Mapping cortical brain asymmetry in 17,141 healthy individuals worldwide via the ENIGMA consortium

Journal article


Kong, Xiang-Zhen, Mathias, Samuel R., Guadalupe, Tulio, ENIGMA Laterality Working Group,, Glahn, David C., Franke, Barbara, Crivello, Fabrice, Tzourio-Mazoyer, Nathalie, Fisher, Simon E., Thompson, Paul M., Francks, Clyde, Lorenzetti, Valentina and ENIGMA Laterality Working Group. (2018). Mapping cortical brain asymmetry in 17,141 healthy individuals worldwide via the ENIGMA consortium. Proceedings of the National Academy of Sciences of USA. 115(22), pp. E5154 - E5163. https://doi.org/10.1073/pnas.1718418115
AuthorsKong, Xiang-Zhen, Mathias, Samuel R., Guadalupe, Tulio, ENIGMA Laterality Working Group,, Glahn, David C., Franke, Barbara, Crivello, Fabrice, Tzourio-Mazoyer, Nathalie, Fisher, Simon E., Thompson, Paul M., Francks, Clyde, Lorenzetti, Valentina and ENIGMA Laterality Working Group
Abstract

Hemispheric asymmetry is a cardinal feature of human brain organization. Altered brain asymmetry has also been linked to some cognitive and neuropsychiatric disorders. Here, the ENIGMA (Enhancing NeuroImaging Genetics through Meta-Analysis) Consortium presents the largest-ever analysis of cerebral cortical asymmetry and its variability across individuals. Cortical thickness and surface area were assessed in MRI scans of 17,141 healthy individuals from 99 datasets worldwide. Results revealed widespread asymmetries at both hemispheric and regional levels, with a generally thicker cortex but smaller surface area in the left hemisphere relative to the right. Regionally, asymmetries of cortical thickness and/or surface area were found in the inferior frontal gyrus, transverse temporal gyrus, parahippocampal gyrus, and entorhinal cortex. These regions are involved in lateralized functions, including language and visuospatial processing. In addition to population-level asymmetries, variability in brain asymmetry was related to sex, age, and intracranial volume. Interestingly, we did not find significant associations between asymmetries and handedness. Finally, with two independent pedigree datasets (n = 1,443 and 1,113, respectively), we found several asymmetries showing significant, replicable heritability. The structural asymmetries identified and their variabilities and heritability provide a reference resource for future studies on the genetic basis of brain asymmetry and altered laterality in cognitive, neurological, and psychiatric disorders.

Keywordsbrain asymmetry; lateralization; cortical thickness; surface area; meta-analysis
Year2018
JournalProceedings of the National Academy of Sciences of USA
Journal citation115 (22), pp. E5154 - E5163
PublisherNational Academy of Sciences
ISSN0027-8424
Digital Object Identifier (DOI)https://doi.org/10.1073/pnas.1718418115
Scopus EID2-s2.0-85047904406
Page rangeE5154 - E5163
Publisher's version
File Access Level
Controlled
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Please refer to the journal article webpage for a complete list of the ENIGMA Laterality Working Group contributors.

