijsdijk F V, et al. Age-related differences and heritability of the perisylvian language networks. J Neurosci, 2015, 35(37): 12625-12634.
42.	Zhong S, He Y, Shu H, et al. Developmental changes in topological asymmetry between hemispheric brain white matter networks from adolescence to young adulthood. Cereb Cortex, 2017, 27(4): 2560-2570.
43.	Brainstorm C, Anttila V, Bulik-Sullivan B, et al. Analysis of shared heritability in common disorders of the brain. Science, 2018, 360(6395): eaap8757.
44.	Lee S J, Zhang J, Neale M C, et al. Quantitative tract-based white matter heritability in 1- and 2-year-old twins. Hum Brain Mapp, 2019, 40(4): 1164-1173.
45.	Kennedy J T, Astafiev S V, Golosheykin S, et al. Shared genetic influences on adolescent body mass index and brain structure: a voxel-based morphometry study in twins. Neuroimage, 2019, 199: 261-272.
46.	Teeuw J, Brouwer R M, Koenis M, et al. Genetic influences on the development of cerebral cortical thickness during childhood and adolescence in a Dutch longitudinal twin sample: the brainscale study. Cereb Cortex, 2019, 29(3): 978-993.

1. Corballis M C, Häberling I S. The many sides of hemispheric asymmetry: a selective review and outlook. J Int Neuropsychol Soc, 2017, 23(9-10): 710-718.
2. Ocklenburg S, Güntürkün O. The lateralized brain - the neuroscience and evolution of hemispheric asymmetries. London, UK: Academic Press, 2018.
3. Hirnstein M, Hugdahl K, Hausmann M. Cognitive sex differences and hemispheric asymmetry: a critical review of 40 years of research. Laterality, 2019, 24(2): 204-252.
4. 尚韡, 王乐, 段凯凯, 等. Broca区的脑半球偏侧化静息态功能连接研究. 中西医结合心脑血管病杂志, 2017, 15(8): 917-923.
5. Corballis M C. The evolution of lateralized brain circuits. Front Psychol, 2017, 8: 1021.
6. Kong X Z, Mathias S R, Guadalupe T, et al. Mapping cortical brain asymmetry in 17, 141 healthy individuals worldwide via the ENIGMA Consortium. Proc Natl Acad Sci U S A, 2018, 115(22): E5154-E5163.
7. Calabria M, Costa A, Green D W, et al. Neural basis of bilingual language control. Ann N Y Acad Sci, 2018, 1426(1): 221-235.
8. Xiang L A-O, Crow T, Roberts N. Automatic analysis of cross-sectional cerebral asymmetry on 3D in vivo MRI scans of human and chimpanzee. J Neurosci Res, 2019, 97(6): 673-682.
9. Toga A W, Thompson P M. Mapping brain asymmetry. Nat Rev Neurosci, 2003, 4(1): 37-48.
10. Güntürkün O, Ocklenburg S. Ontogenesis of lateralization. Neuron, 2017, 94(2): 249-263.
11. Wiberg A, Ng M, Al Omran Y, et al. Handedness, language areas and neuropsychiatric diseases: insights from brain imaging and genetics. Brain, 2019, 142(10): 2938-2947.
12. de Kovel C G F, Lisgo S, Karlebach G, et al. Left-Right asymmetry of maturation rates in human embryonic neural development. Biol Psychiatry, 2017, 82(3): 204-212.
13. de Kovel C G F, Lisgo S N, Fisher S E, et al. Subtle left-right asymmetry of gene expression profiles in embryonic and foetal human brains. Sci Rep, 2018, 8(1): 12606.
14. Ocklenburg S, Schmitz J, Moinfar Z, et al. Epigenetic regulation of lateralized fetal spinal gene expression underlies hemispheric asymmetries. eLife, 2017: e22784.
15. Muntané G, Santpere G, Verendeev A, et al. Interhemispheric gene expression differences in the cerebral cortex of humans and macaque monkeys. Brain Struct Funct, 2017, 222(7): 3241-3254.
16. 王雪雯, 傅一笑, 唐金香, 等. 双生子研究方法在精神障碍研究中的应用与进展. 四川精神卫生, 2019, 32(2): 181-184.
17. Blokland G A, de Zubicaray G I, Mcmahon K L, et al. Genetic and environmental influences on neuroimaging phenotypes: a meta-analytical perspective on twin imaging studies. Twin Res Hum Genet, 2012, 15(3): 351-371.
18. Vuoksimaa E, Panizzon M S, Hagler D J, et al. Heritability of white matter microstructure in late middle age: a twin study of tract-based fractional anisotropy and absolute diffusivity indices. Hum Brain Mapp, 2017, 38(4): 2026-2036.
19. Thompson P M, Ge T, Glahn D C, et al. Genetics of the connectome. Neuroimage, 2013, 80: 475-488.
20. Brouwer R O, Panizzon M S, Glahn D O, et al. Genetic influences on individual differences in longitudinal changes in global and subcortical brain volumes: results of the ENIGMA plasticity working group. Hum Brain Mapp, 2017, 38(9): 4444-4458.
21. 马兴顺, 贺越, 李晓, 等. 遗传和环境因素对青少年脑灰质容积和皮层厚度影响的双生子研究. 中国神经精神疾病杂志, 2018, 44(6): 354-359.
22. Gao W, Grewen K, Knickmeyer R C, et al. A review on neuroimaging studies of genetic and environmental influences on early brain development. Neuroimage, 2019, 185: 802-812.
