Subcortical surface morphometry in substance dependence: An ENIGMA addiction working group study

Yann Chye; Scott Mackey; Boris A. Gutman; Christopher R. K. Ching; Albert Batalla; Sara Blaine; Samantha Brooks; Elisabeth C. Caparelli; Janna Cousijn; Alain Dagher; John J. Foxe; Anna E. Goudriaan; Robert Hester; Kent Hutchison; Neda Jahanshad; Anne M. Kaag; Ozlem Korucuoglu; Chiang-Shan R. Li; Edythe D. London; Valentina Lorenzetti; Maartje Luijten; Rocio Martin-Santos; Shashwath A. Meda; Reza Momenan; Angelica Morales; Catherine Orr; Martin P. Paulus; Godfrey Pearlson; Liesbeth Reneman; Lianne Schmaal; Rajita Sinha; Nadia Solowij; Dan J. Stein; Elliot A. Stein; Deborah Tang; Anne Uhlmann; Ruth van Holst; Dick J. Veltman; Antonio Verdejo-Garcia; Reinout W. Wiers; Murat Yuecel; Paul M. Thompson; Patricia Conrod; Hugh Garavan

doi:10.1111/adb.12830

Subcortical surface morphometry in substance dependence: An ENIGMA addiction working group study

Yann Chye, Scott Mackey, Boris A. Gutman, Christopher R. K. Ching, Albert Batalla, Sara Blaine, Samantha Brooks, Elisabeth C. Caparelli, Janna Cousijn, Alain Dagher, John J. Foxe, Anna E. Goudriaan, Robert Hester, Kent Hutchison, Neda Jahanshad, Anne M. Kaag, Ozlem Korucuoglu, Chiang-Shan R. Li, Edythe D. London, Valentina LorenzettiMaartje Luijten, Rocio Martin-Santos, Shashwath A. Meda, Reza Momenan, Angelica Morales, Catherine Orr, Martin P. Paulus, Godfrey Pearlson, Liesbeth Reneman, Lianne Schmaal, Rajita Sinha, Nadia Solowij, Dan J. Stein, Elliot A. Stein, Deborah Tang, Anne Uhlmann, Ruth van Holst, Dick J. Veltman, Antonio Verdejo-Garcia, Reinout W. Wiers, Murat Yuecel, Paul M. Thompson, Patricia Conrod, Hugh Garavan

Clinical Neuropsychology

Research output: Contribution to Journal › Article › Academic › peer-review

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Abstract

While imaging studies have demonstrated volumetric differences in subcortical structures associated with dependence on various abused substances, findings to date have not been wholly consistent. Moreover, most studies have not compared brain morphology across those dependent on different substances of abuse to identify substance-specific and substance-general dependence effects. By pooling large multinational datasets from 33 imaging sites, this study examined subcortical surface morphology in 1628 nondependent controls and 2277 individuals with dependence on alcohol, nicotine, cocaine, methamphetamine, and/or cannabis. Subcortical structures were defined by FreeSurfer segmentation and converted to a mesh surface to extract two vertex-level metrics—the radial distance (RD) of the structure surface from a medial curve and the log of the Jacobian determinant (JD)—that, respectively, describe local thickness and surface area dilation/contraction. Mega-analyses were performed on measures of RD and JD to test for the main effect of substance dependence, controlling for age, sex, intracranial volume, and imaging site. Widespread differences between dependent users and nondependent controls were found across subcortical structures, driven primarily by users dependent on alcohol. Alcohol dependence was associated with localized lower RD and JD across most structures, with the strongest effects in the hippocampus, thalamus, putamen, and amygdala. Meanwhile, nicotine use was associated with greater RD and JD relative to nonsmokers in multiple regions, with the strongest effects in the bilateral hippocampus and right nucleus accumbens. By demonstrating subcortical morphological differences unique to alcohol and nicotine use, rather than dependence across all substances, results suggest substance-specific relationships with subcortical brain structures.

