This is an outdated version published on 2023-09-18. Read the most recent version.

Comparative study of neuropsychological and neurophysiological functioning in regular users of cannabis and healthy controls

Authors

  • Luz Angela Rojas Bernal Facultad de Ciencias de la Salud y del Deporte, Fundación Universitaria del Área Andina. Bogotá, Colombia.
  • Juan Camilo Mejía Piedrahita Grupo de investigación en Psiquiatría GIPSI, Universidad de Antioquía. Medellín, Colombia.
  • Alejandra María Zapata Villa Centro de Atención en Neurología Pediátrica Integral (CENPI). Medellín, Colombia
  • Jon Duque Grajales Grupo de Neuropsicología y Conducta, Universidad de Antioquia, Medellín, Colombia.
  • Guillermo Alonso Castaño Pérez Grupo de Investigación en Salud Mental, Universidad CES. Medellín, Colombia.

Abstract

The objective of this study is to perform a comparative analysis of the cognitive functioning of a group of cannabis users and healthy controls, by applying neuropsychological tests and potential events related to mismatch negativity (MMN) and P3a in a 32-channel EEG, and evaluate its association with consumption characteristics. The sample consisted of 21 cannabis users (CN) and 22 healthy controls (SN) between 18 and 35 years old. The CN group scored higher on the WMS-III IA word list and Stroop time part A, while the SN group had reduced P3a amplitude in F3, C3, and FCZ and higher latency in F4. In relation to the characteristics of consumption, abstinence from cannabis presented a strong correlation with the percentage of retention in verbal memory, the latency of MMNd/P3a in C4 and the amplitude of P3a in F3, while the number of cannabis cigarettes presented a strong correlation with the latency of P3a in FCZ. In conclusion, our findings corroborate the presence of specific alterations. P3a stands out as a possible neurophysiological marker in clinical and translational research in this population.

Author Biographies

Luz Angela Rojas Bernal, Facultad de Ciencias de la Salud y del Deporte, Fundación Universitaria del Área Andina. Bogotá, Colombia.

MD Psiquiatra MSc PhD. Docente Investigador Facultad de Ciencias de la Salud y del Deporte, Fundación Universitaria del Área Andina. Bogotá, Colombia.

Juan Camilo Mejía Piedrahita, Grupo de investigación en Psiquiatría GIPSI, Universidad de Antioquía. Medellín, Colombia.

Psicólogo. Grupo de investigación en Psiquiatría GIPSI, Universidad de Antioquía. Medellín, Colombia.

Alejandra María Zapata Villa, Centro de Atención en Neurología Pediátrica Integral (CENPI). Medellín, Colombia

Neuropsicóloga Clínica. Centro de Atención en Neurología Pediátrica Integral (CENPI). Grupo Antioqueño de Neurología Pediátrica. Medellín, Colombia.

Jon Duque Grajales, Grupo de Neuropsicología y Conducta, Universidad de Antioquia, Medellín, Colombia.

Ingeniero Biomédico MSc. Grupo de Neuropsicología y Conducta, Universidad de Antioquia, Medellín, Colombia.

Guillermo Alonso Castaño Pérez, Grupo de Investigación en Salud Mental, Universidad CES. Medellín, Colombia.

MD MSc Drogodependencia PhD. Docente investigador Facultad de Medicina. Grupo de Investigación en Salud Mental, Universidad CES. Medellín, Colombia.

References

Referencias

Atkinson, R. J., Michie, P. T., & Schall, U. (2012). Duration mismatch negativity and P3a in first-episode psychosis and individuals at ultra-high risk of psychosis. Biological Psychiatry, 71(2), 98-104. https://doi.org/10.1016/j.biopsych.2011.08.023

Babor, T. F., Higgins-Biddle, J. C., Saunders, J. B., & Monteiro, M. G. (2001). Cuestionario de Identificación de los Transtornos debidos al Consumo de Alcohol. Pautas para su utilización en atención primaria. Ginebra: Organización Mundial de la Salud.

Beck, L. H., Bransome, E. D., Mirsky, A. F., Rosvold, H. E., & Sarason, I. (1956). A continuous performance test of brain damage. Journal of Consulting Psychology, 20(5), 343-350.

