Mapping cortical and subcortical asymmetries in substance dependence: Findings from the ENIGMA Addiction Working Group

Zhipeng Cao; Jonatan Ottino-Gonzalez; Renata B Cupertino; Nathan Schwab; Colin Hoke; Orr Catherine; Janna Cousijn; Alain Dagher; John J Foxe; Anna E Goudriaan; Robert Hester; Kent Hutchison; Chiang-Shan R Li; Edythe D London; Valentina Lorenzetti; Maartje Luijten; Rocio Martin-Santos; Reza Momenan; Martin P Paulus; Lianne Schmaal; Rajita Sinha; Zsuzsika Sjoerds; Nadia Solowij; Dan J Stein; Elliot A Stein; Anne Uhlmann; Ruth J van Holst; Dick J Veltman; Reinout W Wiers; Murat Yücel; Sheng Zhang; Neda Jahanshad; Paul M Thompson; Patricia Conrod; Scott Mackey; Hugh Garavan

doi:10.1111/adb.13010

Mapping cortical and subcortical asymmetries in substance dependence: Findings from the ENIGMA Addiction Working Group

Zhipeng Cao, Jonatan Ottino-Gonzalez, Renata B Cupertino, Nathan Schwab, Colin Hoke, Orr Catherine, Janna Cousijn, Alain Dagher, John J Foxe, Anna E Goudriaan, Robert Hester, Kent Hutchison, Chiang-Shan R Li, Edythe D London, Valentina Lorenzetti, Maartje Luijten, Rocio Martin-Santos, Reza Momenan, Martin P Paulus, Lianne SchmaalRajita Sinha, Zsuzsika Sjoerds, Nadia Solowij, Dan J Stein, Elliot A Stein, Anne Uhlmann, Ruth J van Holst, Dick J Veltman, Reinout W Wiers, Murat Yücel, Sheng Zhang, Neda Jahanshad, Paul M Thompson, Patricia Conrod, Scott Mackey, Hugh Garavan

Clinical Psychology

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

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Abstract

Brain asymmetry reflects left-right hemispheric differentiation, which is a quantitative brain phenotype that develops with age and can vary with psychiatric diagnoses. Previous studies have shown that substance dependence is associated with altered brain structure and function. However, it is unknown whether structural brain asymmetries are different in individuals with substance dependence compared with nondependent participants. Here, a mega-analysis was performed using a collection of 22 structural brain MRI datasets from the ENIGMA Addiction Working Group. Structural asymmetries of cortical and subcortical regions were compared between individuals who were dependent on alcohol, nicotine, cocaine, methamphetamine, or cannabis (n = 1,796) and nondependent participants (n = 996). Substance-general and substance-specific effects on structural asymmetry were examined using separate models. We found that substance dependence was significantly associated with differences in volume asymmetry of the nucleus accumbens (NAcc; less rightward; Cohen's d = 0.15). This effect was driven by differences from controls in individuals with alcohol dependence (less rightward; Cohen's d = 0.10) and nicotine dependence (less rightward; Cohen's d = 0.11). These findings suggest that disrupted structural asymmetry in the NAcc may be a characteristic of substance dependence.

Original language	English
Article number	e13010
Journal	Addiction Biology
Volume	26
Issue number	5
DOIs	https://doi.org/10.1111/adb.13010
Publication status	Published - Sept 2021

Bibliographical note

Funding Information:
Z.C., J.O., R.B.C., N.C., and S.M. received support by NIDA grant R01DA047119, awarded to P.C. and H.G. R.W.W. received support for the Neuro-ADAPT study from VICI grant 453.08.01 from the Netherlands Organization for Scientific Research (NWO). L.S. and D.V. received funding from Netherlands Organization for Health Research and Development (ZonMW) grant 31160003 from NWO. N.S. and D.V. received funding from ZonMW grant 31160004 from NWO. A.E.G. and R.J.H. received funding from ZonMW grant 91676084 from NWO. M.L. and D.V. received funding from VIDI grant 016.08.322 from NWO, awarded to Ingmar H.?A. Franken. J.C. and A.E.G. received funding for the Cannabis Prospective study from ZonMW grant 31180002 from NWO. H.G. and J.F. received funds from NIDA grant R01-DA014100. C.R.L. received funding from NIH grants R01AA021449, R01DA023248, R21DA044749, and R21DA045189. S.Z. received funding from NIDA grant K25DA040032. E.L. was supported by NIDA grant R01 DA020726, the Thomas P. and Katherine K. Pike Chair in Addiction Studies, the Endowment from the Marjorie Greene Family Trust, and UCLA contract 20063287 with Philip Morris, USA. Data collection by R.M. was supported by the Intramural Clinical and Biological Research Program of the National Institute on Alcohol Abuse and Alcoholism (NIAAA). M.P.P. received funding from NIMH grant R01 DA018307. A.S. was supported by the Intramural Research Program of NIDA and NIH. R.S. received funds from NIDA (PL30-1DA024859-01), the NIH National Center for Research Resources (UL1-RR24925-01), and NIAAA (R01-AA013892). N.S. received funding from the Clive and Vera Ramaciotti Foundation for Biomedical Research National and Health and Medical Research Council Project grant 459111 and was supported by Australian Research Council Future Fellowship FT110100752. M.Y. was supported by National Health and Medical Research Council Fellowship 1117188 and the David Winston Turner Endowment Fund. P.T. was supported by NIH grants U54 EB020403 from the Big Data to Knowledge (BD2K) program, R01 MH116147, P41 EB015922, and R01 MH111671. N.J. was supported by NIH grants R01MH117601, R01AG059874, R01MH121246, P41EB015922, and R01MH116147.

