Skip to main content
Log in

Effects of marijuana on neurophysiological signals of working and episodic memory

  • Original Investigation
  • Published:
Psychopharmacology Aims and scope Submit manuscript

Abstract

Rationale

The primary psychoactive constituent of marijuana, Δ9-THC, activates cannabinoid receptors, which are especially abundant in the frontal cortex and hippocampus. Acute marijuana smoking can disrupt working memory (WM) and episodic memory (EM) functions that are known to rely on these regions. However, the effects of marijuana on the brain activity accompanying such cognitive processes remain largely unexplored.

Objectives

To examine such effects on performance and neurophysiological signals of these functions, EEG recordings were obtained from ten subjects (5M, 5F) performing cognitive tasks before and after smoking marijuana (3.45% Δ9-THC) or a placebo. WM was assessed with a spatial N-back task, and EM was evaluated with a test requiring recognition of words after a 5–10 min delay between study and test.

Results

Marijuana increased heart rate and decreased global theta band EEG power, consistent with increased autonomic arousal. Responses in the WM task were slower and less accurate after smoking marijuana, accompanied by reduced alpha band EEG reactivity in response to increased task difficulty. In the EM task, marijuana was associated with an increased tendency to erroneously identify distracter words as having been previously studied. In both tasks, marijuana attenuated stimulus-locked event-related potentials (ERPs).

Conclusions

The results suggest that marijuana disrupted both sustained and transient attention processes resulting in impaired memory task performance. In subjects most affected by marijuana a pronounced ERP difference between previously studied words and new distracter words was also reduced, suggesting disruption of neural mechanisms underlying memory for recent study episodes.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Azorlosa JL, Heishman SJ, Stitzer ML, Mahaffey JM (1992) Marijuana smoking: effect of varying delta 9-tetrahydrocannabinol content and number of puffs. J Pharmacol Exp Ther 261:114–122

    CAS  PubMed  Google Scholar 

  • Baddeley A, Hitch G (1974) Working memory. In: Bower G (ed) Recent advances in learning and motivation. Academic, New York, pp 47–90

  • Bauer LO (2001) Electroencephalographic studies of substance use and abuse. In: Kaufman MJ (ed) Brain imaging in substance abuse: research, clinical, and forensic applications. Humana, Totowa, New Jersey, pp 77–112

  • Block RI, O’Leary DS, Ehrhardt JC, Augustinack JC, Ghoneim MM, Arndt S, Hall JA (2000) Effects of frequent marijuana use on brain tissue volume and composition. Neuroreport 11:491–496

    CAS  PubMed  Google Scholar 

  • Brewer JB, Zhao Z, Desmond JE, Glover GH, Gabrieli JD (1998) Making memories: brain activity that predicts how well visual experience will be remembered. Science 281:1185–1187

    Article  CAS  PubMed  Google Scholar 

  • Chait LD, Pierri J (1992) Effects of smoked marijuana on human performance: a critical review. In: Murphy L, Bartke A (eds) Marijuana/cannabinoids: neurobiology and neurophysiology. CRC, Boca Raton, Fla., pp 387–424

  • Comings DE, Muhleman D, Gade R, Johnson P, Verde R, Saucier G, MacMurray J (1997) Cannabinoid receptor gene (CNR1): association with i.v. drug use. Mol Psychiatry 2:161–168

    Article  CAS  PubMed  Google Scholar 

  • Curran T, Schacter DL, Norman KA, Galluccio L (1997) False recognition after a right frontal lobe infarction: memory for general and specific information. Neuropsychologia 35:1035–1049

    Article  CAS  PubMed  Google Scholar 

  • Devane WA, Dysarz FA III, Johnson MR, Melvin LS, Howlett AC (1988) Determination and characterization of a cannabinoid receptor in rat brain. Mol Pharmacol 34:605–613

