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Cannabis Use and Brain Volume in Adolescent and Young Adult Cannabis Users: Effects Moderated by Sex and Aerobic Fitness

Published online by Cambridge University Press:  15 July 2021

Ryan M. Sullivan Open the ORCID record for Ryan M. Sullivan [Opens in a new window] ,
Alexander L. Wallace Open the ORCID record for Alexander L. Wallace [Opens in a new window] ,
Natasha E. Wade Open the ORCID record for Natasha E. Wade [Opens in a new window] ,
Ann M. Swartz  and
Krista M. Lisdahl
Ryan M. Sullivan
Affiliation:
Department of Psychology, University of Wisconsin-Milwaukee, 2441 E Hartford Avenue, Milwaukee, WI53211, USA
Alexander L. Wallace
Affiliation:
Department of Psychology, University of Wisconsin-Milwaukee, 2441 E Hartford Avenue, Milwaukee, WI53211, USA
Natasha E. Wade
Affiliation:
Department of Psychiatry, UC San Diego School of Medicine, 9500 Gilman Drive, La Jolla, CA92093, USA
Ann M. Swartz
Affiliation:
Department of Kinesiology, University of Wisconsin-Milwaukee, 2400 E Hartford Avenue, Milwaukee, WI53211, USA
Krista M. Lisdahl*
Affiliation:
Department of Psychology, University of Wisconsin-Milwaukee, 2441 E Hartford Avenue, Milwaukee, WI53211, USA
*
*Correspondence and reprint requests to: Krista M. Lisdahl, Department of Psychology, University of Wisconsin-Milwaukee, 2441 East Hartford Ave, Milwaukee, WI 53211, USA. Phone: +1 414-229-7159; Fax: +1 414-229-5219. E-mail: krista.medina@gmail.com
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Abstract

Objectives:

Studies examining the impact of adolescent and young adult cannabis use on structural outcomes have been heterogeneous. One already-identified moderator is sex, while a novel potential moderator is extent of aerobic fitness. Here, we sought to investigate the associations of cannabis use, sex, and aerobic fitness levels on brain volume. Second, we explored brain–behavior relationships to interpret these findings.

Methods:

Seventy-four adolescents and young adults (36 cannabis users and 38 controls) underwent 3 weeks of monitored cannabis abstinence, aerobic fitness testing, structural neuroimaging, and neuropsychological testing. Linear regressions examined cannabis use and its interaction with sex and aerobic fitness on whole-brain cortical volume and subcortical regions of interests.

Results:

No main-effect differences between cannabis users and nonusers were observed; however, cannabis-by-sex interactions identified differences in frontal, temporal, and paracentral volumes. Female cannabis users generally exhibited greater volume while male users exhibited less volume compared to same-sex controls. Positive associations between aerobic fitness and frontal, parietal, cerebellum, and caudate volumes were observed. Cannabis-by-fitness interaction was linked with left superior temporal volume. Preliminary brain–behavior correlations revealed that abnormal volumes were not advantageous in either male or female cannabis users.

Conclusions:

Aerobic fitness was linked with greater brain volume and sex moderated the effect of cannabis use on volume; preliminary brain–behavior correlations revealed that differences in cannabis users were not linked with advantageous cognitive performance. Implications of sex-specific subtleties and mechanisms of aerobic fitness require large-scale investigation. Furthermore, present findings and prior literature on aerobic exercise warrant examinations of aerobic fitness interventions that aimed at improving neurocognitive health in substance-using youth.

Keywords

CannabisPhysical fitnessSex factorsGray matterNeuroimagingMarijuana use
Type
Regular Research
Information
Journal of the International Neuropsychological Society , Volume 27 , Special Issue 6: Clarifying the Complexities of Cannabis and Cognition , July 2021 , pp. 607 - 620
Copyright
Copyright © INS. Published by Cambridge University Press, 2021

