Hostname: page-component-586b7cd67f-tf8b9 Total loading time: 0 Render date: 2024-11-22T06:30:40.888Z Has data issue: false hasContentIssue false
  • English
  • Français

Female Sex as a Protective Factor in the Effects of Chronic Cannabis Use on Verbal Learning and Memory

Published online by Cambridge University Press:  15 July 2021

Rayna Hirst Open the ORCID record for Rayna Hirst [Opens in a new window] ,
Dylan Vaughn ,
Sana Arastu ,
Aubrey Deneen  and
Haig Pilavjian
Rayna Hirst*
Affiliation:
Department of Psychology, Palo Alto University, 1791 Arastradero Road, Palo Alto94304, CA, USA
Dylan Vaughn
Affiliation:
Department of Psychology, Palo Alto University, 1791 Arastradero Road, Palo Alto94304, CA, USA
Sana Arastu
Affiliation:
Department of Psychology, Palo Alto University, 1791 Arastradero Road, Palo Alto94304, CA, USA
Aubrey Deneen
Affiliation:
Department of Psychology, Palo Alto University, 1791 Arastradero Road, Palo Alto94304, CA, USA
Haig Pilavjian
Affiliation:
Department of Psychology, Palo Alto University, 1791 Arastradero Road, Palo Alto94304, CA, USA
*
Correspondence and reprint requests to: Rayna Hirst, Department of Psychology, Palo Alto University, 1791 Arastradero Road, Palo Alto94304, CA, USA. E-mail: [email protected]. Phone: 650-417-2025
Get access Rights & Permissions [Opens in a new window]

Abstract

Objective:

The variability of findings in studies examining the effects of chronic cannabis use on neuropsychological functioning highlights the importance of examining contributing factors. Few studies examine the role of sex in the relationship between cannabis and neuropsychological functioning, despite known neurobiological structural differences between males and females. This study examined whether males and females experience differential cognitive effects of chronic cannabis use.

Method:

Chronic cannabis users (3+ days per week for >12 months, n = 110, 72% male) and non-users (n = 71, 39% male) completed a neuropsychological test battery. Two multivariate analyses of covariance (MANCOVAs) examined for sex differences in performance within users and non-users on neuropsychological tests, controlling for potential confounding variables. Bonferroni corrections were applied to adjust for multiple comparisons.

Results:

Male and female cannabis users did not differ in cannabis use variables. Female cannabis users performed better than males on multiple subtests of the California Verbal Learning Test-II (CVLT-II), a verbal learning and memory test. Male cannabis users performed better than female users on Trial 1 of the CVLT-II (p = .002), and Trail Making Test B (p = .001), which measure attention and cognitive flexibility, respectively. Non-user males and females performed comparably, with the exception of Trail Making Test B (p = .001).

Conclusions:

Results suggest that chronic cannabis use differentially impacts males and females, with females exhibiting better verbal learning and memory despite males demonstrating better attention and cognitive flexibility. Further research is needed to understand the potential protective mechanism of female sex on learning and memory effects of cannabis use.

Keywords

MarijuanaGenderCannabisMemoryRecallAttention
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. 581 - 591
Copyright
Copyright © INS. Published by Cambridge University Press, 2021