Original language	English
Article number	e12830
Pages (from-to)	1-15
Number of pages	15
Journal	Addiction Biology
Volume	25
Issue number	6
Early online date	20 Nov 2019
DOIs	https://doi.org/10.1111/adb.12830
Publication status	Published - Nov 2020

Funding

The authors report no competing interest. Dr C.R.K. Ching and Dr P.M. Thompson receives partial research support from Biogen, Inc. (Boston) for research unrelated to the topic of this manuscript. Dr M. Y\u00FCcel has received funding from Monash University and Australian Government funding bodies such as the National Health and Medical Research Council (NHMRC), the Australian Research Council (ARC), and the Department of Industry, Innovation and Science. He has also received philanthropic donations from the David Winston Turner Endowment Fund as well as payment from law firms in relation to court and/or expert witness reports. This work was supported in part by National Institutes of Health (NIH) grant U54EB020403 from the Big Data to Knowledge (BD2K) program. Dr Y. Chye was supported by the Monash Bridging Post doctoral Fellowship. Data collection: Dr C.R.K. Ching was supported by National Institutes of Health grants NIA T32AG058507, NIH/NIMH 5T32MH073526, and U54EB020403. Dr J. Cousijn and Dr A.E. Goudriaan received funding for the Cannabis Prospective Study from Netherlands Organization for Health Research and Development (ZonMW) grant 31180002 from Netherlands Organization for Scientific Research (NWO). Dr A. Dagher received support from the Canadian Institutes for Health Research (CIHR) Foundation Scheme. Dr H. Garavan and Dr J.J. Foxe received funding from the National Institute on Drug Abuse (NIDA) grant R01\u2010DA014100. Dr A.E. Goudriaan and Dr R.J. van Holst received funding from ZonMW grant 91676084 from NWO. Dr. A. E. Goudriaan is supported by an NWO\u2010ZonMw VIDI grant 91713354. Dr O. Korucuoglu received support for the neuro\u2010ADAPT study from the VICI grant 453.08.001 from the NWO, awarded to Dr R.W. Wiers. Dr C.R. Li received funding from NIDA grants R01AA021449, R01DA023248, and K25DA040032. Dr E.D. London received support from NIH grants DA15179, DA022539, and DA024853, F30 DA021961 (KB), and MOI\u2010RR\u201000865 (UCLA GCRC); endowments from the Katherine K. and Thomas P. Pike Chair in Addiction Studies and Marjorie M. Greene Trust, Philip Morris USA UCLA contract 20063287, and institutional training grants T32 DA 024635 (support of Angelica Morales) and T32 MH17140 (support of Golnaz Tabibnia). Dr M. Luitjen and Dr D.J. Veltman received support from the VIDI grant 016.08.322 from NWO, awarded to Ingmar H.A. Franken. Dr R. Momenan received support from the National Institutes of Alcohol Abuse and Alcoholism (NIAAA)/NIH intramural research funding ZIA AA000125\u201304 to the Clinical NeuroImaging Research Core. Dr A. Morales received support from NIDA grant T32 DA024635. Dr M.P. Paulus received funding from National Institute of Mental Health (NIMH) grant R01 DA018307. Dr G. Pearlson received funding from the NIDA grant R01 DA020709 and the NIAAA grants AA016599 and AA19036. Dr R. Martin\u2010Santos received support from Plan Nacional sobre Drogas. Ministerio de Sanidad y Pol\u00EDtica Social grant PNSD:2011/050 and SGR:2014/1114. Dr L. Reneman received funding from the Netherlands Organisation for Health Research and Development 40\u201000812\u201098\u201011002. Dr L. Schmaal and Dr D.J. Veltman received funding from ZonMW grant 31160003 from NWO. Dr R. Sinha received funding from NIDA (PL31\u20101DA024859\u201001), NIH National Center for Research Resources (UL1\u2010RR24925\u201001), and NIAAA grant (R01\u2010AA013892). Dr Z. Sjoerds and Dr D.J. Veltman received funding from ZonMW grant 31160004 from NWO. Dr N. Solowij received support from the Clive and Vera Ramaciotti Foundation for Biomedical Research, the National Health and Medical Research Council Project grant 459111, and Australian Research Council Future Fellowship grant FT110100752. Dr D. Stein received support from the South African Medical Research Council. Dr E.A. Stein received support from the Intramural Research Program of the National Institute on Drug Abuse (NIDA\u2010NIH). Dr. A. Verdejo\u2010Garcia received support from the Australian Medical Research Future Fund (MRF1141214). Dr M. Y\u00FCcel received support from the National Health and Medical Research Council Fellowship grant 1117188 and the David Winston Turner Endowment Fund.