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References

REFERENCES

Arbuthnott, K., & Frank, J. (2010). Trail Making Test, Part B as a measure of executive control: Validation using a set-switching paradigm. Journal of Clinical and Experimental Neuropsychology, 22(4), 518–528. doi: 10.1076/1380-3395(200008)22:4;1-0;ft518 CrossRefGoogle Scholar
Ashtari, M., Avants, B., Cyckowski, L., Cervellione, K.L., Roofeh, D., Cook, P., … Kumra, S. (2011). Medial temporal structures and memory functions in adolescents with heavy cannabis use. Journal of Psychiatric Research, 45(8), 1055–1066. doi: 10.1016/j.jpsychires.2011.01.004 CrossRefGoogle ScholarPubMed
Batalla, A., Bhattacharyya, S., Yucel, M., Fusar-Poli, P., Crippa, J.A., Nogue, S., … Martin-Santos, R. (2013). Structural and functional imaging studies in chronic cannabis users: a systematic review of adolescent and adult findings. PLoS One, 8(2), e55821. doi: 10.1371/journal.pone.0055821 CrossRefGoogle ScholarPubMed
Bava, S., Jacobus, J., Mahmood, O., Yang, T.T., & Tapert, S.F. (2010). Neurocognitive correlates of white matter quality in adolescent substance users. Brain and Cognitive, 72(3), 347–354. doi: 10.1016/j.bandc.2009.10.012 CrossRefGoogle ScholarPubMed
Benjamini, Y., & Hochberg, Y. (1995). Controlling the false discovery rate: A practical and powerful approach to multiple testing. Journal of the Royal Statistical Society: Series B (Methodological), 57(1), 289–300. doi: 10.1111/j.2517-6161.1995.tb02031.x Google Scholar
Bherer, L., Erickson, K.I., & Liu-Ambrose, T. (2013). A review of the effects of physical activity and exercise on cognitive and brain functions in older adults. Journal of Aging Research, 2013, 657508. doi: 10.1155/2013/657508 Google ScholarPubMed
Brown, S.A., Myers, M.G., Lippke, L., Tapert, S.F., Stewart, D.G., & Vik, P.W. (1998). Psychometric evaluation of the Customary Drinking and Drug Use Record (CDDR): a measure of adolescent alcohol and drug involvement. J Stud Alcohol, 59(4), 427–438. doi: 10.15288/jsa.1998.59.427 CrossRefGoogle ScholarPubMed
Buchowski, M.S., Meade, N.N., Charboneau, E., Park, S., Dietrich, M.S., Cowan, R.L., & Martin, P.R. (2011). Aerobic exercise training reduces cannabis craving and use in non-treatment seeking cannabis-dependent adults. PLoS One, 6(3), e17465. doi: 10.1371/journal.pone.0017465 CrossRefGoogle ScholarPubMed
Burston, J.J., Wiley, J.L., Craig, A.A., Selley, D.E., & Sim-Selley, L.J. (2010). Regional enhancement of cannabinoid CB茡 receptor desensitization in female adolescent rats following repeated delta-tetrahydrocannabinol exposure. British Journal of Pharmacology, 161(1), 103–112. Doi: 10.1111/j.1476-5381.2010.00870.x CrossRefGoogle ScholarPubMed
Carliner, H., Brown, Q.L., Sarvet, A.L., & Hasin, D.S. (2017). Cannabis use, attitudes, and legal status in the U.S.: A review. Preventive Medicine, 104, 13–23. doi: 10.1016/j.ypmed.2017.07.008 CrossRefGoogle ScholarPubMed
Chaddock, L., Pontifex, M.B., Hillman, C.H., & Kramer, A.F. (2011). A review of the relation of aerobic fitness and physical activity to brain structure and function in children. Journal of the International Neuropsychological Society, 17(6), 975–985. doi: 10.1017/S1355617711000567 CrossRefGoogle ScholarPubMed
Cheetham, A., Allen, N.B., Whittle, S., Simmons, J.G., Yucel, M., & Lubman, D.I. (2012). Orbitofrontal volumes in early adolescence predict initiation of cannabis use: a 4-year longitudinal and prospective study. Biological Psychiatry, 71(8), 684–692. doi: 10.1016/j.biopsych.2011.10.029 CrossRefGoogle ScholarPubMed
Crane, N.A., Schuster, R.M., Fusar-Poli, P., & Gonzalez, R. (2013). Effects of cannabis on neurocognitive functioning: recent advances, neurodevelopmental influences, and sex differences. Neuropsychology Review, 23(2), 117–137. doi: 10.1007/s11065-012-9222-1 CrossRefGoogle ScholarPubMed
Crane, N.A., Schuster, R.M., Mermelstein, R.J., & Gonzalez, R. (2015). Neuropsychological sex differences associated with age of initiated use among young adult cannabis users. Journal of Clinical Experimental Neuropsychology, 37(4), 389–401. doi: 10.1080/13803395.2015.1020770 CrossRefGoogle ScholarPubMed
