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Aerobic Fitness Level Moderates the Association Between Cannabis Use and Executive Functioning and Psychomotor Speed Following Abstinence in Adolescents and Young Adults

Published online by Cambridge University Press:  26 November 2018

Natasha E. Wade ,
Alexander L. Wallace ,
Ann M. Swartz  and
Krista M. Lisdahl
Natasha E. Wade
Affiliation:
Department of Psychology, University of Wisconsin-Milwaukee, Milwaukee, Wisconsin
Alexander L. Wallace
Affiliation:
Department of Psychology, University of Wisconsin-Milwaukee, Milwaukee, Wisconsin
Ann M. Swartz
Affiliation:
Department of Kinesiology, University of Wisconsin-Milwaukee, Milwaukee, Wisconsin
Krista M. Lisdahl*
Affiliation:
Department of Psychology, University of Wisconsin-Milwaukee, Milwaukee, Wisconsin
*
Correspondence and reprint requests to: Krista M. Lisdahl, 2441 East Hartford Avenue, Milwaukee, WI 53211. E-mail: krista.medina@gmail.com
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Abstract

Objectives: The high rate of cannabis (CAN) use in emerging adults is concerning given prior research suggesting neurocognitive deficits associated with CAN use in youth. Regular CAN use downregulates endocannabinoid activity, while aerobic exercise upregulates cannabinoid receptor 1 activity and releases endocannabinoids. Here we investigate the influence of regular CAN use on neuropsychological performance, and whether aerobic fitness moderates these effects. Methods: Seventy-nine young adults (37 CAN users) aged 16–26 participated. Groups were balanced for aerobic fitness level. Exclusion criteria included: left-handedness, past-year independent Axis-I disorders, major medical/neurologic disorders, prenatal issues, or prenatal alcohol/illicit drug exposure. After 3 weeks of abstinence, participants completed a neuropsychological battery and a maximal oxygen consumption test (VO2 max). Multiple regressions tested whether past-year CAN use, VO2 max, and CAN*VO2 max interaction predicted neuropsychological performance, controlling for past-year alcohol use, cotinine, gender, and depression symptoms. Results: Increased CAN use was associated with decreased performance on working memory and psychomotor tasks. High aerobic fitness level was related to better performance on visual memory, verbal fluency, and sequencing ability. CAN*VO2 max predicted performance of psychomotor speed, visual memory, and sequencing ability. Conclusions: Following monitored abstinence, increased CAN use was associated with poorer performance in working memory and psychomotor speed. Higher aerobic fitness level moderated the impact of CAN on visual memory, executive function and psychomotor speed, as more aerobically fit CAN users demonstrated better performance relative to low-fit users. Therefore, aerobic fitness may present an affordable and efficacious method to improve cognitive functioning in CAN users. (JINS, 2019, 25, 134–145)

Keywords

CannabisMarijuanaVO2 maxNeurocognitionEmerging adulthoodAerobic fitness
Type
Regular Research
Information
Journal of the International Neuropsychological Society , Volume 25 , Issue 2 , February 2019 , pp. 134 - 145
Copyright
Copyright © The International Neuropsychological Society 2018 

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References

REFERENCES

Bassett, D.R., Howley, E.T., Thompson, D.L., King, G.A., Strath, S.J, McLaughlin, J.E., & Parr, B.B. (2001). Validity of inspiratory and expiratory methods of measuring gas exchange with a computerized system. Journal of Applied Physiology, 91(1), 218–224.Google Scholar
Bassett, D.R., & Howley, E.T. (2000). Limiting factors for maximum oxygen uptake and determinants of endurance performance. Medicine and Science in Sports and Exercise, 32(1), 70–84.Google Scholar