    CAS  PubMed  Google Scholar 

  • Du W, Leong HM, Gevins AS (1994) Ocular artifact minimization by adaptive filtering. Proceedings of the Seventh IEEE SP Workshop on Statistical Signal and Array Processing, Quebec City, Canada, pp 433–436

  • Earleywine M (2002) Understanding marijuana. Oxford University, Oxford

  • ElSohly MA, Ross SA, Mehmedic Z, Arafat R, Yi B, Banahan BF III (2000) Potency trends of delta9-THC and other cannabinoids in confiscated marijuana from 1980–1997. J Forens Sci 45:24–30

    CAS  PubMed  Google Scholar 

  • Engelkamp J, Zimmer H (2001) Categorical and order information in free recall of action phrases. Psicologica 22:71–96

    Google Scholar 

  • Fant RV, Heishman SJ, Bunker EB, Pickworth WB (1998) Acute and residual effects of marijuana in humans. Pharmacol Biochem Behav 60:777–784

    CAS  PubMed  Google Scholar 

  • Fink M (1976) Effects of acute and chronic inhalation of hashish, marijuana, and delta 9-tetrahydrocannabinol on brain electrical activity in man: evidence for tissue tolerance. Ann N Y Acad Sci 282:387–398

    CAS  PubMed  Google Scholar 

  • Friedman D (1990) ERPs during continuous recognition memory for words. Biol Psychol 30:61–87

    Article  CAS  PubMed  Google Scholar 

  • Gaoni Y, Mechoulam R (1964) Isolation, structure, and partial synthesis of active constituent of hashish. J Am Chem Soc 86:1646–1647

    CAS  Google Scholar 

  • Gevins AS, Schaffer RE (1980) A critical review of electroencephalographic EEG correlates of higher cortical functions. Crit Rev Bioeng 4:113–164

    CAS  Google Scholar 

  • Gevins A, Smith ME (2000) Neurophysiological measures of working memory and individual differences in cognitive ability and cognitive style. Cereb Cortex 10:829–839

    Article  CAS  PubMed  Google Scholar 

  • Gevins AS, Bressler SL, Cutillo BA, Illes J, Miller JC, Stern J, Jex HR (1990) Effects of prolonged mental work on functional brain topography. Electroencephalogr Clin Neurophysiol 76:339–350

    CAS  PubMed  Google Scholar 

  • Gevins AS, Smith ME, Le J, Leong H, Bennett J, Martin N, McEvoy L, Du R, Whitfield S (1996) High resolution evoked potential imaging of the cortical dynamics of human working memory. Electroencephalogr Clin Neurophysiol 98:327–348

    Article  CAS  PubMed  Google Scholar 

  • Gevins A, Smith ME, McEvoy L, Yu D (1997) High-resolution EEG mapping of cortical activation related to working memory: effects of task difficulty, type of processing, and practice. Cereb Cortex 7:374–385

    Article  CAS  PubMed  Google Scholar 

  • Gevins A, Smith ME, Leong H, McEvoy L, Whitfield S, Du R, Rush G (1998) Monitoring working memory load during computer-based tasks with EEG pattern recognition methods. Hum Fact 40:79–91

    CAS  PubMed  Google Scholar 

  • Goldman-Rakic P (1987) Circuitry of primate prefrontal cortex and regulation of behavior by representational memory. In: Plum F, Mountcastle V (eds) Handbook of physiology, the nervous system—higher functions of the brain. American Physiological Society, Bethesda, Md., pp 373–417

  • Halgren E, Smith ME (1987) Cognitive evoked potentials as modulatory processes in human memory formation and retrieval. Hum Neurobiol 6:129–139

    CAS  PubMed  Google Scholar 

  • Hampson RE, Deadwyler SA (1999) Cannabinoids, hippocampal function and memory. Life Sci 65:715–723

    CAS  PubMed  Google Scholar 

  • Heit G, Smith ME, Halgren E (1988) Neural encoding on individual words and faces by the human hippocampus and amygdala. Nature 333:773–775