Crippa, J.A., Zuardi, A.W., Martin-Santos, R., Bhattacharyya, S., Atakan, Z., McGuire, P., & Fusar-Poli, P. (2009). Cannabis and anxiety: a critical review of the evidence. Human Psychopharmacology, 24(7), 515–523. doi: 10.1002/hup.1048 CrossRefGoogle Scholar
Cuttler, C., Mischley, L.K., & Sexton, M. (2016). Sex differences in cannabis use and effects: A cross-sectional survey of cannabis users. Cannabis and Cannabinoid Research, 1(1), 166–175. doi: 10.1089/can.2016.0010 CrossRefGoogle ScholarPubMed
Diehr, M.C., Heaton, R.K., Miller, W., & Grant, I. (1998). The Paced Auditory Serial Addition Task (PASAT): Norms for age, education, and ethnicity. Assessment, 5(4), 375–387. doi: 10.1177/107319119800500407 CrossRefGoogle ScholarPubMed
Eggan, S.M., & Lewis, D.A. (2007). Immunocytochemical distribution of the cannabinoid CB1 receptor in the primate neocortex: A regional and laminar analysis. Cerebral Cortex, 17(1), 175–191. doi: 10.1093/cercor/bhj136 CrossRefGoogle ScholarPubMed
Eggan, S.M., Mizoguchi, Y., Stoyak, S.R., & Lewis, D.A. (2010). Development of cannabinoid 1 receptor protein and messenger RNA in monkey dorsolateral prefrontal cortex. Cerebral Cortex, 20(5), 1164–1174. doi: 10.1093/cercor/bhp179 CrossRefGoogle ScholarPubMed
Filbey, F.M., Schacht, J.P., Myers, U.S., Chavez, R.S., & Hutchison, K.E. (2010). Individual and additive effects of the CNR1 and FAAH genes on brain response to marijuana cues. Neuropsychopharmacology, 35(4), 967–975. doi: 10.1038/npp.2009.200 CrossRefGoogle ScholarPubMed
Fleenor, B.S., Marshall, K.D., Durrant, J.R., Lesniewski, L.A., & Seals, D.R. (2010). Arterial stiffening with ageing is associated with transforming growth factor-beta1-related changes in adventitial collagen: reversal by aerobic exercise. The Journal of Physiology, 588(Pt 20), 3971–3982. doi: 10.1113/jphysiol.2010.194753 CrossRefGoogle ScholarPubMed
Fogelholm, M., Malmberg, J., Suni, J., Santtila, M., Kyrolainen, H., Mantysaari, M., & Oja, P. (2006). International Physical Activity Questionnaire: Validity against fitness. Medicine & Science in Sports & Exercise, 38(4), 753–760. doi: 10.1249/01.mss.0000194075.16960.20 CrossRefGoogle ScholarPubMed
Giedd, J.N., Blumenthal, J., Jeffries, N.O., Castellanos, F.X., Liu, H., Zijdenbos, A., … Rapoport, J.L. (1999). Brain development during childhood and adolescence: A longitudinal MRI study. Nature Neuroscience, 2(10), 861–863. doi: 10.1038/13158 CrossRefGoogle ScholarPubMed
Gonzalez, R., Pacheco-Colon, I., Duperrouzel, J.C., & Hawes, S.W. (2017). Does cannabis use cause declines in neuropsychological functioning? A review of longitudinal studies. Journal of the International Neuropsychological Society, 23(9–10), 893–902. doi: 10.1017/S1355617717000789 CrossRefGoogle ScholarPubMed
Goodwin, R.S., Darwin, W.D., Chiang, C.N., Shih, M., Li, S.H., & Huestis, M.A. (2008). Urinary elimination of 11-nor-9-carboxy-delta9-tetrahydrocannnabinol in cannabis users during continuously monitored abstinence. Journal of Analytical Toxicology, 32(8), 562–569. doi: 10.1093/jat/32.8.562 CrossRefGoogle ScholarPubMed
Greve, D.N., & Fischl, B. (2018). False positive rates in surface-based anatomical analysis. NeuroImage, 171, 6–14. doi: 10.1016/j.neuroimage.2017.12.072 CrossRefGoogle ScholarPubMed
Han, B., Compton, W.M., Blanco, C., & Jones, C.M. (2019). Time since first cannabis use and 12-month prevalence of cannabis use disorder among youth and emerging adults in the United States. Addiction, 114(4), 698–707. doi: 10.1111/add.14511 CrossRefGoogle ScholarPubMed
Herting, M.M., & Chu, X. (2017). Exercise, cognition, and the adolescent brain. Birth Defects Research, 109(20), 1672–1679. doi: 10.1002/bdr2.1178 CrossRefGoogle ScholarPubMed
Herting, M.M., & Keenan, M.F. (2017). Exercise and the developing brain in children and adolescents. In Watson, R. R. (Ed.), Physical activity and the aging brain (pp. 13–19). Cambridge, MA: Academic Press.CrossRefGoogle Scholar