Bechara, A., Damasio, A.R., Damasio, H., & Anderson, S.W. (1994). Insensitivity to future consequences following damage to human prefrontal cortex. Cognition, 50(1-3), 7–15.Google Scholar
Beck, A.T. (1996). Beck Depression Inventory-2nd edition. New York: NY: Psychological Corporation.Google Scholar
Becker, M.P., Collins, P.F., & Luciana, M. (2014). Neurocognition in college-aged daily marijuana users. Journal of Clinical and Experimental Neuropsychology, 36(4), 379–398.Google Scholar
Becker, M.P., Collins, P.F., Schultz, A., Urosevic, S., Schmaling, B., & Luciana, M. (2018). Longitudinal changes in cognition in young adult cannabis users. Journal of Clinical and Experimental Neuropsychology, 40, 529–543.Google Scholar
Brellenthin, A.G., & Koltyn, K.F. (2016). Exercise as an adjunctive treatment for cannabis use disorder. The American Journal of Drug and Alcohol Abuse, 42(5), 481–489.Google Scholar
Brellenthin, A.G., Crombie, K.M., Hillard, C.J., & Koltyn, K.F. (2017). Endocannabinoid and mood responses to exercise in adults with varying activity levels. Medicine and Science in Sports and Exercise, 49(8), 1688–1696.Google Scholar
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. Journal of Studies on Alcohol, 59, 427–438.Google Scholar
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 Google Scholar
Budney, A.J., Hughes, J.R., Moore, B.A., & Vandrey, R. (2004). Review of the validity and significance of cannabis withdrawal syndrome. The American Journal of Psychiatry, 161(11), 1967–1977.Google Scholar
Castrén, E., Berninger, B., Leingärtner, A., & Lindholm, D. (1998). Regulation of brain-derived neurotrophic factor mRNA levels in hippocampus by neuronal activity. Progress in Brain Research, 117, 57–64.Google Scholar
Chaouloff, F. (1989). Physical exercise and brain monoamines: A review. Acta Physiologica Scandinavica, 137, 1–13.Google Scholar
Conners, C.K. (2000). Conners’ Continuous Performance Test user’s manual. Toronto, Canada: Multi-Health Systems.Google Scholar
Cotman, C.W., & Berchtold, N.C. (2002). Exercise: A behavioral intervention to enhance brain health and plasticity. Trends in Neuroscience, 25, 295–301.Google Scholar
Cotman, C.W., Berchtold, N.C., & Christie, L.A (2007). Exercise builds brain health: Key roles of growth factor cascades and inflammation. Trends in Neuroscience, 30, 464–472.Google Scholar
Crews, F.T., Nixon, K., & Wilkie, M.E. (2004). Exercise reverses ethanol inhibition of neural stem cell proliferation. Alcohol, 33, 63–71.Google Scholar
Dahlgren, M.K., Sagar, K.A., Racine, M.T., Dreman, M.W., & Gruber, S.A. (2016). Marijuana use predicts cognitive performance on tasks of executive function. Journal of Studies on Alcohol and Drugs, 77(2), 298–308.Google Scholar
Delis, D.C., Kaplan, E., & Kramer, J.H. (2001). Delis-Kaplan Executive Function System (D-KEFS). San Antonio, TX: The Psychological Corporation.Google Scholar
Delis, D.C. Kramer, J.H., Kaplan, E., & Ober, B.A. (2000). California Verbal Learning Test – second edition. Adult version. Manual. San Antonio, TX: Psychological Corporation.Google Scholar
Ding, Y., Li, J., Luan, X., Ding, Y.H., Lai, W., Rafols, J.A., … Diaz, F.G. (2004). Exercise pre-conditioning reduces brain damage in ischemic rats that may be associated with regional angiogenesis and cellular overexpression of neurotrophin. Neuroscience, 124, 583–591.Google Scholar
Di Marzo, V., De Petrocellis, L., & Bisogno, T. (2005). The biosynthesis, fate, and pharmacological properties of endocannabinoids. Handbook of Experimental Pharmacology, 168, 147–185.Google Scholar
Dragunow, M. (1996). A role for immediate-early transcription factors in learning and memory. Behavior Genetics, 26, 293–299.Google Scholar