Place of publicationUnited States of America
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Hall, Wayne, Hoch, Eva and Lorenzetti, Valentina. (2019). Cannabis use and mental health : Risks and benefits [Editorial]. European Archives of Psychiatry and Clinical Neuroscience. 269, pp. 1-3. https://doi.org/10.1007/s00406-019-00986-2
Neuroanatomical alterations in people with high and low cannabis dependence
Lorenzetti, Valentina, Chye, Yann, Suo, Chao, Walterfang, Mark, Lubman, Dan I., Takagi, Michael, Whittle, Sarah, Verdejo-Garcia, Antonio, Cousijn, Janna, Pantelis, Christos, Seal, Marc, Fornito, Alex, Yücel, Murat and Solowij, Nadia. (2019). Neuroanatomical alterations in people with high and low cannabis dependence. Australian and New Zealand Journal of Psychiatry. 54(1), pp. 68-75. https://doi.org/10.1177/0004867419859077
A roadmap for integrating neuroscience into addiction treatment : A consensus of the neuroscience interest group of the international society of addiction medicine
Verdejo-Garcia, Antonio, Lorenzetti, Valentina, Manning, Victoria, Piercy, Hugh, Bruno, Raimondo, Hester, Rob, Pennington, David, Tolomeo, Serenella, Arunogiri, Shalini, Bates, Marsha E., Bowden-Jones, Henrietta, Campanella, Salvatore, Daughters, Stacey B., Kouimtsidis, Christos, Lubman, Dan I., Meyerhoff, Dieter J., Ralph, Annaketurah, Rezapour, Tara, Tavakoli, Hosna, ... Ekhtiari, Hamed. (2019). A roadmap for integrating neuroscience into addiction treatment : A consensus of the neuroscience interest group of the international society of addiction medicine. Frontiers in Psychiatry. 10, p. Article 877. https://doi.org/10.3389/fpsyt.2019.00877
Defining compulsive behavior
Luigjes, Judy, Lorenzetti, Valentina, de Haan, Sanneke, Youssef, George J., Murawski, Carsten, Sjoerds, Zsuzsika, van den Brink, Wim, Denys, Damiaan, Fontenelle, Leonardo F. and Yücel, Murat. (2019). Defining compulsive behavior. Neuropsychology Review. 29(1), pp. 4-13. https://doi.org/10.1007/s11065-019-09404-9
Transdiagnostic variations in impulsivity and compulsivity in obsessive-compulsive disorder and gambling disorder correlate with effective connectivity in cortical-striatal-thalamic-cortical circuits
Parkes, Linden, Tiego, Jeggan, Aquino, Kevin, Braganza, Leah, Chamberlain, Samuel R., Fontenelle, Leonardo F., Harrison, Ben J., Lorenzetti, Valentina, Paton, Bryan, Razi, Adeel, Fornito, Alex and Yücel, Murat. (2019). Transdiagnostic variations in impulsivity and compulsivity in obsessive-compulsive disorder and gambling disorder correlate with effective connectivity in cortical-striatal-thalamic-cortical circuits. NeuroImage. 202, p. 116070. https://doi.org/10.1016/j.neuroimage.2019.116070
Does regular cannabis use affect neuroanatomy? An updated systematic review and meta-analysis of structural neuroimaging studies
Lorenzetti, Valentina, Chye, Yann, Silva, Pedro, Solowij, Nadia and Roberts, Carl A.. (2019). Does regular cannabis use affect neuroanatomy? An updated systematic review and meta-analysis of structural neuroimaging studies. European Archives of Psychiatry and Clinical Neuroscience. 269(1), pp. 59 - 71. https://doi.org/10.1007/s00406-019-00979-1
Mega-analysis of gray matter volume in substance dependence: General and substance-specific regional effects
Mackey, Scott, Allgaier, Nicholas, Chaarani, Bader, Spechler, Philip, Orr, Catherine, Bunn, Janice, Allen, Nicholas B., Alia-Klein, Nelly, Batalla, Albert, Blaine, Sara K., Brooks, Samantha, Caparelli, Elisabeth C., Chye, Yann Ying, Cousijn, Janna, Dagher, Alain, Desrivieres, Sylvane, Feldstein-Ewing, Sarah W., Foxe, John J., Goldstein, Rita Z., ... Garavan, Hugh. (2019). Mega-analysis of gray matter volume in substance dependence: General and substance-specific regional effects. American Journal of Psychiatry. 176(2), pp. 119 - 128. https://doi.org/10.1176/appi.ajp.2018.17040415