Funders	Funder number
Australian Medical Research Future Fund	1117188, MRF1141214
Clive and Vera Ramaciotti Foundation for Biomedical Research
NIDA‐NIH
NIH National Center for Research Resources	31160004, R01‐AA013892, UL1‐RR24925‐01
NIH/NIMH	5T32MH073526
NWO‐ZonMw VIDI	453.08.001, F30 DA021961, MOI‐RR‐00865, DA024853, 91713354, DA15179, DA022539
Netherlands Organization for Health Research and Development
Netherlands Organization for Scientific Research
National Institutes of Health	U54EB020403
National Institute of Mental Health	R01 DA018307, AA016599, R01 DA020709, AA19036
National Institute on Drug Abuse	R01DA023248, 91676084, K25DA040032, R01‐DA014100
National Institute on Alcohol Abuse and Alcoholism	R01AA013892, T32 DA024635, R01AA021449, ZIA AA000125–04
National Institute on Aging	T32AG058507
University of California, Los Angeles
Marjorie M. Greene Trust
Philip Morris International	T32 DA 024635, 016.08.322, T32 MH17140, 20063287
Australian Government
Canadian Institutes of Health Research
Australian Research Council	FT110100752
National Health and Medical Research Council	459111
South African Medical Research Council
Monash University
ZonMw	40‐00812‐98‐11002, 31180002, 31160003, PL31‐1DA024859‐01
Nederlandse Organisatie voor Wetenschappelijk Onderzoek
Department of Industry, Innovation and Science, Australian Government

Keywords

addiction
structural MRI
substance dependence

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

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10.1111/adb.12830

Subcortical surface morphometry in substance dependence An ENIGMA addiction workingFinal published version, 48.2 MBLicence: Article 25fa Dutch Copyright Act

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Chye, Y., Mackey, S., Gutman, B. A., Ching, C. R. K., Batalla, A., Blaine, S., Brooks, S., Caparelli, E. C., Cousijn, J., Dagher, A., Foxe, J. J., Goudriaan, A. E., Hester, R., Hutchison, K., Jahanshad, N., Kaag, A. M., Korucuoglu, O., Li, C.-S. R., London, E. D., ... Garavan, H. (2020). Subcortical surface morphometry in substance dependence: An ENIGMA addiction working group study. Addiction Biology, 25(6), 1-15. Article e12830. https://doi.org/10.1111/adb.12830

@article{a44817b21b014ed59eed7e221cdbf97f,

title = "Subcortical surface morphometry in substance dependence: An ENIGMA addiction working group study",

abstract = "While imaging studies have demonstrated volumetric differences in subcortical structures associated with dependence on various abused substances, findings to date have not been wholly consistent. Moreover, most studies have not compared brain morphology across those dependent on different substances of abuse to identify substance-specific and substance-general dependence effects. By pooling large multinational datasets from 33 imaging sites, this study examined subcortical surface morphology in 1628 nondependent controls and 2277 individuals with dependence on alcohol, nicotine, cocaine, methamphetamine, and/or cannabis. Subcortical structures were defined by FreeSurfer segmentation and converted to a mesh surface to extract two vertex-level metrics—the radial distance (RD) of the structure surface from a medial curve and the log of the Jacobian determinant (JD)—that, respectively, describe local thickness and surface area dilation/contraction. Mega-analyses were performed on measures of RD and JD to test for the main effect of substance dependence, controlling for age, sex, intracranial volume, and imaging site. Widespread differences between dependent users and nondependent controls were found across subcortical structures, driven primarily by users dependent on alcohol. Alcohol dependence was associated with localized lower RD and JD across most structures, with the strongest effects in the hippocampus, thalamus, putamen, and amygdala. Meanwhile, nicotine use was associated with greater RD and JD relative to nonsmokers in multiple regions, with the strongest effects in the bilateral hippocampus and right nucleus accumbens. By demonstrating subcortical morphological differences unique to alcohol and nicotine use, rather than dependence across all substances, results suggest substance-specific relationships with subcortical brain structures.",