Dunn, A.L., & Dishman, R.K. (1991). Exercise and the neurobiology of depression. Exercise and Sport Sciences Reviews, 19, 41–98.Google Scholar
Dunn, A.L., Reigle, T.G., Youngstedt, S.D., Armstrong, R.B., & Dishman, R.K. (1996). Brain norepinephrine and metabolites after treadmill training and wheel running in rats. Medicine and Science in Sports and Exercise, 28, 204–209.Google Scholar
Egan, M.F., Kojima, M., Callicott, J.H., Goldberg, T.E., Kolachana, B.S., Bertolino, A., … Weinberger, D.R. (2003) The BDNF val66met polymorphism affects activity-dependent secretion of BDNF and human memory and hippocampal function. Cell, 112, 257–269.Google Scholar
Egerton, A., Allison, C., Brett, R.R., & Pratt, J.A. (2006). Cannabinoids and prefrontal cortical function: Insights from preclinical studies. Neuroscience and Biobehavioral Reviews, 30(5), 680–695.Google Scholar
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.Google Scholar
Elam, M., Svensson, T.H., & Thorén, P. (1987). Brain monoamine metabolism is altered in rats following spontaneous, long-distance running. Acta Physiologica Scandinavica, 130, 313–316.Google Scholar
Fergusson, D.M., & Boden, J.M. (2008). Cannabis use and later life outcomes. Addiction, 103(6), 969–976.Google Scholar
Ferreira-Vieira, T.H., Bastos, C.P., Pereira, G.S., Moreira, F.A., & Massensini, A.R. (2014). A role for the endocannabinoid system in exercise-induced spatial memory enhancement in mice. Hippocampus, 24(1), 79–88.Google Scholar
Fried, P.A., Watkinson, B., & Gray, R. (2005). Neurocognitive consequences of marihuana--A comparison with pre-drug performance. Neurotoxicology and Teratology, 27(2), 231–239. doi:10.1016/j.ntt.2004.11.003 Google Scholar
Ganzer, F., Bröning, S., Kraft, S., Sack, P.M., & Thomasius, R. (2016). Weighing the evidence: A systematic review on long-term neurocognitive effects of cannabis use in abstinent adolescents and adults. Neuropsychology Review, 26, 186–222 Google Scholar
Grevenstein, D., & Kroninger-Jungaberle, H. (2015). Two patterns of cannabis use among adolescents: Results of a 10-year prospective study using a growth mixture model. Substance Abuse, 36(1), 85–89.Google Scholar
Gur, R.C., Richard, J., Hughett, P., Calkins, M.E., Macy, L., Bilker, W.B., … Gur, R.E. (2010). A cognitive neuroscience based computerized battery for efficient measurement of individual differences: Standardization and initial construct validation. Journal of Neuroscience Methods, 187(2), 254–262.Google Scholar
Hamilton, G.F., Criss, K.J., & Klintsova, A.Y (2015). Voluntary exercise partially reverses neonatal alcohol-induced deficits in mPFC layer II/III dendritic morphology of male adolescent rats. Synapse, 69, 405–415.Google Scholar
Hanson, K.L., Winward, J.L., Schweinsburg, A.D., Medina, K.L., Brown, S.A., & Tapert, S.F. (2010). Longitudinal study of cognition among adolescent marijuana users over three weeks of abstinence. Addictive Behaviors, 35(11), 970–976. doi:10.1016/j.addbeh.2010.06.012 Google Scholar
He, J., Yamada, K., & Nabeshima, T. (2002). A role of Fos expression in the CA3 region of the hippocampus in spatial memory formation in rats. Neuropsychopharmacology, 26, 259–268.Google Scholar
Helfer, J.L., Goodlett, C.R., Greenough, W.T., & Klintsova, A.Y (2009). The effects of exercise on adolescent hippocampal neurogenesis in a rat model of binge alcohol exposure during the brain growth spurt. Brain Research, 1294, 1–11.Google Scholar
Henchoz, Y., Dupuis, M., Deline, S., Studer, J., Baggio, S., N’Goran, A.A., … Gmel, G. (2014). Associations of physical activity and sport and exercise with at-risk substance use in young men: A longitudinal study. Preventive Medicine, 64, 27–31.Google Scholar
Herkenham, M., Lynn, A.B., Little, M.D., Johnson, M.R., Melvin, L.S., de Costa, B.R., & Rice, K.C. (1990. Cannabinoid receptor localization in brain. Proceedings of the National Academy of Sciences of the United States of America, 87(5), 1932–1936.Google Scholar