From socioeconomic disadvantage to obesity: The mediating role of psychological distress and emotional eating
Spinosa, Jade, Christiansen, Paul, Dickson, Joanne M., Lorenzetti, Valentina and Hardman, Charlotte A.. (2019). From socioeconomic disadvantage to obesity: The mediating role of psychological distress and emotional eating. Obesity. 27(4), pp. 559 - 564. https://doi.org/10.1002/oby.22402
Impulsivity and body fat accumulation are linked to cortical and subcortical brain volumes among adolescents and adults
Kakoschke, Naomi, Lorenzetti, Valentina, Caeyenberghs, Karen and Verdejo-García, Antonio. (2019). Impulsivity and body fat accumulation are linked to cortical and subcortical brain volumes among adolescents and adults. Scientific Reports. 9(1), pp. 1 - 11. https://doi.org/10.1038/s41598-019-38846-7
Alteration to hippocampal volume and shape confined to cannabis dependence: A multi-site study
Chye, Yann, Lorenzetti, Valentina, Suo, Chao, Batalla, Albert, Cousijn, Janna, Goudriaan, Anna E., Jenkinson, Mark, Martin-Santos, Rocio, Whittle, Sarah, Yücel, Murat and Solowij, Nadia. (2019). Alteration to hippocampal volume and shape confined to cannabis dependence: A multi-site study. Addiction Biology. 24(4), pp. 822 - 834. https://doi.org/10.1111/adb.12652
Cortical surface morphology in long-term cannabis users: A multi-site MRI study
Chye, Yann, Suo, Chao, Lorenzetti, Valentina, Batalla, Albert, Cousijn, Janna, Goudriaan, Anna E., Martin-Santos, Rocio, Whittle, Sarah, Solowij, Nadia and Yücel, Murat. (2019). Cortical surface morphology in long-term cannabis users: A multi-site MRI study. European Neuropsychopharmacology. 29(2), pp. 257 - 265. https://doi.org/10.1016/j.euroneuro.2018.11.1110
Reduced amygdala volumes are related to motor and cognitive signs in Huntington's disease: The IMAGE-HD study
Ahveninen, Lotta M., Stout, Julie C., Georgiou-Karistianis, Nellie, Lorenzetti, Valentina and Glikmann-Johnston, Yifat. (2018). Reduced amygdala volumes are related to motor and cognitive signs in Huntington's disease: The IMAGE-HD study. NeuroImage: Clinical. 18, pp. 881 - 887. https://doi.org/10.1016/j.nicl.2018.03.027
The anticipation and outcome phases of reward and loss processing: A neuroimaging meta-analysis of the monetary incentive delay task
Oldham, Stuart, Murawski, Carsten, Fornito, Alex, Youssef, George J., Yücel, Murat and Lorenzetti, Valentina. (2018). The anticipation and outcome phases of reward and loss processing: A neuroimaging meta-analysis of the monetary incentive delay task. Human Brain Mapping. 39(8), pp. 3398 - 3418. https://doi.org/10.1002/hbm.24184
Exploring the association of legalisation status of cannabis with problematic cannabis use and impulsivity in the USA
Destrée, Louise, Amiet, Danielle, Carter, Adrian, Lee, Rico, Lorenzetti, Valentina, Segrave, Rebecca, Youssef, George, Solowij, Nadia and Yücel, Murat. (2018). Exploring the association of legalisation status of cannabis with problematic cannabis use and impulsivity in the USA. Drugs in Context. 7, pp. 1 - 5. https://doi.org/10.7573/dic.212541
Emotion regulation using virtual environments and real-time fMRI neurofeedback
Lorenzetti, Valentina, Melo, Bruno, Basílio, Rodrigo, Suo, Chao, Yücel, Murat, Tierra-Criollo, Carlos J. and Moll, Jorge. (2018). Emotion regulation using virtual environments and real-time fMRI neurofeedback. Frontiers in Neurology. 9, pp. 1 - 15. https://doi.org/10.3389/fneur.2018.00390