    CAS  PubMed  Google Scholar 

  • Herkenham M, Lynn AB, Little MD, Johnson MR, Melvin LS, de Costa BR, Rice KC (1990) Cannabinoid receptor localization in brain. Proc Natl Acad Sci USA 87:1932–1936

    CAS  PubMed  Google Scholar 

  • Hooker WD, Jones RT (1987) Increased susceptibility to memory intrusions and the Stroop interference effect during acute marijuana intoxication. Psychopharmacology 91:20–24

    CAS  PubMed  Google Scholar 

  • Huestis MA, Sampson AH, Holicky BJ, Henningfield JE, Cone EJ (1992) Characterization of the absorption phase of marijuana smoking. Clin Pharmacol Ther 52:31–41

    CAS  PubMed  Google Scholar 

  • Ilan AB, Gevins A (2001) Prolonged neurophysiological effects of cumulative wine drinking. Alcohol 25:137–152

    Article  CAS  PubMed  Google Scholar 

  • Iversen LL (2000) The science of marijuana. Oxford University, New York

  • Iversen L (2003) Cannabis and the brain. Brain 126:1252–1270

    Article  PubMed  Google Scholar 

  • Johnson JP, Muhleman D, MacMurray J, Gade R, Verde R, Ask M, Kelley J, Comings DE (1997) Association between the cannabinoid receptor gene (CNR1) and the P300 event-related potential. Mol Psychiatry 2:169–171

    Article  CAS  PubMed  Google Scholar 

  • Jonides J, Smith EE, Koeppe RA, Awh E, Minoshima S, Mintun M (1993) Spatial working memory in humans as revealed by PET. Nature 363:623–625

    CAS  PubMed  Google Scholar 

  • Joy JE, Watson SJ Jr, Benson JA Jr (1999) Marijuana and medicine: assessing the science base. National Academy, Washington D.C.

    Google Scholar 

  • Kirk JM, Doty P, de Wit H (1998) Effects of expectancies on subjective responses to oral delta9-tetrahydrocannabinol. Pharmacol Biochem Behav 59:287–293

    CAS  PubMed  Google Scholar 

  • Lee AC, Robbins TW, Owen AM (2000) Episodic memory meets working memory in the frontal lobe: functional neuroimaging studies of encoding and retrieval. Crit Rev Neurobiol 14:165–197

    CAS  PubMed  Google Scholar 

  • Lukas SE, Mendelson JH, Benedikt R (1995) Electroencephalographic correlates of marihuana-induced euphoria. Drug Alcohol Depend 37:131–140

    Article  CAS  PubMed  Google Scholar 

  • Manns JR, Hopkins RO, Reed JM, Kitchener EG, Squire LR (2003) Recognition memory and the human hippocampus. Neuron 37:171–180

    CAS  PubMed  Google Scholar 

  • Mathew RJ, Wilson WH, Turkington TG, Coleman RE (1998) Cerebellar activity and disturbed time sense after THC. Brain Res 797:183–189

    Article  CAS  PubMed  Google Scholar 

  • McCallister TW, Sparling MB, Flashman LA, Gueirn SJ, Mamourian AC, Saykin AJ (2001) Differential working memory load effects after mild traumatic brain injury. Neuroimage 14:1004–1012

    Article  PubMed  Google Scholar 

  • McCarthy G, Blamire AM, Puce A, Nobre AC, Bloch G, Hyder F, Goldman-Rakic P, Shulman RG (1994) Functional magnetic resonance imaging of human prefrontal cortex activation during a spatial working memory task. Proc Natl Acad Sci USA 91:8690–8694

    CAS  PubMed  Google Scholar 

  • McEvoy LK, Smith ME, Gevins A (1998) Dynamic cortical networks of verbal and spatial working memory: effects of memory load and task practice. Cereb Cortex 8:563–574

    Article  CAS  PubMed  Google Scholar 

  • McEvoy LK, Smith ME, Gevins A (2000) Test–retest reliability of cognitive EEG. Clin Neurophysiol 111:457–463