Blest-Hopley, G., Giampietro, V., & Bhattacharyya, S. (2020). A Systematic Review of Human Neuroimaging Evidence of Memory-Related Functional Alterations Associated with Cannabis Use Complemented with Preclinical and Human Evidence of Memory Performance Alterations. Brain Sciences, 10(2), E102. https://doi.org/10.3390/brainsci10020102

Broyd, S. J., Greenwood, L., van Hell, H. H., Croft, R. J., Coyle, H., Lee-Bates, B., Todd, J., Johnstone, S. J., Michie, P. T., & Solowij, N. (2016). Mismatch negativity and P50 sensory gating in abstinent former cannabis users. Neural plasticity, 2016.

Caspi, A., Moffitt, T. E., Cannon, M., McClay, J., Murray, R., Harrington, H., Taylor, A., Arseneault, L., Williams, B., & Braithwaite, A. (2005). Moderation of the effect of adolescent-onset cannabis use on adult psychosis by a functional polymorphism in the catechol-O-methyltransferase gene: Longitudinal evidence of a gene X environment interaction. Biological psychiatry, 57(10), 1117-1127.

Dougherty, D. M., Mathias, C. W., Dawes, M. A., Furr, R. M., Charles, N. E., Liguori, A., Shannon, E. E., & Acheson, A. (2013). Impulsivity, attention, memory, and decision-making among adolescent marijuana users. Psychopharmacology, 226(2), 307-319. https://doi.org/10.1007/s00213-012-2908-5

D’Souza, D. C., Fridberg, D. J., Skosnik, P. D., Williams, A., Roach, B., Singh, N., Carbuto, M., Elander, J., Schnakenberg, A., Pittman, B., Sewell, R. A., Ranganathan, M., & Mathalon, D. (2012). Dose-related modulation of event-related potentials to novel and target stimuli by intravenous ?9-THC in humans. Neuropsychopharmacology: Official Publication of the American College of Neuropsychopharmacology, 37(7), 1632-1646. https://doi.org/10.1038/npp.2012.8

Duncan, C. C., Barry, R. J., Connolly, J. F., Fischer, C., Michie, P. T., Näätänen, R., Polich, J., Reinvang, I., & Van Petten, C. (2009). Event-related potentials in clinical research: Guidelines for eliciting, recording, and quantifying mismatch negativity, P300, and N400. Clinical Neurophysiology: Official Journal of the International Federation of Clinical Neurophysiology, 120(11), 1883-1908. https://doi.org/10.1016/j.clinph.2009.07.045

Englund, A., Morrison, P. D., Nottage, J., Hague, D., Kane, F., Bonaccorso, S., Stone, J. M., Reichenberg, A., Brenneisen, R., Holt, D., Feilding, A., Walker, L., Murray, R. M., & Kapur, S. (2013). Cannabidiol inhibits THC-elicited paranoid symptoms and hippocampal-dependent memory impairment. Journal of Psychopharmacology (Oxford, England), 27(1), 19-27. https://doi.org/10.1177/0269881112460109

Garrido, M. I., Kilner, J. M., Stephan, K. E., & Friston, K. J. (2009). The mismatch negativity: A review of underlying mechanisms. Clinical Neurophysiology, 120(3), 453-463. https://doi.org/10.1016/j.clinph.2008.11.029

Gonzalez, R., Schuster, R. M., Mermelstein, R. J., Vassileva, J., Martin, E. M., & Diviak, K. R. (2012). Performance of young adult cannabis users on neurocognitive measures of impulsive behavior and their relationship to symptoms of cannabis use disorders. Journal of Clinical and Experimental Neuropsychology, 34(9), 962-976. https://doi.org/10.1080/13803395.2012.703642

Groppe, D. M., Urbach, T. P., & Kutas, M. (2011). Mass univariate analysis of event-related brain potentials/fields I: A critical tutorial review. Psychophysiology, 48(12), 1711-1725. https://doi.org/10.1111/j.1469-8986.2011.01273.x

Gruber, S. A., & Yurgelun-Todd, D. A. (2005). Neuroimaging of marijuana smokers during inhibitory processing: A pilot investigation. Brain Research. Cognitive Brain Research, 23(1), 107-118. https://doi.org/10.1016/j.cogbrainres.2005.02.016

Gutiérrez Giraldo, N., Rangel Galvis, C. E., Tovar, C., & Rafael, J. (2013). Medición del potencial evocado cognitivo, P300, en un grupo de individuos colombianos sanos. Revista Ciencias de la Salud, 11(2), 195-204.