keywords = "addiction, structural MRI, substance dependence",

author = "Yann Chye and Scott Mackey and Gutman, {Boris A.} and Ching, {Christopher R. K.} and Albert Batalla and Sara Blaine and Samantha Brooks and Caparelli, {Elisabeth C.} and Janna Cousijn and Alain Dagher and Foxe, {John J.} and Goudriaan, {Anna E.} and Robert Hester and Kent Hutchison and Neda Jahanshad and Kaag, {Anne M.} and Ozlem Korucuoglu and Li, {Chiang-Shan R.} and London, {Edythe D.} and Valentina Lorenzetti and Maartje Luijten and Rocio Martin-Santos and Meda, {Shashwath A.} and Reza Momenan and Angelica Morales and Catherine Orr and Paulus, {Martin P.} and Godfrey Pearlson and Liesbeth Reneman and Lianne Schmaal and Rajita Sinha and Nadia Solowij and Stein, {Dan J.} and Stein, {Elliot A.} and Deborah Tang and Anne Uhlmann and {van Holst}, Ruth and Veltman, {Dick J.} and Antonio Verdejo-Garcia and Wiers, {Reinout W.} and Murat Yuecel and Thompson, {Paul M.} and Patricia Conrod and Hugh Garavan",

year = "2020",

month = nov,

doi = "10.1111/adb.12830",

language = "English",

volume = "25",

pages = "1--15",

journal = "Addiction Biology",

issn = "1355-6215",

publisher = "Wiley-Blackwell",

number = "6",

}

Chye, Y, Mackey, S, Gutman, BA, Ching, CRK, Batalla, A, Blaine, S, Brooks, S, Caparelli, EC, Cousijn, J, Dagher, A, Foxe, JJ, Goudriaan, AE, Hester, R, Hutchison, K, Jahanshad, N, Kaag, AM, Korucuoglu, O, Li, C-SR, London, ED, Lorenzetti, V, Luijten, M, Martin-Santos, R, Meda, SA, Momenan, R, Morales, A, Orr, C, Paulus, MP, Pearlson, G, Reneman, L, Schmaal, L, Sinha, R, Solowij, N, Stein, DJ, Stein, EA, Tang, D, Uhlmann, A, van Holst, R, Veltman, DJ, Verdejo-Garcia, A, Wiers, RW, Yuecel, M, Thompson, PM, Conrod, P & Garavan, H 2020, 'Subcortical surface morphometry in substance dependence: An ENIGMA addiction working group study', Addiction Biology, vol. 25, no. 6, e12830, pp. 1-15. https://doi.org/10.1111/adb.12830

TY - JOUR

T1 - Subcortical surface morphometry in substance dependence: An ENIGMA addiction working group study

AU - Chye, Yann

AU - Mackey, Scott

AU - Gutman, Boris A.

AU - Ching, Christopher R. K.

AU - Batalla, Albert

AU - Blaine, Sara

AU - Brooks, Samantha

AU - Caparelli, Elisabeth C.

AU - Cousijn, Janna

AU - Dagher, Alain

AU - Foxe, John J.

AU - Goudriaan, Anna E.

AU - Hester, Robert

AU - Hutchison, Kent

AU - Jahanshad, Neda

AU - Kaag, Anne M.

AU - Korucuoglu, Ozlem

AU - Li, Chiang-Shan R.

AU - London, Edythe D.

AU - Lorenzetti, Valentina

AU - Luijten, Maartje

AU - Martin-Santos, Rocio

AU - Meda, Shashwath A.

AU - Momenan, Reza

AU - Morales, Angelica

AU - Orr, Catherine

AU - Paulus, Martin P.