23. Ge T, Chen C Y, Vettermann R, et al. The shared genetic basis of human fluid intelligence and brain morphology. Cereb Cortex, 2018, 29(8): 3471-3481.
24. Elliott L T, Sharp K, Alfaro-Almagro F, et al. Genome-wide association studies of brain imaging phenotypes in UK Biobank. Nature, 2018, 562(7726): 210-216.
25. Eyler L T, Vuoksimaa E, Panizzon M S, et al. Conceptual and data-based investigation of genetic influences and brain asymmetry: a twin study of multiple structural phenotypes. J Cogn Neurosci, 2014, 26(5): 1100-1117.
26. Liu S, Li A, Zhu M, et al. Genetic influences on cortical myelination in the human brain. Genes Brain Behav, 2019, 18(4): e12537.
27. Wen W, Thalamuthu A, Mather K A, et al. Distinct genetic influences on cortical and subcortical brain structures. Scientific Reports, 2016, 6: 32760.
28. Zhao B, Ibrahim J G, Li Y, et al. Heritability of regional brain volumes in large-scale neuroimaging and genetic studies. Cereb Cortex, 2019, 29(7): 2904-2914.
29. Geschwind D H, Miller B L, Decarli C, et al. Heritability of lobar brain volumes in twins supports genetic models of cerebral laterality and handedness. Proc Natl Acad Sci U S A, 2002, 99(5): 3176-3181.
30. Yoon U, Fahim C, Perusse D, et al. Lateralized genetic and environmental influences on human brain morphology of 8-year-old twins. Neuroimage, 2010, 53(3): 1117-1125.
31. Yoon U, Perusse D, Evans A C. Mapping genetic and environmental influences on cortical surface area of pediatric twins. Neuroscience, 2012, 220: 169-178.
32. van der Lee S J, Roshchupkin G V, Adams H H, et al. Gray matter heritability in family-based and population-based studies using voxel-based morphometry. Hum Brain Mapp, 2017, 38(5): 2408-2423.
33. Yoon U, Perusse D, Lee J M, et al. Genetic and environmental influences on structural variability of the brain in pediatric twin: deformation based morphometry. Neurosci Lett, 2011, 493(1/2): 8-13.
34. Lebel C, Deoni S. The development of brain white matter microstructure. Neuroimage, 2018, 182(1): 207-218.
35. Guadalupe T, Mathias S R, Vanerp T, et al. Human subcortical brain asymmetries in 15, 847 people worldwide reveal effects of age and sex. Brain Imaging Behav, 2017, 11(5): 1497-1514.
36. Parma V, Brasselet R, Zoia S, et al. The origin of human handedness and its role in pre-birth motor control. Sci Rep, 2017, 7(1): 16804.
37. Young G. Causality and Development. Berlin, Germany: Springer, Cham, 2019.
38. Barzilay E, Bar-Yosef O, Dorembus S, et al. Fetal brain anomalies associated with ventriculomegaly or asymmetry: an MRI-based study. AJNR Am J Neuroradiol, 2017, 38(2): 371-375.
39. Andescavage N N, Du Plessis A, Mccarter R, et al. Complex trajectories of brain development in the healthy human fetus. Cereb Cortex, 2017, 27(11): 5274-5283.
40. Jahanshad N, Lee A D, Barysheva M, et al. Genetic influences on brain asymmetry: a DTI study of 374 twins and siblings. Neuroimage, 2010, 52(2): 455-469.
41. Budisavljevic S, Dell'acqua F, Rijsdijk F V, et al. Age-related differences and heritability of the perisylvian language networks. J Neurosci, 2015, 35(37): 12625-12634.
42. Zhong S, He Y, Shu H, et al. Developmental changes in topological asymmetry between hemispheric brain white matter networks from adolescence to young adulthood. Cereb Cortex, 2017, 27(4): 2560-2570.
43. Brainstorm C, Anttila V, Bulik-Sullivan B, et al. Analysis of shared heritability in common disorders of the brain. Science, 2018, 360(6395): eaap8757.
44. Lee S J, Zhang J, Neale M C, et al. Quantitative tract-based white matter heritability in 1- and 2-year-old twins. Hum Brain Mapp, 2019, 40(4): 1164-1173.
45. Kennedy J T, Astafiev S V, Golosheykin S, et al. Shared genetic influences on adolescent body mass index and brain structure: a voxel-based morphometry study in twins. Neuroimage, 2019, 199: 261-272.
46. Teeuw J, Brouwer R M, Koenis M, et al. Genetic influences on the development of cerebral cortical thickness during childhood and adolescence in a Dutch longitudinal twin sample: the brainscale study. Cereb Cortex, 2019, 29(3): 978-993.

Journal of Biomedical Engineering

Research progress on genetic effects of the asymmetry of human brain structure revealed by magnetic resonance imaging

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