Hart, C. L., Ilan, A. B., Gevins, A., Gunderson, E. W., Role, K., Colley, J., & Foltin, R. W. (2010). Neurophysiological and cognitive effects of smoked marijuana in frequent users. Pharmacology, Biochemistry, and Behavior, 96(3), 333-341. https://doi.org/10.1016/j.pbb.2010.06.003

Hermens, D. F., Ward, P. B., Hodge, M. A. R., Kaur, M., Naismith, S. L., & Hickie, I. B. (2010). Impaired MMN/P3a complex in first-episode psychosis: Cognitive and psychosocial associations. Progress in Neuro-Psychopharmacology & Biological Psychiatry, 34(6), 822-829. https://doi.org/10.1016/j.pnpbp.2010.03.019

Higuchi, Y., Seo, T., Miyanishi, T., Kawasaki, Y., Suzuki, M., & Sumiyoshi, T. (2014). Mismatch negativity and p3a/reorienting complex in subjects with schizophrenia or at-risk mental state. Frontiers in Behavioral Neuroscience, 8, 172. https://doi.org/10.3389/fnbeh.2014.00172

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

Javitt, D. C. (2015). Neurophysiological models for new treatment development in schizophrenia: Early sensory approaches: Neurophysiological models for schizophrenia. Annals of the New York Academy of Sciences, 1344(1), 92-104. https://doi.org/10.1111/nyas.12689

Kaur, M., Battisti, R. A., Ward, P. B., Ahmed, A., Hickie, I. B., & Hermens, D. F. (2011). MMN/P3a deficits in first episode psychosis: Comparing schizophrenia-spectrum and affective-spectrum subgroups. Schizophrenia Research, 130(1-3), 203-209. https://doi.org/10.1016/j.schres.2011.03.025

Kempel, P., Lampe, K., Parnefjord, R., Hennig, J., & Kunert, H. J. (2003). Auditory-evoked potentials and selective attention: Different ways of information processing in cannabis users and controls. Neuropsychobiology, 48(2), 95-101. https://doi.org/72884

Konings, M., Henquet, C., Maharajh, H., Hutchinson, G., & Van Os, J. (2008). Early exposure to cannabis and risk for psychosis in young adolescents in Trinidad. Acta Psychiatrica Scandinavica, 118(3), 209-213.

Lázaro, J. C. F., Solís, F. O., & Gutiérrez, A. L. (2008). Batería de funciones frontales y ejecutivas: Presentación. Revista Neuropsicología, Neuropsiquiatría y Neurociencias, 8(1), 141-158.

Light, G. A., Swerdlow, N. R., & Braff, D. L. (2007). Preattentive sensory processing as indexed by the MMN and P3a brain responses is associated with cognitive and psychosocial functioning in healthy adults. Journal of Cognitive Neuroscience, 19(10), 1624-1632. https://doi.org/10.1162/jocn.2007.19.10.1624

Light, G. A., Swerdlow, N. R., Thomas, M. L., Calkins, M. E., Green, M. F., Greenwood, T. A., Gur, R. E., Gur, R. C., Lazzeroni, L. C., Nuechterlein, K. H., Pela, M., Radant, A. D., Seidman, L. J., Sharp, R. F., Siever, L. J., Silverman, J. M., Sprock, J., Stone, W. S., Sugar, C. A., … Turetsky, B. I. (2015). Validation of mismatch negativity and P3a for use in multi-site studies of schizophrenia: Characterization of demographic, clinical, cognitive, and functional correlates in COGS-2. Schizophrenia Research, 163(1-3), 63-72. https://doi.org/10.1016/j.schres.2014.09.042