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Anderson, B. M., Rizzo, M., Block, R. I., Pearlson, G. D., & O’Leary, D. S. (2010). Sex, drugs, and cognition: Effects of marijuana. Journal of Psychoactive Drugs, 42(4), 413–424. https://doi.org/10.1080/02791072.2010.10400704 CrossRefGoogle ScholarPubMed
Asperholm, M., Högman, N., Rafi, J., & Herlitz, A. (2019). What did you do yesterday? A meta-analysis of sex differences in episodic memory. Psychological Bulletin, 145(8), 785–821. https://doi.org/10.1037/bul0000197 CrossRefGoogle Scholar
Auer, R., Vittinghoff, E., Yaffe, K., Künzi, A., Kertesz, S. G., Levine, D. A., … Pletcher, M. J. (2016). Association between lifetime marijuana use and cognitive function in middle age. JAMA Internal Medicine, 176(3), 352. https://doi.org/10.1001/jamainternmed.2015.7841 CrossRefGoogle ScholarPubMed
Batalla, A., Bhattacharyya, S., Yücel, M., Fusar-Poli, P., Crippa, J. A., Nogué, 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). https://doi.org/10.1371/journal.pone.0055821 CrossRefGoogle ScholarPubMed
Blakesley, R. E., Mazumdar, S., Dew, M. A., Houck, P. R., Tang, G., Reynolds, C. F. III, & Butters, M. A. (2009). Comparisons of methods for multiple hypothesis testing in neuropsychological research. Neuropsychology, 23(2), 255–264. https://doi.org/10.1037/a0012850 CrossRefGoogle ScholarPubMed
Blair, J. R. & Spreen, O. (1989). Predicting premorbid IQ: A revision of the national adult reading test. Clinical Neuropsychologist, 3(2), 129–136. https://doi.org/10.1080/13854048908403285 CrossRefGoogle Scholar
Bolla, K., Eldreth, D., Matochik, J., & Cadet, J. (2005). Neural substrates of faulty decision-making in abstinent marijuana users. NeuroImage, 26(2), 480–492. https://doi.org/10.1016/j.neuroimage.2005.02.012 CrossRefGoogle ScholarPubMed
Bosker, W. M., Karschner, E. L., Lee, D., Goodwin, R. S., Hirvonen, J., Innis, R. B., … Ramaekers, J. G. (2013). Psychomotor function in chronic daily cannabis smokers during sustained abstinence. PLoS ONE, 8(1). https://doi.org/10.1371/journal.pone.0053127 CrossRefGoogle ScholarPubMed
Brady, K. T. (2020). Medical marijuana: Putting the cart before the horse. American Journal of Psychiatry, 177(7), 570–571. https://doi.org/10.1176/appi.ajp.2020.20050648 CrossRefGoogle Scholar
Broyd, S. J., van Hell, H. H., Beale, C., Yücel, M., & Solowij, N. (2016). Acute and chronic effects of cannabinoids on human cognition—A systematic review. Biological Psychiatry, 79(7), 557–567. https://doi.org/10.1016/j.biopsych.2015.12.002 CrossRefGoogle ScholarPubMed
Cooper, Z. D. & Craft, R. M. (2018). Sex-dependent effects of cannabis and cannabinoids: A translational perspective. Neuropsychopharmacology, 43(1), 34–51. https://doi.org/10.1038/npp.2017.140 CrossRefGoogle ScholarPubMed
Cosgrove, K. P., Mazure, C. M., & Staley, J. K. (2007). Evolving knowledge of sex differences in brain structure, function, and chemistry. Biological Psychiatry, 62(8), 847–855. https://doi.org/10.1016/j.biopsych.2007.03.001 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 and Experimental Neuropsychology, 37(4), 389–401. https://doi.org/10.1080/13803395.2015.1020770 CrossRefGoogle ScholarPubMed
Declues, K., Perez, S., & Figueroa, A. (2016). A 2-year study of δ 9-tetrahydrocannabinol concentrations in drivers: Examining driving and field sobriety test performance. Journal of Forensic Sciences, 61(6), 1664–1670. https://doi.org/10.1111/1556-4029.13168 CrossRefGoogle ScholarPubMed
Delis, D. C., Kramer, J. H., Kaplan, E., & Ober, B. A. (2000). California Verbal Learning Test – Second Edition. San Antonio, TX: Psychological Corporation.Google Scholar