Herting, M.M., & Nagel, B.J. (2013). Differences in brain activity during a verbal associative memory encoding task in high- and low-fit adolescents. The Journal of Cognitive Neuroscience, 25(4), 595–612. doi: 10.1162/jocn_a_00344 CrossRefGoogle ScholarPubMed
Heyman, E., Gamelin, F.X., Goekint, M., Piscitelli, F., Roelands, B., Leclair, E., … Meeusen, R. (2012). Intense exercise increases circulating endocannabinoid and BDNF levels in humans--possible implications for reward and depression. Psychoneuroendocrinology, 37(6), 844–851. doi: 10.1016/j.psyneuen.2011.09.017 CrossRefGoogle ScholarPubMed
Higuera-Matas, A., Botreau, F., Del Olmo, N., Miguens, M.,Olias, O., Montoya, G.L., … Ambrosio, E. (2010). Periadolescent exposure to cannabinoids alters the striatal and hippocampal dopaminergic system in the adult rat brain. European College of Neuropsychopharmacology, 20(12), 895–906. doi: 10.1016/j.euroneuro.2010.06.017 CrossRefGoogle ScholarPubMed
Hillard, C.J. (2018). Circulating endocannabinoids: From whence do they come and where are they going? Neuropsychopharmacology, 43(1), 155–172. doi: 10.1038/npp.2017.130 CrossRefGoogle ScholarPubMed
Hirvonen, J., Goodwin, R.S., Li, C.T., Terry, G.E., Zoghbi, S.S., Morse, C., … Innis, R.B. (2012). Reversible and regionally selective downregulation of brain cannabinoid CB1 receptors in chronic daily cannabis smokers. Molecular Psychiatry, 17(6), 642–649. doi: 10.1038/mp.2011.82 CrossRefGoogle ScholarPubMed
Howley, E.T., Bassett, D.R. Jr., & Welch, H.G. (1995). Criteria for maximal oxygen uptake: review and commentary. Medicine & Science in Sports & Exercise, 27(9), 1292–1301. Retrieved from https://www.ncbi.nlm.nih.gov/pubmed/8531628 CrossRefGoogle ScholarPubMed
Huang, T., Larsen, K.T., Ried-Larsen, M., Moller, N.C., & Andersen, L.B. (2014). The effects of physical activity and exercise on brain-derived neurotrophic factor in healthy humans: A review. Scandinavian Journal of Medicine & Science in Sports, 24(1), 1–10. doi: 10.1111/sms.12069 CrossRefGoogle ScholarPubMed
Hwang, J., Castelli, D.M., & Gonzalez-Lima, F. (2017). The positive cognitive impact of aerobic fitness is associated with peripheral inflammatory and brain-derived neurotrophic biomarkers in young adults. Physiology and Behavior, 179, 75–89. doi: 10.1016/j.physbeh.2017.05.011 CrossRefGoogle ScholarPubMed
Jackson, N.J., Isen, J.D., Khoddam, R., Irons, D., Tuvblad, C., Iacono, W.G., … Baker, L.A. (2016). Impact of adolescent marijuana use on intelligence: Results from two longitudinal twin studies. Proceedings of the National Academy of Sciences of U S A, 113(5), E500–508. doi: 10.1073/pnas.1516648113 CrossRefGoogle ScholarPubMed
Jacobus, J., Goldenberg, D., Wierenga, C.E., Tolentino, N.J., Liu, T.T., & Tapert, S.F. (2012). Altered cerebral blood flow and neurocognitive correlates in adolescent cannabis users. Psychopharmacology (Berl), 222(4), 675–684. doi: 10.1007/s00213-012-2674-4 CrossRefGoogle ScholarPubMed
Johnston, L.D., Miech, R.A., O’Malley, P.M., Bachman, J.G., Schulenberg, J.E., & Patrick, M.E. (2020). Monitoring the Future national survey results on drug use 1975–2019: Overview, key findings on adolescent drug use. Ann Arbor: Institute for Social Research, The University of Michigan.Google Scholar
Khan, S.S., Secades-Villa, R., Okuda, M., Wang, S., Perez-Fuentes, G., Kerridge, B.T., & Blanco, C. (2013). Gender differences in cannabis use disorders: results from the National Epidemiologic Survey of Alcohol and Related Conditions. Drug and Alcohol Dependence, 130(1–3), 101–108. doi: 10.1016/j.drugalcdep.2012.10.015 CrossRefGoogle ScholarPubMed
Koltyn, K.F., Brellenthin, A.G., Cook, D.B., Sehgal, N., & Hillard, C. (2014). Mechanisms of exercise-induced hypoalgesia. The Journal of Pain, 15(12), 1294–1304. doi: 10.1016/j.jpain.2014.09.006 CrossRefGoogle ScholarPubMed