Herting, M.M., & Chu, X. (2017). Exercise, cognition, and the adolescent brain. Birth Defects Research, 109(20), 1672–1679.Google Scholar
Heyes, M.P., Garnett, E.S., & Coates, G. (1985). Central dopaminergic activity influences rats ability to exercise. Life Science, 36, 671–677.Google Scholar
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 Google Scholar
Horwood, L.J., Fergusson, D.M., Hayatbakhsh, M.R., Najman, J.M., Coffey, C., Patton, G.C., … Hutchinson, D.M. (2010). Cannabis use and education achievement: Findings from three Australasian cohort studies. Drug and Alcohol Dependence, 110(3), 247–253.Google Scholar
Howley, E.T., Bassett, D.R., & Welch, H.G. (1995). Criteria for maximal oxygen uptake: Review and commentary. Medicine and Science in Sports and Exercise, 27(9), 1292–1301.Google Scholar
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 & Behavior, 179, 75–89.Google Scholar
Jacobus, J., Squeglia, L.M., Infante, M.A., Castro, N., Brumback, T., Meruelo, A.D., & Tapert, S.F. (2015). Neuropsychological performance in adolescent marijuana users with co-occurring alcohol use: A three-year longitudinal study. Neuropsychology, 29(6), 829–843.Google Scholar
Jacobus, J., Squeglia, L.M., Sorg, S.F., Nguyen-Louie, T.T., & Tapert, S.F. (2014). Cortical thickness and neurocognition in adolescent marijuana and alcohol users following 28 days of monitored abstinence. Journal of Studies on Alcohol and Drugs, 5(5), 729–743.Google Scholar
Kang, D.H., Boss, K., & Clowtis, L. (2016). Social support and cognition: Early childhood versus older adulthood. Western Journal of Nursing Research, 38(12), 1639–1659.Google Scholar
Kim, H., Lee, S.H., Kim, S.S., Yoo, J.H., & Kim, C.J. (2007). The influence of maternal treadmill running during pregnancy on short-term memory and hippocampal cell survival in rat pups. International Journal of Developmental Neuroscience, 25, 243–249.Google Scholar
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 Google Scholar
Leasure, J.L., & Jones, M (2008). Forced and voluntary exercise differentially affect brain and behavior. Neuroscience, 156, 456–465.Google Scholar
Leasure, J.L., & Nixon, K. (2010). Exercise neuroprotection in a rat model of binge alcohol consumption. Alcoholism, Clinical and Experimental Research, 34, 404–414.Google Scholar
Lee, H.H., Kim, H., Lee, J.W., Kim, Y.S., Yang, H.Y., Chang, H.L., … Kim, C.J. (2006). Maternal swimming during pregnancy enhances short-term memory and neurogenesis in the hippocampus of rat pups. Brain Development, 28, 147–154.Google Scholar
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.Google Scholar
Lee, T.T., & Gorzalka, B.B. (2012). Timing is everything: Evidence for a role of corticolimbic endocannabinoids in modulating hypothalamic-pituitary-adrenal axis activity across development periods. Neuroscience, 204, 17–30.Google Scholar
Li, X.C., Jarvis, E.D., Alvarez-Borda, B., Lim, D.A., & Nottebohm, F. (2000). A relationship between behavior, neurotrophin expression, and new neuron survival. Proceedings of the National Academy of Sciences of the United States of America, 97, 8584–8589.Google 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 Google Scholar
Lisdahl, K.M., Gilbart, E.R., Shollenbarger, S., & Wright, N (2013). Dare to delay?: The impacts of adolescent alcohol and marijuana use onset on cognition, brain structure and function. Frontiers in Psychiatry; 4, 53. PMID: 23847550.Google Scholar
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.Google Scholar
Liu, D., Diorio, J., Day, J.C., Francis, D.D., & Meaney, M.J. (2000). Maternal care, hippocampal synaptogenesis and cognitive development in rats. Nature Neuroscience, 3, 799–806.Google Scholar