Publisher Copyright:
© 2021 Society for the Study of Addiction

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Cao, Z., Ottino-Gonzalez, J., Cupertino, R. B., Schwab, N., Hoke, C., Catherine, O., Cousijn, J., Dagher, A., Foxe, J. J., Goudriaan, A. E., Hester, R., Hutchison, K., Li, C.-S. R., London, E. D., Lorenzetti, V., Luijten, M., Martin-Santos, R., Momenan, R., Paulus, M. P., ... Garavan, H. (2021). Mapping cortical and subcortical asymmetries in substance dependence: Findings from the ENIGMA Addiction Working Group. Addiction Biology, 26(5), Article e13010. https://doi.org/10.1111/adb.13010

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title = "Mapping cortical and subcortical asymmetries in substance dependence: Findings from the ENIGMA Addiction Working Group",

abstract = "Brain asymmetry reflects left-right hemispheric differentiation, which is a quantitative brain phenotype that develops with age and can vary with psychiatric diagnoses. Previous studies have shown that substance dependence is associated with altered brain structure and function. However, it is unknown whether structural brain asymmetries are different in individuals with substance dependence compared with nondependent participants. Here, a mega-analysis was performed using a collection of 22 structural brain MRI datasets from the ENIGMA Addiction Working Group. Structural asymmetries of cortical and subcortical regions were compared between individuals who were dependent on alcohol, nicotine, cocaine, methamphetamine, or cannabis (n = 1,796) and nondependent participants (n = 996). Substance-general and substance-specific effects on structural asymmetry were examined using separate models. We found that substance dependence was significantly associated with differences in volume asymmetry of the nucleus accumbens (NAcc; less rightward; Cohen's d = 0.15). This effect was driven by differences from controls in individuals with alcohol dependence (less rightward; Cohen's d = 0.10) and nicotine dependence (less rightward; Cohen's d = 0.11). These findings suggest that disrupted structural asymmetry in the NAcc may be a characteristic of substance dependence.",

author = "Zhipeng Cao and Jonatan Ottino-Gonzalez and Cupertino, {Renata B} and Nathan Schwab and Colin Hoke and Orr Catherine and Janna Cousijn and Alain Dagher and Foxe, {John J} and Goudriaan, {Anna E} and Robert Hester and Kent Hutchison and Li, {Chiang-Shan R} and London, {Edythe D} and Valentina Lorenzetti and Maartje Luijten and Rocio Martin-Santos and Reza Momenan and Paulus, {Martin P} and Lianne Schmaal and Rajita Sinha and Zsuzsika Sjoerds and Nadia Solowij and Stein, {Dan J} and Stein, {Elliot A} and Anne Uhlmann and {van Holst}, {Ruth J} and Veltman, {Dick J} and Wiers, {Reinout W} and Murat Y{\"u}cel and Sheng Zhang and Neda Jahanshad and Thompson, {Paul M} and Patricia Conrod and Scott Mackey and Hugh Garavan",