Lee, T.M., Wong, M.L., Lau, B.W., Lee, J.C., Yau, S.Y., & So, K.F. (2014). Aerobic exercise interacts with neurotrophic factors to predict cognitive functioning in adolescents. Psychoneuroendocrinology, 39, 214–224. doi: 10.1016/j.psyneuen.2013.09.019 CrossRefGoogle ScholarPubMed
Lenroot, R.K., Gogtay, N., Greenstein, D.K., Wells, E.M., Wallace, G.L., Clasen, L.S., … Giedd, J.N. (2007). Sexual dimorphism of brain developmental trajectories during childhood and adolescence. NeuroImage, 36(4), 1065–1073. doi: 10.1016/j.neuroimage.2007.03.053 CrossRefGoogle ScholarPubMed
Lev-Ran, S., Roerecke, M., Le Foll, B., George, T.P., McKenzie, K., & Rehm, J. (2014). The association between cannabis use and depression: a systematic review and meta-analysis of longitudinal studies. Psychological Medicine, 44(4), 797–810. doi: 10.1017/S0033291713001438 CrossRefGoogle ScholarPubMed
Lezak, M.D., Howieson, D.B., Loring, D.W., & Fischer, J.S. (2004). Neuropsychological assessment. New York: Oxford University Press.Google Scholar
Lisdahl, K.M., Gilbart, E.R., Wright, N.E., & Shollenbarger, S. (2013). Dare to delay? The impacts of adolescent alcohol and marijuana use onset on cognition, brain structure, and function. Frontiers in Psychiatry, 4(53), 53. doi: 10.3389/fpsyt.2013.00053 CrossRefGoogle Scholar
Lisdahl, K.M., & Price, J.S. (2012). Increased marijuana use and gender predict poorer cognitive functioning in adolescents and emerging adults. Journal of the International Neuropsychological Society, 18(4), 678–688. doi: 10.1017/S1355617712000276 CrossRefGoogle ScholarPubMed
Lisdahl, K.M., Sher, K.J., Conway, K.P., Gonzalez, R., Feldstein Ewing, S.W., Nixon, S.J., … Heitzeg, M. (2018). Adolescent brain cognitive development (ABCD) study: Overview of substance use assessment methods. Developmental Cognitive Neuroscience, 32, 80–96. doi: 10.1016/j.dcn.2018.02.007 CrossRefGoogle ScholarPubMed
Lisdahl, K.M., Tamm, L., Epstein, J.N., Jernigan, T., Molina, B.S., Hinshaw, S.P., … Group, M.T.A.N. (2016). The impact of ADHD persistence, recent cannabis use, and age of regular cannabis use onset on subcortical volume and cortical thickness in young adults. Drug and Alcohol Dependence, 161, 135–146. doi: 10.1016/j.drugalcdep.2016.01.032 CrossRefGoogle ScholarPubMed
Lisdahl, K.M., Wright, N.E., Kirchner-Medina, C., Maple, K.E., & Shollenbarger, S. (2014). Considering cannabis: The Effects of regular cannabis use on neurocognition in adolescents and young adults. Current Addiction Reports, 1(2), 144–156. doi: 10.1007/s40429-014-0019-6 CrossRefGoogle ScholarPubMed
Lorenzetti, V., Chye, Y., Silva, P., Solowij, N., & Roberts, C.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), 59–71. doi: 10.1007/s00406-019-00979-1 CrossRefGoogle ScholarPubMed
Maple, K.E., Thomas, A.M., Kangiser, M.M., & Lisdahl, K.M. (2019). Anterior cingulate volume reductions in abstinent adolescent and young adult cannabis users: Association with affective processing deficits. Psychiatry Research: Neuroimaging, 288, 51–59. doi: 10.1016/j.pscychresns.2019.04.011 CrossRefGoogle Scholar
Matochik, J.A., Eldreth, D.A., Cadet, J.L., & Bolla, K.I. (2005). Altered brain tissue composition in heavy marijuana users. Drug and Alcohol Dependence, 77(1), 23–30. doi: 10.1016/j.drugalcdep.2004.06.011 CrossRefGoogle ScholarPubMed
McQueeny, T., Padula, C.B., Price, J., Medina, K.L., Logan, P., & Tapert, S.F. (2011). Gender effects on amygdala morphometry in adolescent marijuana users. Behavioural Brain Research, 224(1), 128–134. doi: 10.1016/j.bbr.2011.05.031 CrossRefGoogle ScholarPubMed
Mechoulam, R., & Parker, L.A. (2013). The endocannabinoid system and the brain. Annual Review of Psychology, 64(1), 21–47. doi: 10.1146/annurev-psych-113011-143739 CrossRefGoogle ScholarPubMed
Medina, K.L., McQueeny, T., Nagel, B.J., Hanson, K.L., Yang, T.T., & Tapert, S.F. (2009). Prefrontal cortex morphometry in abstinent adolescent marijuana users: Subtle gender effects. Addiction Biology, 14(4), 457–468. doi: 10.1111/j.1369-1600.2009.00166.x CrossRefGoogle ScholarPubMed