AU - Pearlson, Godfrey

AU - Reneman, Liesbeth

AU - Schmaal, Lianne

AU - Sinha, Rajita

AU - Solowij, Nadia

AU - Stein, Dan J.

AU - Stein, Elliot A.

AU - Tang, Deborah

AU - Uhlmann, Anne

AU - van Holst, Ruth

AU - Veltman, Dick J.

AU - Verdejo-Garcia, Antonio

AU - Wiers, Reinout W.

AU - Yuecel, Murat

AU - Thompson, Paul M.

AU - Conrod, Patricia

AU - Garavan, Hugh

PY - 2020/11

Y1 - 2020/11

N2 - While imaging studies have demonstrated volumetric differences in subcortical structures associated with dependence on various abused substances, findings to date have not been wholly consistent. Moreover, most studies have not compared brain morphology across those dependent on different substances of abuse to identify substance-specific and substance-general dependence effects. By pooling large multinational datasets from 33 imaging sites, this study examined subcortical surface morphology in 1628 nondependent controls and 2277 individuals with dependence on alcohol, nicotine, cocaine, methamphetamine, and/or cannabis. Subcortical structures were defined by FreeSurfer segmentation and converted to a mesh surface to extract two vertex-level metrics—the radial distance (RD) of the structure surface from a medial curve and the log of the Jacobian determinant (JD)—that, respectively, describe local thickness and surface area dilation/contraction. Mega-analyses were performed on measures of RD and JD to test for the main effect of substance dependence, controlling for age, sex, intracranial volume, and imaging site. Widespread differences between dependent users and nondependent controls were found across subcortical structures, driven primarily by users dependent on alcohol. Alcohol dependence was associated with localized lower RD and JD across most structures, with the strongest effects in the hippocampus, thalamus, putamen, and amygdala. Meanwhile, nicotine use was associated with greater RD and JD relative to nonsmokers in multiple regions, with the strongest effects in the bilateral hippocampus and right nucleus accumbens. By demonstrating subcortical morphological differences unique to alcohol and nicotine use, rather than dependence across all substances, results suggest substance-specific relationships with subcortical brain structures.

AB - While imaging studies have demonstrated volumetric differences in subcortical structures associated with dependence on various abused substances, findings to date have not been wholly consistent. Moreover, most studies have not compared brain morphology across those dependent on different substances of abuse to identify substance-specific and substance-general dependence effects. By pooling large multinational datasets from 33 imaging sites, this study examined subcortical surface morphology in 1628 nondependent controls and 2277 individuals with dependence on alcohol, nicotine, cocaine, methamphetamine, and/or cannabis. Subcortical structures were defined by FreeSurfer segmentation and converted to a mesh surface to extract two vertex-level metrics—the radial distance (RD) of the structure surface from a medial curve and the log of the Jacobian determinant (JD)—that, respectively, describe local thickness and surface area dilation/contraction. Mega-analyses were performed on measures of RD and JD to test for the main effect of substance dependence, controlling for age, sex, intracranial volume, and imaging site. Widespread differences between dependent users and nondependent controls were found across subcortical structures, driven primarily by users dependent on alcohol. Alcohol dependence was associated with localized lower RD and JD across most structures, with the strongest effects in the hippocampus, thalamus, putamen, and amygdala. Meanwhile, nicotine use was associated with greater RD and JD relative to nonsmokers in multiple regions, with the strongest effects in the bilateral hippocampus and right nucleus accumbens. By demonstrating subcortical morphological differences unique to alcohol and nicotine use, rather than dependence across all substances, results suggest substance-specific relationships with subcortical brain structures.

KW - addiction

KW - structural MRI

KW - substance dependence

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UR - http://www.scopus.com/inward/citedby.url?scp=85075237877&partnerID=8YFLogxK

U2 - 10.1111/adb.12830

DO - 10.1111/adb.12830

M3 - Article

SN - 1355-6215

VL - 25

SP - 1

EP - 15

JO - Addiction Biology

JF - Addiction Biology

IS - 6

M1 - e12830

ER -

Subcortical surface morphometry in substance dependence: An ENIGMA addiction working group study

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