note = "Funding Information: Z.C., J.O., R.B.C., N.C., and S.M. received support by NIDA grant R01DA047119, awarded to P.C. and H.G. R.W.W. received support for the Neuro-ADAPT study from VICI grant 453.08.01 from the Netherlands Organization for Scientific Research (NWO). L.S. and D.V. received funding from Netherlands Organization for Health Research and Development (ZonMW) grant 31160003 from NWO. N.S. and D.V. received funding from ZonMW grant 31160004 from NWO. A.E.G. and R.J.H. received funding from ZonMW grant 91676084 from NWO. M.L. and D.V. received funding from VIDI grant 016.08.322 from NWO, awarded to Ingmar H.?A. Franken. J.C. and A.E.G. received funding for the Cannabis Prospective study from ZonMW grant 31180002 from NWO. H.G. and J.F. received funds from NIDA grant R01-DA014100. C.R.L. received funding from NIH grants R01AA021449, R01DA023248, R21DA044749, and R21DA045189. S.Z. received funding from NIDA grant K25DA040032. E.L. was supported by NIDA grant R01 DA020726, the Thomas P. and Katherine K. Pike Chair in Addiction Studies, the Endowment from the Marjorie Greene Family Trust, and UCLA contract 20063287 with Philip Morris, USA. Data collection by R.M. was supported by the Intramural Clinical and Biological Research Program of the National Institute on Alcohol Abuse and Alcoholism (NIAAA). M.P.P. received funding from NIMH grant R01 DA018307. A.S. was supported by the Intramural Research Program of NIDA and NIH. R.S. received funds from NIDA (PL30-1DA024859-01), the NIH National Center for Research Resources (UL1-RR24925-01), and NIAAA (R01-AA013892). N.S. received funding from the Clive and Vera Ramaciotti Foundation for Biomedical Research National and Health and Medical Research Council Project grant 459111 and was supported by Australian Research Council Future Fellowship FT110100752. M.Y. was supported by National Health and Medical Research Council Fellowship 1117188 and the David Winston Turner Endowment Fund. P.T. was supported by NIH grants U54 EB020403 from the Big Data to Knowledge (BD2K) program, R01 MH116147, P41 EB015922, and R01 MH111671. N.J. was supported by NIH grants R01MH117601, R01AG059874, R01MH121246, P41EB015922, and R01MH116147. Publisher Copyright: {\textcopyright} 2021 Society for the Study of Addiction",

year = "2021",

month = sep,

doi = "10.1111/adb.13010",

language = "English",

volume = "26",

journal = "Addiction Biology",

issn = "1355-6215",

publisher = "Wiley-Blackwell",

number = "5",

}

Cao, Z, Ottino-Gonzalez, J, Cupertino, RB, Schwab, N, Hoke, C, Catherine, O, Cousijn, J, Dagher, A, Foxe, JJ, Goudriaan, AE, Hester, R, Hutchison, K, Li, C-SR, London, ED, Lorenzetti, V, Luijten, M, Martin-Santos, R, Momenan, R, Paulus, MP, Schmaal, L, Sinha, R, Sjoerds, Z, Solowij, N, Stein, DJ, Stein, EA, Uhlmann, A, van Holst, RJ, Veltman, DJ, Wiers, RW, Yücel, M, Zhang, S, Jahanshad, N, Thompson, PM, Conrod, P, Mackey, S & Garavan, H 2021, 'Mapping cortical and subcortical asymmetries in substance dependence: Findings from the ENIGMA Addiction Working Group', Addiction Biology, vol. 26, no. 5, e13010. https://doi.org/10.1111/adb.13010