Medina, K.L., Nagel, B.J., & Tapert, S.F. (2010). Abnormal cerebellar morphometry in abstinent adolescent marijuana users. Psychiatry Research, 182(2), 152–159. doi: 10.1016/j.pscychresns.2009.12.004 CrossRefGoogle ScholarPubMed
Medina, K.L., Schweinsburg, A.D., Cohen-Zion, M., Nagel, B.J., & Tapert, S.F. (2007). Effects of alcohol and combined marijuana and alcohol use during adolescence on hippocampal volume and asymmetry. Neurotoxicology and Teratology, 29(1), 141–152. doi: 10.1016/j.ntt.2006.10.010 CrossRefGoogle ScholarPubMed
Meier, M.H., Caspi, A., Ambler, A., Harrington, H., Houts, R., Keefe, R.S., … Moffitt, T.E. (2012). Persistent cannabis users show neuropsychological decline from childhood to midlife. Proceedings of the National Academy of Sciences of U S A, 109(40), E2657–2664. doi: 10.1073/pnas.1206820109 CrossRefGoogle ScholarPubMed
Meyer, J.D., Crombie, K.M., Cook, D.B., Hillard, C.J., & Koltyn, K.F. (2019). Serum Endocannabinoid and mood changes after exercise in major depressive disorder. Medicine & Science in Sports & Exercise, 51(9), 1909–1917. doi: 10.1249/MSS.0000000000002006 CrossRefGoogle ScholarPubMed
Mills, K.L., Goddings, A.L., Herting, M.M., Meuwese, R., Blakemore, S.J., Crone, E.A., … Tamnes, C.K. (2016). Structural brain development between childhood and adulthood: Convergence across four longitudinal samples. NeuroImage, 141, 273–281. doi: 10.1016/j.neuroimage.2016.07.044 CrossRefGoogle ScholarPubMed
Nokia, M.S., Lensu, S., Ahtiainen, J.P., Johansson, P.P., Koch, L.G., Britton, S.L., & Kainulainen, H. (2016). Physical exercise increases adult hippocampal neurogenesis in male rats provided it is aerobic and sustained. The Journal of Physiology, 594(7), 1855–1873. doi: 10.1113/JP271552 CrossRefGoogle ScholarPubMed
Ortega, F.B., Campos, D., Cadenas-Sanchez, C., Altmae, S., Martinez-Zaldivar, C., Martin-Matillas, M., … Campoy, C. (2019). Physical fitness and shapes of subcortical brain structures in children. British Journal of Nutrition, 122(s1), S49–S58. doi: 10.1017/S0007114516001239 CrossRefGoogle ScholarPubMed
Palmer, C.E., Zhao, W., Loughnan, R., Zou, J., Fan, C.C., Thompson, W.K., … Jernigan, T.L. (2020). Fluid and crystallised intelligence are associated with distinct regionalisation patterns of cortical morphology. bioRxiv, doi: 10.1101/2020.02.13.948596 CrossRefGoogle Scholar
Pereira, A.C., Huddleston, D.E., Brickman, A.M., Sosunov, A.A., Hen, R., McKhann, G.M., … Small, S.A. (2007). An invivo correlate of exercise-induced neurogenesis in the adult dentate gyrus. Proceedings National Academy of Sciences of the U S A, 104(13), 5638–5643. doi: 10.1073/pnas.0611721104 CrossRefGoogle Scholar
Pescatello, L. S. (2014). ACSM’s guidelines for exercise testing and prescription (9th ed.). Philadelphia: Wolters Kluwer/Lippincott Williams & Wilkins Health.Google Scholar
Price, J.S., McQueeny, T., Shollenbarger, S., Browning, E L., Wieser, J., & Lisdahl, K M. (2015). Effects of marijuana use on prefrontal and parietal volumes and cognition in emerging adults. Psychopharmacology (Berl), 232(16), 2939–2950. doi: 10.1007/s00213-015-3931-0 CrossRefGoogle ScholarPubMed
R Development Core Team. (2010). R: A language and environment for statistical computing (Version 3.5.2). Vienna, Austria: R Foundation for Statistical Computing. Retrieved from http://www.R-project.org Google Scholar
Ramseyer, G.C. (2015). Testing the difference between dependent correlations using the Fisher z. The Journal of Experimental Education, 47(4), 307–310. doi: 10.1080/00220973.1979.11011698 CrossRefGoogle Scholar
Renard, J., Rushlow, W.J., & Laviolette, S.R. (2016). What Can rats tell us about adolescent cannabis exposure? Insights from preclinical research. The Canadian Journal of Psychiatry, 61(6), 328–334. doi: 10.1177/0706743716645288 CrossRefGoogle ScholarPubMed
Rodriguez de Fonseca, F., Ramos, J.A., Bonnin, A., & Fernandez-Ruiz, J J. (1993). Presence of cannabinoid binding sites in the brain from early postnatal ages. Neuroreport, 4(2), 135–138. doi: 10.1097/00001756-199302000-00005 CrossRefGoogle ScholarPubMed