    Article  CAS  PubMed  Google Scholar 

  • Miller LL, McFarland D, Cornett TL, Brightwell D (1977) Marijuana and memory impairment: effect on free recall and recognition memory. Pharmacol Biochem Behav 7:99–103

    Article  CAS  PubMed  Google Scholar 

  • Miller L, Cornett T, McFarland D (1978) Marijuana: an analysis of storage and retrieval deficits in memory with the technique of restricted reminding. Pharmacol Biochem Behav 8:327–332

    Article  CAS  PubMed  Google Scholar 

  • Mouzak A, Agathos P, Kerezoudi E, Mantas A, Vourdeli-Yiannakoura E (2000) Transient ischemic attack in heavy cannabis smokers—how “safe” is it? Eur Neurol 44:42–44

    Article  CAS  PubMed  Google Scholar 

  • Niedermeyer E (1993) The normal EEG of the waking adult. In: Niedermeyer E, Lopes da Silva F (eds) Electroencephalography. Basic principles, clinical applications, and related fields. Williams and Wilkins, Baltimore, pp 131–152

  • O’Brien CP (1996) Drug addiction and drug abuse. In: Hardman JG, Limbird LE, Molinoff PB, Ruddon RW, Gilman AG (eds) Goodman and Gilman’s the pharmacological basis of therapeutics. McGraw-Hill, New York, pp 557–577

  • O’Leary DS, Block RI, Koeppel JA, Flaum M, Schultz SK, Andreasen NC, Ponto LB, Watkins GL, Hurtig RR, Hichwa RD (2002) Effects of smoking marijuana on brain perfusion and cognition. Neuropsychopharmacology 26:802–816

    Article  CAS  PubMed  Google Scholar 

  • Perlstein WM, Dixit NK, Carter CS, Noll DC, Cohen JD (2003) Prefrontal cortex dysfunction mediates deficits in working memory and prepotent responding in schizophrenia. Biol Psychiatry 53:25–38

    Article  PubMed  Google Scholar 

  • Pfurtscheller G, Stancak A Jr, Neuper C (1996) Event-related synchronization (ERS) in the alpha band—an electrophysiological correlate of cortical idling: a review. Int J Psychophysiol 24:39–46

    Google Scholar 

  • Pollan M (2001) The botany of desire. Random House, New York

  • Rugg MD, Nagby ME (1989) Event-related potentials and recognition memory for words. Electroencephalogr Clin Neurophysiol 72:395–406

    Article  CAS  PubMed  Google Scholar 

  • Rugg MD, Roberts RC, Potter DD, Pickles CD, Nagy ME (1991) Event-related potentials related to recognition memory. Effects of unilateral temporal lobectomy and temporal lobe epilepsy. Brain 114:2313–2332

    PubMed  Google Scholar 

  • Schacter DL, Curran T, Galluccio L, Milberg WP, Bates JF (1996) False recognition and the right frontal lobe: a case study. Neuropsychologia 34:793–808

    Article  CAS  PubMed  Google Scholar 

  • Schmidt LG, Samochowiec J, Finckh U, Fiszer-Piosik E, Horodnicki J, Wendel B, Rommelspacher H, Hoehe MR (2002) Association of a CB1 cannabinoid receptor gene (CNR1) polymorphism with severe alcohol dependence. Drug Alcohol Depend 65:221–224

    Article  CAS  PubMed  Google Scholar 

  • Smith ME (1993) Neurophysiological manifestations of recollective experience during recognition judgments. J Cognit Neurosci 5:1–13

    Google Scholar 

  • Smith ME, Guster K (1993) Decomposition of recognition memory event-related potentials yields target, repetition, and retrieval effects. Electroencephalogr Clin Neurophysiol 86:335–343

    Article  CAS  PubMed  Google Scholar 

  • Smith ME, Halgren E (1989) Dissociation of recognition memory components following temporal lobe lesions. J Exp Psychol [Learn Mem Cognit] 15:50–60