TY - JOUR

T1 - Mapping cortical and subcortical asymmetries in substance dependence

T2 - Findings from the ENIGMA Addiction Working Group

AU - Cao, Zhipeng

AU - Ottino-Gonzalez, Jonatan

AU - Cupertino, Renata B

AU - Schwab, Nathan

AU - Hoke, Colin

AU - Catherine, Orr

AU - Cousijn, Janna

AU - Dagher, Alain

AU - Foxe, John J

AU - Goudriaan, Anna E

AU - Hester, Robert

AU - Hutchison, Kent

AU - Li, Chiang-Shan R

AU - London, Edythe D

AU - Lorenzetti, Valentina

AU - Luijten, Maartje

AU - Martin-Santos, Rocio

AU - Momenan, Reza

AU - Paulus, Martin P

AU - Schmaal, Lianne

AU - Sinha, Rajita

AU - Sjoerds, Zsuzsika

AU - Solowij, Nadia

AU - Stein, Dan J

AU - Stein, Elliot A

AU - Uhlmann, Anne

AU - van Holst, Ruth J

AU - Veltman, Dick J

AU - Wiers, Reinout W

AU - Yücel, Murat

AU - Zhang, Sheng

AU - Jahanshad, Neda

AU - Thompson, Paul M

AU - Conrod, Patricia

AU - Mackey, Scott

AU - Garavan, Hugh

N1 - Funding Information: Z.C., J.O., R.B.C., N.C., and S.M. received support by NIDA grant R01DA047119, awarded to P.C. and H.G. R.W.W. received support for the Neuro-ADAPT study from VICI grant 453.08.01 from the Netherlands Organization for Scientific Research (NWO). L.S. and D.V. received funding from Netherlands Organization for Health Research and Development (ZonMW) grant 31160003 from NWO. N.S. and D.V. received funding from ZonMW grant 31160004 from NWO. A.E.G. and R.J.H. received funding from ZonMW grant 91676084 from NWO. M.L. and D.V. received funding from VIDI grant 016.08.322 from NWO, awarded to Ingmar H.?A. Franken. J.C. and A.E.G. received funding for the Cannabis Prospective study from ZonMW grant 31180002 from NWO. H.G. and J.F. received funds from NIDA grant R01-DA014100. C.R.L. received funding from NIH grants R01AA021449, R01DA023248, R21DA044749, and R21DA045189. S.Z. received funding from NIDA grant K25DA040032. E.L. was supported by NIDA grant R01 DA020726, the Thomas P. and Katherine K. Pike Chair in Addiction Studies, the Endowment from the Marjorie Greene Family Trust, and UCLA contract 20063287 with Philip Morris, USA. Data collection by R.M. was supported by the Intramural Clinical and Biological Research Program of the National Institute on Alcohol Abuse and Alcoholism (NIAAA). M.P.P. received funding from NIMH grant R01 DA018307. A.S. was supported by the Intramural Research Program of NIDA and NIH. R.S. received funds from NIDA (PL30-1DA024859-01), the NIH National Center for Research Resources (UL1-RR24925-01), and NIAAA (R01-AA013892). N.S. received funding from the Clive and Vera Ramaciotti Foundation for Biomedical Research National and Health and Medical Research Council Project grant 459111 and was supported by Australian Research Council Future Fellowship FT110100752. M.Y. was supported by National Health and Medical Research Council Fellowship 1117188 and the David Winston Turner Endowment Fund. P.T. was supported by NIH grants U54 EB020403 from the Big Data to Knowledge (BD2K) program, R01 MH116147, P41 EB015922, and R01 MH111671. N.J. was supported by NIH grants R01MH117601, R01AG059874, R01MH121246, P41EB015922, and R01MH116147. Publisher Copyright: © 2021 Society for the Study of Addiction

PY - 2021/9

Y1 - 2021/9

N2 - Brain asymmetry reflects left-right hemispheric differentiation, which is a quantitative brain phenotype that develops with age and can vary with psychiatric diagnoses. Previous studies have shown that substance dependence is associated with altered brain structure and function. However, it is unknown whether structural brain asymmetries are different in individuals with substance dependence compared with nondependent participants. Here, a mega-analysis was performed using a collection of 22 structural brain MRI datasets from the ENIGMA Addiction Working Group. Structural asymmetries of cortical and subcortical regions were compared between individuals who were dependent on alcohol, nicotine, cocaine, methamphetamine, or cannabis (n = 1,796) and nondependent participants (n = 996). Substance-general and substance-specific effects on structural asymmetry were examined using separate models. We found that substance dependence was significantly associated with differences in volume asymmetry of the nucleus accumbens (NAcc; less rightward; Cohen's d = 0.15). This effect was driven by differences from controls in individuals with alcohol dependence (less rightward; Cohen's d = 0.10) and nicotine dependence (less rightward; Cohen's d = 0.11). These findings suggest that disrupted structural asymmetry in the NAcc may be a characteristic of substance dependence.

AB - Brain asymmetry reflects left-right hemispheric differentiation, which is a quantitative brain phenotype that develops with age and can vary with psychiatric diagnoses. Previous studies have shown that substance dependence is associated with altered brain structure and function. However, it is unknown whether structural brain asymmetries are different in individuals with substance dependence compared with nondependent participants. Here, a mega-analysis was performed using a collection of 22 structural brain MRI datasets from the ENIGMA Addiction Working Group. Structural asymmetries of cortical and subcortical regions were compared between individuals who were dependent on alcohol, nicotine, cocaine, methamphetamine, or cannabis (n = 1,796) and nondependent participants (n = 996). Substance-general and substance-specific effects on structural asymmetry were examined using separate models. We found that substance dependence was significantly associated with differences in volume asymmetry of the nucleus accumbens (NAcc; less rightward; Cohen's d = 0.15). This effect was driven by differences from controls in individuals with alcohol dependence (less rightward; Cohen's d = 0.10) and nicotine dependence (less rightward; Cohen's d = 0.11). These findings suggest that disrupted structural asymmetry in the NAcc may be a characteristic of substance dependence.

UR - http://www.scopus.com/inward/record.url?scp=85099801261&partnerID=8YFLogxK

U2 - 10.1111/adb.13010

DO - 10.1111/adb.13010

M3 - Article

C2 - 33508888

SN - 1355-6215

VL - 26

JO - Addiction Biology

JF - Addiction Biology

IS - 5

M1 - e13010

ER -

Mapping cortical and subcortical asymmetries in substance dependence: Findings from the ENIGMA Addiction Working Group

Abstract

Bibliographical note

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