Light, G. A., Williams, L. E., Minow, F., Sprock, J., Rissling, A., Sharp, R., Swerdlow, N. R., & Braff, D. L. (2010). Electroencephalography (EEG) and Event-Related Potentials (ERPs) with Human Participants. En J. N. Crawley, C. R. Gerfen, M. A. Rogawski, D. R. Sibley, P. Skolnick, & S. Wray (Eds.), Current Protocols in Neuroscience. John Wiley & Sons, Inc. https://doi.org/10.1002/0471142301.ns0625s52

Løberg, E.-M., & Hugdahl, K. (2009). Cannabis use and cognition in schizophrenia. Frontiers in Human Neuroscience, 3, 53.

Lopez-Calderon, J., & Luck, S. J. (2014). ERPLAB: An open-source toolbox for the analysis of event-related potentials. Frontiers in Human Neuroscience, 8, 213. https://doi.org/10.3389/fnhum.2014.00213

Manly, J. J., Jacobs, D. M., Touradji, P., Small, S. A., & Stern, Y. (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. https://doi.org/10.1017/S1355617702813157

Marder, S. R., & Fenton, W. (2004). Measurement and Treatment Research to Improve Cognition in Schizophrenia: NIMH MATRICS initiative to support the development of agents for improving cognition in schizophrenia. Schizophrenia Research, 72(1), 5-9. https://doi.org/10.1016/j.schres.2004.09.010

Meier, M. H., Caspi, A., Ambler, A., Harrington, H., Houts, R., Keefe, R. S. E., McDonald, K., Ward, A., Poulton, R., & Moffitt, T. E. (2012). Persistent cannabis users show neuropsychological decline from childhood to midlife. Proceedings of the National Academy of Sciences of the United States of America, 109(40), E2657-2664. https://doi.org/10.1073/pnas.1206820109

Miller, L. S., & Rohling, M. L. (2001). A statistical interpretive method for neuropsychological test data. Neuropsychology review, 11(3), 143-169.

Moore, T. H. M., Zammit, S., Lingford-Hughes, A., Barnes, T. R. E., Jones, P. B., Burke, M., & Lewis, G. (2007). Cannabis use and risk of psychotic or affective mental health outcomes: A systematic review. Lancet (London, England), 370(9584), 319-328. https://doi.org/10.1016/S0140-6736(07)61162-3

Morgan, C. J. A., Das, R. K., Joye, A., Curran, H. V., & Kamboj, S. K. (2013). Cannabidiol reduces cigarette consumption in tobacco smokers: Preliminary findings. Addictive Behaviors, 38(9), 2433-2436. https://doi.org/10.1016/j.addbeh.2013.03.011

Morgan, C. J. A., Schafer, G., Freeman, T. P., & Curran, H. V. (2010). Impact of cannabidiol on the acute memory and psychotomimetic effects of smoked cannabis: Naturalistic study: naturalistic study [corrected]. The British Journal of Psychiatry: The Journal of Mental Science, 197(4), 285-290. https://doi.org/10.1192/bjp.bp.110.077503

Mounteney, J., Griffiths, P., Sedefov, R., Noor, A., Vicente, J., & Simon, R. (2016). The drug situation in Europe: An overview of data available on illicit drugs and new psychoactive substances from European monitoring in 2015. Addiction (Abingdon, England), 111(1), 34-48. https://doi.org/10.1111/add.13056

Murray, R. M., Englund, A., Abi-Dargham, A., Lewis, D. A., Di Forti, M., Davies, C., Sherif, M., McGuire, P., & D’Souza, D. C. (2017). Cannabis-associated psychosis: Neural substrate and clinical impact. Neuropharmacology, 124, 89-104.

Näätänen, R., Kujala, T., Kreegipuu, K., Carlson, S., Escera, C., Baldeweg, T., & Ponton, C. (2011). The mismatch negativity: An index of cognitive decline in neuropsychiatric and neurological diseases and in ageing. Brain, 134(12), 3435-3453.