    Article  CAS  PubMed  Google Scholar 

  • Smith ME, Stapleton JM, Halgren E (1986) Human medial temporal lobe potentials evoked in memory and language tasks. Electroencephalogr Clin Neurophysiol 63:145–159

    Article  CAS  PubMed  Google Scholar 

  • Snodgrass JG, Corwin J (1988) Pragmatics of measuring recognition memory: applications to dementia and amnesia. J Exp Psychol [Gen] 117

    Google Scholar 

  • Solowij N (1995) Do cognitive impairments recover following cessation of cannabis use? Life Sci 56:2119–2126

    Article  CAS  PubMed  Google Scholar 

  • Squire LR, Knowlton BJ (1995) Memory, hippocampus, and brain systems. In: Gazzaniga MS (ed) The cognitive neurosciences. MIT, Cambridge, Mass., pp 825–837

  • Squire LR, Knowlton B (2000) The medial temporal lobe, the hippocampus, and the memory systems of the brain. In: Gazzaniga MS (ed) The new cognitive neurosciences. MIT, Cambridge, Mass.

  • Struve FA, Manno BR, Kemp P, Patrick G, Manno JE (2003) Acute marihuana (THC) exposure produces a “transient” topographic quantitative EEG profile identical to the “persistent” profile seen in chronic heavy users. Clin Electroencephalogr 34:75–83

    PubMed  Google Scholar 

  • Terranova JP, Storme JJ, Lafon N, Perio A, Rinaldi-Carmona M, Le Fur G, Soubrie P (1996) Improvement of memory in rodents by the selective CB1 cannabinoid receptor antagonist, SR 141716. Psychopharmacology 126:165–172

    CAS  PubMed  Google Scholar 

  • Thomas BF, Parker VL, Caddell LW, Jones LV, Sabharwal SK, McDaniel AI, Keimowitz AR, Scheffler NM, Hart ED, Mitchell JM, Davis KHJ (1999) Composition and stability of a standard marihuana cigarette. In: Nahas GG, Sutin KM, Harvey DJ, Agurell S (eds) Marihuana and medicine. Humana, Totowa, New Jersey, pp 137–143

  • Torsvall L, Åkerstedt T (1988) Extreme sleepiness: quantification of EOG and spectral EEG parameters. Int J Neurosci 38:435–441

    CAS  PubMed  Google Scholar 

  • Tulving E (1983) Elements of episodic memory. Oxford University, New York

  • Tulving E (2002) Episodic memory: from mind to brain. Annu Rev Psychol 23:1–25

    Article  Google Scholar 

  • Varvel SA, Lichtman AH (2002) Evaluation of CB(1) receptor knockout mice in the morris water maze. J Pharmacol Exp Ther 301:915–924

    Article  CAS  PubMed  Google Scholar 

  • Wachtel SR, ElSohly MA, Ross SA, Ambre J, de Wit H (2002) Comparison of the subjective effects of Delta(9)-tetrahydrocannabinol and marijuana in humans. Psychopharmacology 161:331–339

    CAS  PubMed  Google Scholar 

  • Watter S, Geffen GM, Geffen LB (2001) The n-back as a dual-task: P300 morphology under divided attention. Psychophysiology 38:998–1003

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This research was supported by a grant from the National Institute on Drug Abuse. We gratefully acknowledge the dedicated effort of Elizabeth Nichols during data acquisition and analysis, the contributions of Patrick Sullivan and An Jiang in developing the software used to collect and analyze the neurophysiological data, and Dr. Linda McEvoy for scientific advice and guidance. The experiment complied with the current laws of the United States of America.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Aaron B. Ilan.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ilan, A.B., Smith, M.E. & Gevins, A. Effects of marijuana on neurophysiological signals of working and episodic memory. Psychopharmacology 176, 214–222 (2004). https://doi.org/10.1007/s00213-004-1868-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00213-004-1868-9

Keywords

Navigation