DeLisi, L. E., Bertisch, H. C., Szulc, K. U., Majcher, M., Brown, K., Bappal, A., & Ardekani, B. A. (2006). A preliminary DTI study showing no brain structural change associated with Adolescent cannabis use. Harm Reduction Journal, 3(1), 17. https://doi.org/10.1186/1477-7517-3-17 CrossRefGoogle ScholarPubMed
Etherton, J. L., Bianchini, K. J., Greve, K. W., & Ciota, M. A. (2005). Test of memory malingering performance is unaffected by laboratory-induced pain: Implications for clinical use. Archives of Clinical Neuropsychology, 20(3), 375–384. https://doi.org/10.1016/j.acn.2004.09.007 CrossRefGoogle ScholarPubMed
Fattore, L. & Fratta, W. (2010). How important are sex differences in cannabinoid action? British Journal of Pharmacology, 160(3), 544–548. https://doi.org/10.1111/j.1476-5381.2010.00776.x CrossRefGoogle ScholarPubMed
Ferguson, C. J. (2016). An effect size primer: A guide for clinicians and researchers. Professional Psychology: Research and Practice, 40(5), 532–538. https://doi.org/10.1037/a0015808 CrossRefGoogle Scholar
Gonzalez, R., Carey, C., & Grant, I. (2002). Nonacute (residual) neuropsychological effects of cannabis use: A qualitative analysis and systematic review. The Journal of Clinical Pharmacology, 42(S1), 48S–57S. https://doi.org/10.1002/j.1552-4604.2002.tb06003.x CrossRefGoogle ScholarPubMed
Green, P. (2003). Word Memory Test for Windows: User’s manual and program. Edmonton: Green’s Publishing.Google Scholar
Grissom, N. M. & Reyes, T. M. (2019). Let’s call the whole thing off: Evaluating gender and sex differences in executive function. Neuropsychopharmacology, 44(1), 86–96. https://doi.org/10.1038/s41386-018-0179-5 CrossRefGoogle ScholarPubMed
Gruber, S. A., Sagar, K. A., Dahlgren, M. K., Racine, M., & Lukas, S. E. (2012). Age of onset of marijuana use and executive function. Psychology of Addictive Behaviors, 26(3), 496. https://doi.org/10.1037/a0026269 CrossRefGoogle ScholarPubMed
Han, B. H. & Palamar, J. J. (2020). Trends in cannabis use among older adults in the United States, 2015-2018. JAMA Internal Medicine, 180(4), 609–611. https://doi.org/10.1001/jamainternmed.2019.7517 CrossRefGoogle ScholarPubMed
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. https://doi.org/10.1016/j.addbeh.2010.06.012 CrossRefGoogle ScholarPubMed
Hirnstein, M., Hugdahl, K., & Hausmann, M. (2019). Cognitive sex differences and hemispheric asymmetry: A critical review of 40 years of research. Laterality: Asymmetries of Body, Brain, and Cognition, 24(2), 204–252. https://doi.org/10.1080/1357650X.2018.1497044 CrossRefGoogle ScholarPubMed
Hirst, R. B., Young, K. R., Sodos, L. M., Wickham, R. E., & Earleywine, M. (2017). Trying to remember: Effort mediates the relationship between frequency of cannabis use and memory performance. Journal of Clinical and Experimental Neuropsychology, 39(5), 502–512. https://doi.org/10.1080/13803395.2016.1237617 CrossRefGoogle ScholarPubMed
Hooper, S. R., Woolley, D., & De Bellis, M. D. (2014). Intellectual, neurocognitive, and academic achievement in abstinent adolescents with cannabis use disorder. Psychopharmacology, 231(8), 1467–1477. https://doi.org/10.1007/s00213-014-3463-z CrossRefGoogle ScholarPubMed
Huizenga, H. M., Smeding, H., Grasman, R. P., & Schmand, B. (2007). Multivariate normative comparisons. Neuropsychologia, 45(11), 2534–2542. https://doi.org/10.1016/j.neuropsychologia.2007.03.011 CrossRefGoogle ScholarPubMed
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. https://doi.org/10.1037/neu0000203 CrossRefGoogle ScholarPubMed