A systematic review and meta-analysis of the neural correlates of psychological therapies in major depression
Sankar, Anjali, Melin, Alice, Lorenzetti, Valentina, Horton, Paul, Costafreda, Sergi G. and Fu, Cynthia H. Y.. (2018). A systematic review and meta-analysis of the neural correlates of psychological therapies in major depression. Psychiatry Research: Neuroimaging. 279, pp. 31 - 39. https://doi.org/10.1016/j.pscychresns.2018.07.002
A transdiagnostic dimensional approach towards a neuropsychological assessment for addiction: an international Delphi consensus study
Yucel, Murat, Oldenhof, Erin, Ahmed, Serge H., Belin, David, Billieux, Joel, Bowden-Jones, Henrietta, Carter, Adrian, Chamberlain, Samuel R., Clark, Luke, Connor, Jason P., Daglish, Mark, Dom, Geert, Dannon, Pinhas, Duka, Theodora, Fernandez-Serrano, Maria Jose, Field, Matt, Franken, Ingmar, Goldstein, Rita Z., Gonzalez, Raul, ... Verdejo-Garcia, Antonio. (2018). A transdiagnostic dimensional approach towards a neuropsychological assessment for addiction: an international Delphi consensus study. Addiction. 114(6), pp. 1095 - 1109. https://doi.org/10.1111/add.14424
Unpacking the role of self-reported compulsivity and impulsivity in obsessive-compulsive disorder
Prochazkova, Luisa, Parkes, Linden, Dawson, Andrew, Youssef, George J., Ferreira, Gabriela M., Lorenzetti, Valentina, Segrave, Rebecca A., Fontenelle, Leonardo F. and Yücel, Murat. (2018). Unpacking the role of self-reported compulsivity and impulsivity in obsessive-compulsive disorder. CNS Spectrums. 23(1), pp. 51 - 58. https://doi.org/10.1017/S1092852917000244
Neuroscience in gambling policy and treatment: an interdisciplinary perspective
Murat Yucel, Adrian Carter, Amy R Allen, Bernard Balleine, Luke Clark, Nicki A Dowling, Sally M Gainsbury, Anna E Goudriaan, Jon Grant, Alan Hayes, David Hodgins, Ruth van Holst, Ralph Lattimore, Charles Livingstone, Valentina Lorenzetti, Dan Lubman, Carsten Murawski, Linden Parkes, Nancy Petry, ... Wayne Hall. (2017). Neuroscience in gambling policy and treatment: an interdisciplinary perspective. The Lancet Psychiatry. 4(6), pp. 501-506. https://doi.org/10.1016/S2215-0366(16)30369-8
Orbitofrontal and caudate volumes in cannabis users: A multi-site mega-analysis comparing dependent versus non-dependent users
Chye, Yann, Solowij, Nadia, Suo, Chao, Batalla, Albert, Cousijn, Janna, Goudriaan, Anna E., Martin-Santos, Rocio, Whittle, Sarah, Lorenzetti, Valentina and Yücel, Murat. (2017). Orbitofrontal and caudate volumes in cannabis users: A multi-site mega-analysis comparing dependent versus non-dependent users. Psychopharmacology. 234(13), pp. 1985 - 1995. https://doi.org/10.1007/s00213-017-4606-9
Cannabis-related hippocampal volumetric abnormalities specific to subregions in dependent users
Chye, Yann, Suo, Chao, Yücel, Murat, den Ouden, Lauren, Solowij, Nadia and Lorenzetti, Valentina. (2017). Cannabis-related hippocampal volumetric abnormalities specific to subregions in dependent users. Psychopharmacology. 234(14), pp. 2149 - 2157. https://doi.org/10.1007/s00213-017-4620-y
A psychometric validation study of the Impulsive-Compulsive Behaviours Checklist: A transdiagnostic tool for addictive and compulsive behaviours
Guo, Karen, Youssef, George J., Dawson, Andrew, Parkes, Linden, Oostermeijer, Sanne, López-Solà, Clara, Lorenzetti, Valentina, Greenwood, Christopher, Fontenelle, Leonardo F. and Yücel, Murat. (2017). A psychometric validation study of the Impulsive-Compulsive Behaviours Checklist: A transdiagnostic tool for addictive and compulsive behaviours. Addictive Behaviors. 67, pp. 26 - 33. https://doi.org/10.1016/j.addbeh.2016.11.021
Longitudinal study of hippocampal volumes in heavy cannabis users