Manly, J.J., Jacobs, D.M., & Touradji, P. (2002). Reading level attenuates differences in neuropsychological test performance between African American and White elders. Journal of the International Neuropsychological Society, 8(3):341–348.Google Scholar
Miech, R.A., Johnston, L.D., O’Malley, P.M., Bachman, J.G., Schulenberg, J.E., & Patrick, M.E. (2017). Monitoring the Future national survey results on drug use, 1975-2014: Volume I Secondary school students. Ann Arbor: Institute for Social Research.Google Scholar
Medina, K.L., Hanson, K., Schweinsburg, A.D., Cohen-Zion, M., Nagel, B.J., & Tapert, S.F. (2007). Neuropsychological functioning in adolescent marijuana users: Subtle deficits detectable after 30 days of abstinence. Journal of the International Neuropsychological Society, 13(5), 807–820.Google Scholar
Meyers, J.E., & Meyers, K.R. (1995). Rey complex figure test and recognition trial: Professional manual. Lutz, FL: PAR, Inc.Google Scholar
Mueller, K., Moller, H.E., Horstmann, A., Busse, F., Lepsien, J., Bluher, M., … Pleger, B. (2015). Physical exercise in overweight to obese individuals induces metabolic- and neurotrophic-related structural brain plasticity. Frontiers in Human Neuroscience, 9, 372.Google Scholar
Nguyen-Louie, T.T., Tracas, A., Squeglia, L.M., Matt, G.E., Eberson-Shumate, S., & Tapert, S.F. (2016). Learning and memory in adolescent moderate, binge, and extreme-binge drinkers. Alcoholism, Clinical and Experimental Research, 40(9), 1895–1904.Google Scholar
Nguyen-Louie, T.T., Castro, N., Matt, G.E., Squeglia, L.M., Brumback, T., & Tapert, S.F. (2015). Effect of emerging alcohol and marijuana use behaviors on adolescents’ neuropsychological functioning over four years. Journal of Studies on Alcohol and Drugs, 76(5), 738–748.Google Scholar
Nguyen-Louie, T.T., Matt, G.E., Jacobus, J., Li, I., Cota, C., Castro, N., & Tapert, S.F. (2017). Earlier alcohol use onset predicts poorer neuropsychological functioning in young adults. Alcoholism, Clinical and Experimental Research, 41(12), 2082–2092.Google Scholar
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. Journal of Physiology, 594, 1855–1873.Google Scholar
Pescatello, L.S. (2014). ACSM’s guidelines for exercise testing and prescription (9th ed.). Philadelphia: Wolters Kluwer/Lippincott Williams & Wilkins Health.Google Scholar
Radak, Z., Kumagai, S., Taylor, A.W., Naito, H., & Goto, S. (2007). Effects of exercise on brain function: Role of free radicals. Applied Physiology, Nutrition, and Metabolism, 32, 942–946.Google Scholar
Rosen, A.S., Sodos, L.M., Hirst, R.B., Vaughn, D., & Lorkiewicz, S.A. (2018). Cream of the crop: Clinical representativeness of eligible and ineligible cannabis users in research. Substance Use and Misuse, 53, 1937–1950.Google Scholar
Sakurai, T., Izawa, T., Kizaki, T., Ogasawara, J.E., Shirato, K., Imaizumi, K., … Ohno, H. (2009). Exercise training decreases expression of inflammation-related adipokines through reduction of oxidative stress in rat white adipose tissue. Biochemical and Biophysical Research Communications, 379, 605–609.Google Scholar
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.Google Scholar
Sheehan, D.V., Lecrubier, Y., Sheehan, K.H., Amorim, P., Janavs, J., Weiller, E., … Dunbar, G.C. (1998). The Mini-International Neuropsychiatric Interview (M.I.N.I.): The development and validation of a structured diagnostic psychiatric interview for DSM-IV and ICD-10. Journal of Clinical Psychiatry, 59(Suppl 20), 22–33.Google Scholar
Sim, Y.J., Kim, S., Shin, M.S., Chang, H.K., Shin, M.C., Ko, I.G., … Kim, C.J. (2008). Effect of postnatal treadmill exercise on c-Fos expression in the hippocampus of rat pups born from the alcohol-intoxicated mothers. Brain & Development, 30, 118–125.Google Scholar