Laurikainen, H., Tuominen, L., Tikka, M., Merisaari, H., Armio, R., Sormunen, E., … Hietala, J. (2019). Sex difference in brain CB1 receptor availability in man. NeuroImage, 184, 834–842. https://doi.org/10.1016/j.neuroimage.2018.10.013 CrossRefGoogle ScholarPubMed
Lezak, M. D., Howieson, D. B., Bigler, E. D., & Tranel, D. (2012). Neuropsychological Assessment (5th ed.). Oxford University Press.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. https://doi.org/10.1017/S1355617712000276 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. https://doi.org/10.1007/s00406-019-00979-1 CrossRefGoogle ScholarPubMed
Lyons, M. J., Bar, J. L., Panizzon, M. S., Toomey, R., Eisen, S., Xian, H., & Tsuang, M. T. (2004). Neuropsychological consequences of regular marijuana use: A twin study. Psychological Medicine, 34(7), 1239–1250. https://doi.org/10.1017/S0033291704002260 CrossRefGoogle ScholarPubMed
Macher, R. B. & Earleywine, M. (2012). Enhancing neuropsychological performance in chronic cannabis users: The role of motivation. Journal of Clinical and Experimental Neuropsychology, 34(4), 405–415. https://doi.org/10.1080/13803395.2011.646957 CrossRefGoogle ScholarPubMed
Madras, B. K. (2015). Update of Cannabis and its Medical Use. Geneva: World Health Organization.Google Scholar
Medina, K. L., Nagel, B. J., & Tapert, S. F. (2010). Abnormal cerebellar morphometry in abstinent adolescent marijuana users. Psychiatry Research: Neuroimaging, 182(2), 152–159. https://doi.org/10.1016/j.pscychresns.2009.12.004 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, 109(40). https://doi.org/10.1073/pnas.1206820109 CrossRefGoogle ScholarPubMed
Oswald, L. M., Wand, G. S., Zhu, S., & Selby, V. (2013). Volunteerism and self-selection bias in human positron emission tomography neuroimaging research. Brain Imaging and Behavior, 7(2), 163–176. https://doi.org/10.1007/s11682-012-9210-3 CrossRefGoogle ScholarPubMed
Papafotiou, K., Carter, J. D., & Stough, C. (2005). An evaluation of the sensitivity of the Standardised Field Sobriety Tests (SFSTs) to detect impairment due to marijuana intoxication. Psychopharmacology, 180(1), 107–114. https://doi.org/10.1007/s00213-004-2119-9 CrossRefGoogle ScholarPubMed
Pope, H. G., Jacobs, A., Mialet, J. P., Yurgelun-Todd, D., & Gruber, S. (1997). Evidence for a sex-specific residual effect of cannabis on visuospatial memory. Psychotherapy and Psychosomatics, 66(4), 179–184. https://doi.org/10.1159/000289132 CrossRefGoogle ScholarPubMed
Pope, H. G., Gruber, A. J., Hudson, J. I., Huestis, M. A., & Yurgelun-Todd, D. (2001). Neuropsychological performance in long-term cannabis users. Archives of General Psychiatry, 58(10), 909–915. https://doi.org/10.1001/archpsyc.58.10.909 CrossRefGoogle ScholarPubMed
Prashad, S., Hammonds, R. P., Wiese, A. L., Milligan, A. L., Filbey, F. M. (2020). Sex-related differences in subjective, but not neutral, cue-elicited craving response in heavy cannabis users. Drug and Alcohol Dependence, 209(1), 107931. https://doi.org/10.1016/j.drugalcdep.2020.107931 CrossRefGoogle ScholarPubMed
Rabin, L. A., Paolillo, E., & Barr, W. B. (2016). Stability in test-usage practices of clinical neuropsychologists in the United States and Canada over a 10-year period: A follow-up survey of INS and NAN members. Archives of Clinical Neuropsychology, 31(3), 206–230. https://doi.org/10.1093/arclin/acw007 CrossRefGoogle Scholar
Reitan, R. M. & Wolfson, D. (1992). The Halstead–Reitan Neuropsychological Battery: Theory and Clinical Interpretation (2nd ed.). South Tucson, AZ: Neuropsychology Press.Google Scholar
Rey, A. (1941). L’examen psychologique dans le cas d’encephalopathie traumatique [Psychological examination of traumatic encephalopathy]. Archives de Psychologie, 28, 286–340. Retrieved from http://psycnet.apa.org/psycinfo/1943-03814-001 Google Scholar