Observatorio Interamericano de Drogas OAS CICAD. (2011). Protocolo de la encuesta sobre drogas en hogares. Instrumentos para la realización de los Estudios Nacionales de Drogas en Población General (pp. 1-80). Sistema Interamericano de Datos Uniformes. http://www.cicad.oas.org/oid/protocols/1_PROTOCOLO_Encuesta_Hogares_Julio_2011.pdf

OMS. (2020). Management of substance abuse: Cannabis. https://www.who.int/substance_abuse/facts/cannabis/en/

Palacio, C. A., García, J., Arbeláez, M. P., Sánchez, R., Aguirre, B., Garcés, I. C., Montoya, G. J., Gómez, J., Agudelo, A., López, C. A., Calle, J. J., Cardeño, C. A., Cano, J. F., López, M. C., Montoya, P., Herrera, C. P., González, N., González, A., Bedoya, G., … Ospina, J. (2004). [Validation of the Diagnostic Interview for Genetic Studies (DIGS) in Colombia]. Biomédica: Revista Del Instituto Nacional De Salud, 24(1), 56-62.

Pesa, N., Hermens, D. F., Battisti, R. A., Kaur, M., Hickie, I. B., & Solowij, N. (2012). Delayed preattentional functioning in early psychosis patients with cannabis use. Psychopharmacology, 222(3), 507-518. https://doi.org/10.1007/s00213-012-2676-2

Petker, T., Owens, M. M., Amlung, M. T., Oshri, A., Sweet, L. H., & MacKillop, J. (2019). Cannabis involvement and neuropsychological performance: Findings from the Human Connectome Project. Journal of Psychiatry & Neuroscience: JPN, 44(6), 414-422. https://doi.org/10.1503/jpn.180115

Polich, J. (2007). Updating P300: An integrative theory of P3a and P3b. Clinical Neurophysiology: Official Journal of the International Federation of Clinical Neurophysiology, 118(10), 2128-2148. https://doi.org/10.1016/j.clinph.2007.04.019

Pope, H. G., Gruber, A. J., Hudson, J. I., Huestis, M. A., & Yurgelun-Todd, D. (2002). Cognitive measures in long-term cannabis users. Journal of Clinical Pharmacology, 42(11 Suppl), 41S-47S.

Pozo-Hernández, E., Mariño-Tamayo, C., & Ramos-Galarza, C. (2019). Efectos neuropsicológicos por el consumo de marihuana en adultos jóvenes. Cuadernos de Neuropsicología/Panamerican Journal of Neuropsychology, 13(3).

Rabin, R. A., Barr, M. S., Goodman, M. S., Herman, Y., Zakzanis, K. K., Kish, S. J., Kiang, M., Remington, G., & George, T. P. (2017). Effects of extended cannabis abstinence on cognitive outcomes in cannabis dependent patients with schizophrenia vs non-psychiatric controls. Neuropsychopharmacology, 42(11), 2259-2271.

Rentzsch, J., Buntebart, E., Stadelmeier, A., Gallinat, J., & Jockers-Scherübl, M. C. (2011). Differential effects of chronic cannabis use on preattentional cognitive functioning in abstinent schizophrenic patients and healthy subjects. Schizophrenia Research, 130(1-3), 222-227. https://doi.org/10.1016/j.schres.2011.05.011

Rosas, R., Tenorio, M., Pizarro, M., Cumsille, P., Bosch, A., Arancibia, S., Carmona-Halty, M., Pérez-Salas, C. P., Pino, E., & Vizcarra, B. (2014). Estandarización de la Escala Wechsler de Inteligencia para Adultos: Cuarta edición en Chile. Psykhe (Santiago), 23(1), 1-18.

Ross, J. M., Ellingson, J. M., Rhee, S. H., Hewitt, J. K., Corley, R. P., Lessem, J. M., & Friedman, N. P. (2020). Investigating the causal effect of cannabis use on cognitive function with a quasi-experimental co-twin design. Drug and alcohol dependence, 206, 107712.