Koenders, L., Lorenzetti, Valentina, de Haan, L., Suo, C., Vingerhoets, W. A. M., van den Brink, W., Wiers, R. W., Meijer, C. J., MacHielsen, M. W. J., Goudriaan, Anna E., Veltman, D. J., Yücel, Murat and Cousijn, Janna. (2017). Longitudinal study of hippocampal volumes in heavy cannabis users. Journal of Psychopharmacology. 31(8), pp. 1027 - 1034. https://doi.org/10.1177/0269881117718380
Role of orbitofrontal sulcogyral pattern on lifetime cannabis use and depressive symptoms
Chye, Yann, Solowij, Nadia, Ganella, Eleni P., Suo, Chao, Yücel, Murat, Batalla, Albert, Cousijn, Janna, Goudriaan, Anna E., Martin-Santos, Rocio, Whittle, Sarah, Bartholomeusz, Cali F. and Lorenzetti, Valentina. (2017). Role of orbitofrontal sulcogyral pattern on lifetime cannabis use and depressive symptoms. Progress in Neuropsychopharmacology and Biological Psychiatry. 79, pp. 392 - 400. https://doi.org/10.1016/j.pnpbp.2017.07.017
Investigating the role of anticipatory reward and habit strength in obsessive-compulsive disorder
Ferreira, Gabriela M., Yücel, Murat, Dawson, Andrew, Lorenzetti, Valentina and Fontenelle, Leonardo F.. (2017). Investigating the role of anticipatory reward and habit strength in obsessive-compulsive disorder. CNS Spectrums. 22(3), pp. 295 - 304. https://doi.org/10.1017/S1092852916000535
Neuroimaging of the human brain in adolescent substance users
Takagi, Michael, Youssef, George and Lorenzetti, Valentina. (2016). Neuroimaging of the human brain in adolescent substance users. In In De Micheli, Denise, Andrade, André Luiz Monezi, da Silva, Eroy Aparecida and de Souza Formigoni, Maria Lucia Oliveira (Ed.). Drug abuse in adolescence : Neurobiological, cognitive, and psychological issues pp. 69-99 Springer. https://doi.org/10.1007/978-3-319-17795-3_6
Cannabis use disorders and altered brain morphology : Where is the evidence?
Lorenzetti, Valentina, Batalla, Albert and Cousijn, Janna. (2016). Cannabis use disorders and altered brain morphology : Where is the evidence? Current Addiction Reports. 3(2), pp. 189-198. https://doi.org/10.1007/s40429-016-0102-2
The neurobiology of cannabis use disorders: A call for evidence
Valentina Lorenzetti, Janna Cousijn, Nadia Solowij, Hugh Garavan, Chao Suo, Murat Yucel and Antonio Verdejo-Garcia. (2016). The neurobiology of cannabis use disorders: A call for evidence. Frontiers in Behavioral Neuroscience. 10, pp. 1-3. https://doi.org/10.3389/fnbeh.2016.00086
Olfactory sulcus morphology in patients with current and past major depression
Takahashi, Tsutomu, Nishikawa, Yumiko, Yücel, Murat, Whittle, Sarah, Lorenzetti, Valentina, Walterfang, Mark, Sasabayashi, Daiki, Suzuki, Michio, Pantelis, Christos and Allen, Nicholas B.. (2016). Olfactory sulcus morphology in patients with current and past major depression. Psychiatry Research: Neuroimaging. 255, pp. 60 - 65. https://doi.org/10.1016/j.pscychresns.2016.07.008
Genetic imaging consortium for addiction medicine: From neuroimaging to genes
Mackey, Scott, Kan, Kees-Jan, Chaarani, Bader, Alia-Klein, Nelly, Batalla, Albert, Brooks, Samantha, Cousijn, Janna, Dagher, Alain, de Ruiter, Michiel, Desrivieres, Sylvane, Feldstein Ewing, Sarah W., Goldstein, Rita Z., Goudriaan, Anna E., Heitzeg, Mary M., Hutchison, Kent, Li, Chiang-Shan R., London, Edythe D., Lorenzetti, Valentina, Luijten, Maartje, ... Conrod, Patricia. (2016). Genetic imaging consortium for addiction medicine: From neuroimaging to genes. In Neuroscience for addiction medicine: From prevention to rehabilitation - methods and interventions pp. 203 - 223 Elsevier. https://doi.org/10.1016/bs.pbr.2015.07.026
Adolescent cannabis use: What is the evidence for functional brain alteration?