Root, J. C., Robbins, R. N., Chang, L., & Van Gorp, W. G. (2006). Detection of inadequate effort on the California Verbal Learning Test – Second Edition: Forced choice recognition and critical item analysis. Journal of the International Neuropsychological Society, 12(5), 688–696. https://doi.org/10.10170S1355617706060838 CrossRefGoogle ScholarPubMed
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 & Misuse, 53(12), 1937–1950. https://doi.org/10.1080/10826084.2018.1441312 CrossRefGoogle ScholarPubMed
Ruffolo, L. F., Guilmette, T. J., & Willis, G. W. (2000). FORUM comparison of time and error rates on the trail making test among patients with head injuries, experimental malingerers, patients with suspect effort on testing, and normal controls. The Clinical Neuropsychologist, 14(2), 223–230. https://doi.org/10.1076/1385-4046(200005)14:2;1-Z;FT223 CrossRefGoogle Scholar
Schreiner, A. M. & Dunn, M. E. (2012). Residual effects of cannabis use on neurocognitive performance after prolonged abstinence: a meta-analysis. Experimental and Clinical Psychopharmacology, 20(5), 420–429. https://doi.org/10.1037/a0029117 CrossRefGoogle ScholarPubMed
Sodos, L. M., Hirst, R. B., Watson, J., & Vaughn, D. (2018). Don’t judge a book by its cover: Examiner expectancy effects predict neuropsychological performance for individuals judged as chronic cannabis users. Archives of Clinical Neuropsychology, 33(7), 821–831. https://doi.org/10.1093/arclin/acx114 CrossRefGoogle Scholar
Substance Abuse and Mental Health Services Administration (SAMHSA; 2019). R esults from the 2018 National Survey on Drug Use and Health: Detailed tables. Rockville, MD: Center for Behavioral Health Statistics and Quality. [Table]. https://www.samhsa.gov/data/ Google Scholar
Sundermann, E. E., Biegon, A., Rubin, L. H., Lipton, R. B., Landau, S., & Maki, P. M. (2017). Does the female advantage in verbal memory contribute to underestimating Alzheimer’s disease pathology in women versus men? Journal of Alzheimer’s Disease, 56(3), 947–957. https://doi.org/10.3233/JAD-160716 CrossRefGoogle ScholarPubMed
Tait, R. J., Mackinnon, A., & Christensen, H. (2011). Cannabis use and cognitive function: 8-year trajectory in a young adult cohort. Addiction, 106(12), 2195–2203. https://doi.org/10.1111/j.1360-0443.2011.03574.x CrossRefGoogle Scholar
Verdejo-Garcia, A., Benbrook, A., Funderburk, F., David, P., Cadet, J. L., & Bolla, K. I. (2007). The differential relationship between cocaine use and marijuana use on decision-making performance over repeat testing with the Iowa Gambling Task. Drug and Alcohol Dependence, 90(1), 2–11. https://doi.org/10.1016/j.drugalcdep.2007.02.004 CrossRefGoogle ScholarPubMed
Wechsler, D. (1997). Wechsler Adult Intelligence Scale – Third Edition (WAIS-III): Administration and Scoring Manual. San Antonio, TX: Psychological Corporation.Google Scholar
Wilson, R. I. & Nicoll, R. A. (2002). Endocannabinoid signaling in the brain. Science, 296(5568), 678–682. https://doi.org/10.1126/science.1063545 CrossRefGoogle Scholar
World Health Organization (2020). Management of Substance Abuse: Cannabis. Retrieved July 1, 2020 from https://www.who.int/substance_abuse/facts/cannabis/en/ Google Scholar
Yanes, J. A., Riedel, M. C., Ray, K. L., Kirkland, A. E., Bird, R. T., Boeving, E. R., … & Sutherland, M. T. (2018). Neuroimaging meta-analysis of cannabis use studies reveals convergent functional alterations in brain regions supporting cognitive control and reward processing. Journal of Psychopharmacology, 32(3), 283–295. https://doi.org/10.1177/0269881117744995 CrossRefGoogle ScholarPubMed