Schoeler, T., & Bhattacharyya, S. (2013). The effect of cannabis use on memory function: An update. Substance Abuse and Rehabilitation, 4, 11-27. https://doi.org/10.2147/SAR.S25869

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

Scott, J. C., Wolf, D. H., Calkins, M. E., Bach, E. C., Weidner, J., Ruparel, K., Moore, T. M., Jones, J. D., Jackson, C. T., Gur, R. E., & Gur, R. C. (2017). Cognitive functioning of adolescent and young adult cannabis users in the Philadelphia Neurodevelopmental Cohort. Psychology of Addictive Behaviors: Journal of the Society of Psychologists in Addictive Behaviors, 31(4), 423-434. https://doi.org/10.1037/adb0000268

Seidman, L. J., Bruder, G. E., & Giuliano, A. J. (2008). Neuropsychological Assessment and Neurophysiological Evaluation. En A. Tasman, J. Kay, J. A. Lieberman, M. B. First, & M. Maj (Eds.), Psychiatry (pp. 556-569). John Wiley & Sons, Ltd. https://doi.org/10.1002/9780470515167.ch32

Skosnik, P. D., Park, S., Dobbs, L., & Gardner, W. L. (2008). Affect processing and positive syndrome schizotypy in cannabis users. Psychiatry Research, 157(1-3), 279-282. https://doi.org/10.1016/j.psychres.2007.02.010

Solowij, N., Michie, P. T., & Fox, A. M. (1995). Differential impairments of selective attention due to frequency and duration of cannabis use. Biological psychiatry, 37(10), 731-739.

Tait, R. J., Mackinnon, A., & Christensen, H. (2011). Cannabis use and cognitive function: 8-year trajectory in a young adult cohort. Addiction (Abingdon, England), 106(12), 2195-2203. https://doi.org/10.1111/j.1360-0443.2011.03574.x

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. https://doi.org/10.1016/j.addbeh.2014.01.019

Theunissen, E. L., Kauert, G. F., Toennes, S. W., Moeller, M. R., Sambeth, A., Blanchard, M. M., & Ramaekers, J. G. (2012). Neurophysiological functioning of occasional and heavy cannabis users during THC intoxication. Psychopharmacology, 220(2), 341-350. https://doi.org/10.1007/s00213-011-2479-x

Troup, L. J., Bastidas, S., Nguyen, M. T., Andrzejewski, J. A., Bowers, M., & Nomi, J. S. (2016). An event-related potential study on the effects of cannabis on emotion processing. PLoS One, 11(2), e0149764.

Tziraki, S. (2012). Trastornos mentales y afectación neuropsicológica relacionados con el uso crónico de cannabis. Rev Neurol, 54(12), 750-760.

Umbricht, D., & Krljes, S. (2005). Mismatch negativity in schizophrenia: A meta-analysis. Schizophrenia Research, 76(1), 1-23. https://doi.org/10.1016/j.schres.2004.12.002

Urine testing for drugs of abuse. (1986). NIDA Research Monograph, 73, 1-114.

Verdejo-García, A. (2011). Efectos neuropsicológicos del consumo de cannabis. Trastornos adictivos, 13(3), 97-101.

Volkow, N. D. (2009). Substance Use Disorders in Schizophrenia—Clinical Implications of Comorbidity. Schizophrenia Bulletin, 35(3), 469-472. https://doi.org/10.1093/schbul/sbp016

Volkow, N. D., Swanson, J. M., Evins, A. E., DeLisi, L. E., Meier, M. H., Gonzalez, R., Bloomfield, M. A., Curran, H. V., & Baler, R. (2016). Effects of cannabis use on human behavior, including cognition, motivation, and psychosis: A review. JAMA psychiatry, 73(3), 292-297.

Wechsler, D. (2004). Escala de Memoria de Wechsler III: Manual de aplicación. Madrid: tea Ediciones SA.

Wechsler, D., Meng, Y., Martínez, I., & Zhu, J. (2014). WAIS-IV: Escala Wechsler de Inteligencia para Adultos-IV. El Manual Moderno.

Zamora, R. C., Von Seggern, B., Toledo, R., & Harrell, E. H. (1990). El inventario de Edimburgo: Evaluación de la lateralidad cerebral en una población mexicana. Salud mental, 13(2), 11-17.

Published

2023-09-18

Versions