Lorenzetti, Valentina, Alonso-Lana, Silvia, Youssef, G. J., Verdejo-Garcia, Antonio, Suo, Chao, Cousijn, Janna, Takagi, Michael, Yucel, Murat and Solowij, Nadia. (2016). Adolescent cannabis use: What is the evidence for functional brain alteration? Current Pharmaceutical Design. 22(42), pp. 6353 - 6365. https://doi.org/10.2174/1381612822666160805155922
The role of cannabinoids in neuroanatomic alterations in cannabis users
Lorenzetti, Valentina, Solowij, Nadia and Yücel, Murat. (2016). The role of cannabinoids in neuroanatomic alterations in cannabis users. Biological Psychiatry. 79(7), pp. e17 - e31. https://doi.org/10.1016/j.biopsych.2015.11.013
Hippocampal harms, protection and recovery following regular cannabis use
Yücel, Murat, Lorenzetti, Valentina, Suo, C., Zalesky, Andrew, Fornito, Alex, Takagi, Michael J., Lubman, Dan I. and Solowij, Nadia. (2016). Hippocampal harms, protection and recovery following regular cannabis use. Translational Psychiatry. 6(1), pp. 1 - 7. https://doi.org/10.1038/tp.2015.201
An MRI study of white matter tract integrity in regular cannabis users: Effects of cannabis use and age
Jakabek, David, Yucel, Murat, Lorenzetti, Valentina and Solowij, Nadia. (2016). An MRI study of white matter tract integrity in regular cannabis users: Effects of cannabis use and age. Psychopharmacology. 233(19-20), pp. 3627 - 3637. https://doi.org/10.1007/s00213-016-4398-3
Gross morphological brain changes with chronic, heavy cannabis use
Lorenzetti, Valentina, Solowij, Nadia, Whittle, Sarah, Fornito, Alex, Lubman, Dan I., Pantelis, Christos and Yücel, Murat. (2015). Gross morphological brain changes with chronic, heavy cannabis use. British Journal of Psychiatry. 206(1), pp. 77 - 78. https://doi.org/10.1192/bjp.bp.114.151407
Cortico-limbic network abnormalities in individuals with current and past major depressive disorder
Klauser, Paul, Fornito, Alex, Lorenzetti, Valentina, Davey, Christopher G., Dwyer, Dominic B., Allen, Nicholas B. and Yücel, Murat. (2015). Cortico-limbic network abnormalities in individuals with current and past major depressive disorder. Journal of Affective Disorders. 173, pp. 45 - 52. https://doi.org/10.1016/j.jad.2014.10.041
The association between regular cannabis exposure and alterations of human brain morphology: An updated review of the literature
Lorenzetti, Valentina, Solowij, Nadia, Fornito, Alex, Lubman, Dan Ian and Yücel, Murat. (2014). The association between regular cannabis exposure and alterations of human brain morphology: An updated review of the literature. Current Pharmaceutical Design. 20(13), pp. 2138 - 2167. https://doi.org/10.2174/13816128113199990435
The neural cascade of olfactory processing: A combined fMRI-EEG study
Masaoka, Yuri, Harding, Ian H., Koiwa, Nobuyoshi, Yoshida, Masaki, Harrison, Ben J., Lorenzetti, Valentina, Ida, Masahiro, Izumizaki, Masahiko, Pantelis, Christos and Homma, Ikuo. (2014). The neural cascade of olfactory processing: A combined fMRI-EEG study. Respiratory Physiology & Neurobiology. 204, pp. 71 - 77. https://doi.org/10.1016/j.resp.2014.06.008
Human amygdala volume is predicted by common DNA variation in the stathmin and serotonin transporter genes
Stjepanović, D., Lorenzetti, Valentina, Yücel, Murat, Hawi, Z. and Bellgrove, M. A.. (2013). Human amygdala volume is predicted by common DNA variation in the stathmin and serotonin transporter genes. Translational Psychiatry. 3(7), pp. 1 - 7. https://doi.org/10.1038/tp.2013.41
Alteration to hippocampal shape in cannabis users with and without schizophrenia
Solowij, Nadia, Walterfang, Mark, Lubman, Dan I., Whittle, Sarah, Lorenzetti, Valentina, Styner, Martin, Velakoulis, Dennis, Pantelis, Christos and Yucel, Murat. (2013). Alteration to hippocampal shape in cannabis users with and without schizophrenia. Schizophrenia Research. 143(1), pp. 179 - 184. https://doi.org/10.1016/j.schres.2012.10.040