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 Yücel; 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 Yücel, Paul M Thompson, Patricia Conrod, Hugh Garavan

Radiology & Nuclear Medicine

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

43 Citations (Scopus)

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
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

Bibliographical note

FUNDING INFORMATION
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‐DA014100. 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‐ZonMw VIDI grant 91713354. Dr O. Korucuoglu received
support for the neuro‐ADAPT 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‐RR‐00865 (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 AA000125–04 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‐Santos received support
from Plan Nacional sobre Drogas. Ministerio de Sanidad y Política
Social grant PNSD:2011/050 and SGR:2014/1114. Dr L. Reneman
received funding from the Netherlands Organisation for Health
Research and Development 40‐00812‐98‐11002. Dr L. Schmaal
and Dr D.J. Veltman received funding from ZonMW grant
31160003 from NWO. Dr R. Sinha received funding from NIDA
(PL31‐1DA024859‐01), NIH National Center for Research Resources
(UL1‐RR24925‐01), and NIAAA grant (R01‐AA013892). 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‐NIH). Dr. A.
Verdejo‐Garcia received support from the Australian Medical
Research Future Fund (MRF1141214). Dr M. Yücel received support
from the National Health and Medical Research Council Fellowship
grant 1117188 and the David Winston Turner Endowment Fund.

© 2019 Society for the Study of Addiction.

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10.1111/adb.12830

Cite this

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), Article e12830. https://doi.org/10.1111/adb.12830

@article{68c9aa40cc464f45851c85d2a9045a8b,

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.",

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 Y{\"u}cel and Thompson, \{Paul M\} and Patricia Conrod and Hugh Garavan",

note = "FUNDING INFORMATION 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‐DA014100. 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‐ZonMw VIDI grant 91713354. Dr O. Korucuoglu received support for the neuro‐ADAPT 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‐RR‐00865 (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 AA000125–04 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‐Santos received support from Plan Nacional sobre Drogas. Ministerio de Sanidad y Pol{\'i}tica Social grant PNSD:2011/050 and SGR:2014/1114. Dr L. Reneman received funding from the Netherlands Organisation for Health Research and Development 40‐00812‐98‐11002. Dr L. Schmaal and Dr D.J. Veltman received funding from ZonMW grant 31160003 from NWO. Dr R. Sinha received funding from NIDA (PL31‐1DA024859‐01), NIH National Center for Research Resources (UL1‐RR24925‐01), and NIAAA grant (R01‐AA013892). 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‐NIH). Dr. A. Verdejo‐Garcia received support from the Australian Medical Research Future Fund (MRF1141214). Dr M. Y{\"u}cel received support from the National Health and Medical Research Council Fellowship grant 1117188 and the David Winston Turner Endowment Fund. {\textcopyright} 2019 Society for the Study of Addiction.",

year = "2020",

month = nov,

doi = "10.1111/adb.12830",

language = "English",

volume = "25",

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, Yücel, 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. https://doi.org/10.1111/adb.12830

TY - JOUR

T1 - Subcortical surface morphometry in substance dependence

T2 - 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 - Yücel, Murat

AU - Thompson, Paul M

AU - Conrod, Patricia

AU - Garavan, Hugh

N1 - FUNDING INFORMATION 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‐DA014100. 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‐ZonMw VIDI grant 91713354. Dr O. Korucuoglu received support for the neuro‐ADAPT 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‐RR‐00865 (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 AA000125–04 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‐Santos received support from Plan Nacional sobre Drogas. Ministerio de Sanidad y Política Social grant PNSD:2011/050 and SGR:2014/1114. Dr L. Reneman received funding from the Netherlands Organisation for Health Research and Development 40‐00812‐98‐11002. Dr L. Schmaal and Dr D.J. Veltman received funding from ZonMW grant 31160003 from NWO. Dr R. Sinha received funding from NIDA (PL31‐1DA024859‐01), NIH National Center for Research Resources (UL1‐RR24925‐01), and NIAAA grant (R01‐AA013892). 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‐NIH). Dr. A. Verdejo‐Garcia received support from the Australian Medical Research Future Fund (MRF1141214). Dr M. Yücel received support from the National Health and Medical Research Council Fellowship grant 1117188 and the David Winston Turner Endowment Fund. © 2019 Society for the Study of Addiction.

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.

U2 - 10.1111/adb.12830

DO - 10.1111/adb.12830

M3 - Article

C2 - 31746534

SN - 1355-6215

VL - 25

JO - Addiction Biology

JF - Addiction Biology

IS - 6

M1 - e12830

ER -

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

Abstract

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