Rubino, T., & Parolaro, D. (2015). Sex-dependent vulnerability to cannabis abuse in adolescence. Frontiers of Psychiatry, 6(56), 56. doi: 10.3389/fpsyt.2015.00056 CrossRefGoogle ScholarPubMed
Rubino, T., Vigano, D., Realini, N., Guidali, C., Braida, D., Capurro, V., … Parolaro, D. (2008). Chronic delta 9-tetrahydrocannabinol during adolescence provokes sex-dependent changes in the emotional profile in adult rats: behavioral and biochemical correlates. Neuropsychopharmacology, 33(11), 2760–2771. doi: 10.1038/sj.npp.1301664 CrossRefGoogle ScholarPubMed
Ruff, R.M., Niemann, H., Allen, C.C., Farrow, C.E., & Wylie, T. (1992). The Ruff 2 and 7 Selective Attention Test: A neuropsychological application. Perceptual and Motor Skills, 75(3 Pt 2), 1311–1319. doi: 10.2466/pms.1992.75.3f.1311 CrossRefGoogle ScholarPubMed
Sanchez-Cubillo, I., Perianez, J.A., Adrover-Roig, D., Rodriguez-Sanchez, J.M., Rios-Lago, M., Tirapu, J., & Barcelo, F. (2009). Construct validity of the Trail Making Test: Role of task-switching, working memory, inhibition/interference control, and visuomotor abilities. Journal of the International Neuropsychological Society, 15(3), 438–450. doi: 10.1017/S1355617709090626 CrossRefGoogle ScholarPubMed
Schulenberg, J.E., Johnston, L.D., O’Malley, P.M., Bachman, J.G., Miech, R.A., & Patrick, M.E. (2019). Monitoring the Future national survey results on drug use, 1975–2018: Volume II, College students and adults ages 19–60. Ann Arbor: Institute for Social Research. Retrieved from http://monitoringthefuture.org/pubs.html#monographs CrossRefGoogle Scholar
Schwarb, H., Johnson, C.L., Daugherty, A.M., Hillman, C.H., Kramer, A.F., Cohen, N.J., & Barbey, A.K. (2017). Aerobic fitness, hippocampal viscoelasticity, and relational memory performance. NeuroImage, 153, 179–188. doi: 10.1016/j.neuroimage.2017.03.061 CrossRefGoogle ScholarPubMed
Schwartz, D.H., Dickie, E., Pangelinan, M.M., Leonard, G., Perron, M., Pike, G.B., … Paus, T. (2014). Adiposity is associated with structural properties of the adolescent brain. NeuroImage, 103, 192–201. doi: 10.1016/j.neuroimage.2014.09.030 CrossRefGoogle ScholarPubMed
Scott, J.C., Slomiak, S.T., Jones, J.D., Rosen, A.F.G., Moore, T.M., & Gur, R.C. (2018). Association of cannabis with cognitive functioning in adolescents and young adults: A Systematic review and meta-analysis. JAMA Psychiatry, 75(6), 585–595. doi: 10.1001/jamapsychiatry.2018.0335 CrossRefGoogle Scholar
Shollenbarger, S.G., Price, J., Wieser, J., & Lisdahl, K. (2015). Poorer frontolimbic white matter integrity is associated with chronic cannabis use, FAAH genotype, and increased depressive and apathy symptoms in adolescents and young adults. Neuroimage: Clinical, 8, 117–125. doi: 10.1016/j.nicl.2015.03.024 CrossRefGoogle ScholarPubMed
Sobell, L.C., & Sobell, M.B. (1992). Timeline Follow-Back. In Litten, R. Z. & Allen, J. P. (Eds.), Measuring Alcohol Consumption (pp. 41–72). Totowa, NJ: Humana Press.CrossRefGoogle Scholar
Sullivan, R.M., Wallace, A.L., Wade, N.E., Swartz, A.M., & Lisdahl, K.M. (2020). Assessing the Role of cannabis use on cortical surface structure in adolescents and young adults: Exploring gender and aerobic fitness as potential moderators. Brain Sciences, 10(2), 117. doi: 10.3390/brainsci10020117 CrossRefGoogle Scholar
Tervo-Clemmens, B., Quach, A., Calabro, F.J., Foran, W., & Luna, B. (2020). Meta-analysis and review of functional neuroimaging differences underlying adolescent vulnerability to substance use. NeuroImage, 209, 116476. doi: 10.1016/j.neuroimage.2019.116476 CrossRefGoogle ScholarPubMed
Thomas, A.G., Dennis, A., Bandettini, P.A., & Johansen-Berg, H. (2012). The effects of aerobic activity on brain structure. Frontiers in Psychology, 3(86), 86. doi: 10.3389/fpsyg.2012.00086 CrossRefGoogle ScholarPubMed
Thomas, S., Reading, J., & Shephard, R.J. (1992). Revision of the Physical Activity Readiness Questionnaire (PAR-Q). Canadian Journal of Sport Sciences, 17(4), 338–345. Retrieved from https://www.ncbi.nlm.nih.gov/pubmed/1330274 Google Scholar