Sobell, L.C., & Sobell, M.B. (1992). Timeline follow-back: A technique for assessing self-reported ethanol consumption. In J. Allen & R. Z. Litten (Eds.), Measuring alcohol consumption: Psychosocial and biological methods (pp. 41–72). Totowa, NJ: Humana Press.Google Scholar
Solowij, N., Jones, K.A., Rozman, M.E., Davis, S.M., Ciarrochi, J., Heaven, P.C., … Yücel, M. (2011). Verbal learning and memory in adolescent cannabis users, alcohol users and non-users. Psychopharmacology (Berlin), 216(1), 131–144.Google Scholar
Stewart, D.G., & Brown, S.A. (1995). Withdrawal and dependency symptoms among adolescent alcohol and drug abusers. Addiction, 90, 627–635.Google Scholar
Stranahan, A.M., Lee, K., Becker, K.G., Zhang, Y., Maudsley, S., Martin, B., … Mattson, M.P. (2010). Hippocampal gene expression patterns underlying the enhancement of memory by running in aged mice. Neurobiology of Aging, 31, 1937–1949.Google Scholar
Suerken, C.K., Reboussin, B.A., Egan, K.L., Sutfin, E.L., Wagoner, K.G., Spangler, J., & Wolfson, M. (2016). Marijuana use trajectories and academic outcomes among college students. Drug and Alcohol Dependence, 162, 137–145.Google Scholar
Thames, A.D., Arbid, N., & Sayegh, P. (2014). Cannabis use and neurocognitive functioning in a non-clinical sample of users. Addictive Behaviors, 39(5), 994–999.Google Scholar
van Praag, H., Christie, B.R., Sejnowski, T.J., & Gage, F.H(1999). Running enhances neurogenesis, learning, and long-term potentiation in mice. Proceedings of the National Academy of Sciences of the United States of America, 96, 13427–13431.Google Scholar
Vann, S.D., Brown, M.W., Erichsen, J.T., & Aggleton, J.P. (2000). Fos imaging reveals differential patterns of hippocampal and parahippocampal subfield activation in rats in response to different spatial memory tests. The Journal of Neuroscience, 20, 2711–2718.Google Scholar
Varlinskaya, E.I., & Spear, L.P. (2015). Social consequences of ethanol: Impact of age, stress, and prior history of ethanol exposure. Physiology & Behavior, 148, 145–150.Google Scholar
Vaynman, S., Ying, Z., & Gomez-Pinilla, F (2004). Hippocampal BDNF mediates the efficacy of exercise on synaptic plasticity and cognition. European Journal of Neuroscience, 20, 2580–2590.Google Scholar
Waters, R.P., Emerson, A.J., Watt, M.J., Forster, G.L., Swallow, J.G., & Summers, C.H. (2005). Stress induces rapid changes in central catecholaminergic activity in Anolis carolinensis: Restraint and forced physical activity. Brain Research Bulletin, 67, 210–218.Google Scholar
Wechsler, D. (1997). WAIS-III Administration and scoring manual. San Antonio, TX: The Psychological Corporation.Google Scholar
Wengaard, E., Kristoffersen, M., Harris, A., & Gundersen, H. (2017). Cardiorespiratory fitness is associated with selective attention in healthy male high-school students. Frontiers in Human Neuroscience, 11, 330.Google Scholar
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 morephometry study. NeuroImage, 126, 229–238.Google Scholar
Whiteman, A.S., Young, D.E., He, X., Chen, T.C., Wagenaar, R.C., Stern, C.E., & Schon, K. (2014). Interaction between serum BDNF and aerobic fitness predicts recognition memory in healthy young adults. Behavioural Brain Research, 259, 302–312. doi:10.1016/j.bbr.2013.11.023 Google Scholar
Winward, J.L., Hanson, K.L., Tapert, S.F., Brown, S.A. (2014). Heavy alcohol use, marijuana use, and concomitant use by adolescents are associated with unique and shared cognitive decrements. Journal of the International Neuropsychological Society, 20(8), 784–795.Google Scholar
Yucel, M., Lorenzetti, V., Suo, C., Zalesky, A., Fornito, A., Takagi, M.J., … Solowij, N. (2016). Hippocampal harms, protection, and recovery following regular cannabis use. Translational Psychiatry, 6, e710.Google Scholar