Verweij, K.J., Zietsch, B.P., Lynskey, M.T., Medland, S.E., Neale, M.C., Martin, N.G., … Vink, J.M. (2010). Genetic and environmental influences on cannabis use initiation and problematic use: A meta-analysis of twin studies. Addiction, 105(3), 417–430. doi: 10.1111/j.1360-0443.2009.02831.x CrossRefGoogle ScholarPubMed
Vijayakumar, N., Allen, N.B., Youssef, G., Dennison, M., Yucel, M., Simmons, J.G., & Whittle, S. (2016). Brain development during adolescence: A mixed-longitudinal investigation of cortical thickness, surface area, and volume. Human Brain Mapping, 37(6), 2027–2038. doi: 10.1002/hbm.23154 CrossRefGoogle ScholarPubMed
Villares, J. (2007). Chronic use of marijuana decreases cannabinoid receptor binding and mRNA expression in the human brain. Neuroscience, 145(1), 323–334. doi: 10.1016/j.neuroscience.2006.11.012 CrossRefGoogle ScholarPubMed
Viveros, M.P., Llorente, R., Moreno, E., & Marco, E.M. (2005). Behavioural and neuroendocrine effects of cannabinoids in critical developmental periods. Behavioural Pharmacology, 16(5–6), 353–362. doi: 10.1097/00008877-200509000-00007 CrossRefGoogle ScholarPubMed
Voss, M.W., Vivar, C., Kramer, A.F., & van Praag, H. (2013). Bridging animal and human models of exercise-induced brain plasticity. Trends in Cognitive Sciences, 17(10), 525–544. doi: 10.1016/j.tics.2013.08.001 CrossRefGoogle ScholarPubMed
Wade, N.E., Wallace, A.L., Swartz, A.M., & Lisdahl, K.M. (2019). Aerobic fitness level moderates the association between cannabis use and executive functioning and psychomotor speed following abstinence in adolescents and young adults. Journal of the International Neuropsychological Society, 25(2), 134–145. doi: 10.1017/S1355617718000966 CrossRefGoogle ScholarPubMed
Wallace, A.L., Wade, N.E., & Lisdahl, K.M. (2020). Impact of 2 weeks of monitored abstinence on cognition in adolescent and young adult cannabis users. Journal of the International Neuropsychological Society, 1–9. doi: 10.1017/S1355617720000260 Google ScholarPubMed
Wallace, A.L., Wade, N.E., Hatcher, K.F., & Lisdahl, K.M. (2019). Effects of cannabis use and subclinical ADHD symptomology on attention based tasks in adolescents and young adults. Archives of Clinical Neuropsychology, 34(5), 700–705. doi: 10.1093/arclin/acy080 CrossRefGoogle ScholarPubMed
Watkins, B.A. (2018). Endocannabinoids, exercise, pain, and a path to health with aging. Molecular Aspects of Medicine, 64, 68–78. doi: 10.1016/j.mam.2018.10.001 CrossRefGoogle Scholar
Westin, A.A., Mjones, G., Burchardt, O., Fuskevag, O.M., & Slordal, L. (2014). Can physical exercise or food deprivation cause release of fat-stored cannabinoids? Basic & Clinical Pharmacology & Toxicology, 115(5), 467–471. doi: 10.1111/bcpt.12235 CrossRefGoogle ScholarPubMed
Whiteman, A.S., Young, D.E., Budson, A.E., Stern, C.E., & Schon, K. (2016). Entorhinal volume, aerobic fitness, and recognition memory in healthy young adults: A voxel-based morphometry study. NeuroImage, 126, 229–238. doi: 10.1016/j.neuroimage.2015.11.049 CrossRefGoogle ScholarPubMed
Wittfeld, K., Jochem, C., Dorr, M., Schminke, U., Glaser, S., Bahls, M., … Grabe, H.J. (2020). Cardiorespiratory fitness and gray matter volume in the temporal, frontal, and cerebellar regions in the general population. Mayo Clinic Proceedings, 95(1), 44–56. doi: 10.1016/j.mayocp.2019.05.030 CrossRefGoogle ScholarPubMed
Wong, A., Montebello, M.E., Norberg, M.M., Rooney, K., Lintzeris, N., Bruno, R., … McGregor, I.S. (2013). Exercise increases plasma THC concentrations in regular cannabis users. Drug and Alcohol Dependence, 133(2), 763–767. doi: 10.1016/j.drugalcdep.2013.07.031 CrossRefGoogle ScholarPubMed
Zinkstok, J., Schmitz, N., van Amelsvoort, T., de Win, M., van den Brink, W., Baas, F., & Linszen, D. (2006). The COMT val158met polymorphism and brain morphometry in healthy young adults. Neuroscience Letters, 405(1–2), 34–39. doi: 10.1016/j.neulet.2006.06.034 CrossRefGoogle ScholarPubMed
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