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Δ9-Tetrahydrocannabinol at Retrieval Drives False Recollection of Neutral and Emotional Memories

      Abstract

      Background

      It is well established that the main psychoactive constituent of cannabis, Δ9-tetrahydrocannabinol (THC), impairs episodic memory encoding and modulates emotional processing, but little is known about the impact of THC during the retrieval of emotional episodic memories. With the rise of cannabis to treat medical conditions, including those characterized by emotional and episodic memory disturbances, there is an urgent need to determine the effects of THC on memory accuracy and distortion. Here, we report the first study investigating the effects of THC during retrieval of neutral and emotional episodic memories.

      Methods

      Using a double-blind, placebo-controlled, within-subjects design, healthy volunteers (N = 23) viewed negative, neutral, and positive pictures (emotional memory task) and lists of semantically related words (false memory task). Forty-eight hours later, participants ingested a capsule containing either THC (15 mg) or placebo and completed tasks to test their memories for the previously studied pictures and words.

      Results

      THC during retrieval did not reduce the number of correct responses to studied items. Instead, it robustly increased false recollection on both the emotional memory and false memory tasks. This effect was found for both neutral and emotional items.

      Conclusions

      These findings show that THC has adverse effects during memory retrieval, distorting both neutral and emotional memories. Coupled with THC’s known effects during encoding, these new retrieval findings are important in light of the spreading acceptance of cannabis.

      Keywords

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      References

        • Curran H.V.
        • Freeman T.P.
        • Mokrysz C.
        • Lewis D.A.
        • Morgan C.J.
        • Parson L.H.
        Keep off the grass? Cannabis, cognition and addiction.
        Nat Rev Neurosci. 2016; 17: 293-306
        • Ilan A.B.
        • Smith M.E.
        • Gevins A.
        Effects of marijuana on neurophysiological signals of working and episodic memory.
        Psychopharmacology (Berl). 2004; 176: 214-222
        • Miller L.L.
        • McFarland D.
        • Cornett T.L.
        • Brightwell D.
        Marijuana and memory impairment: Effect on free recall and recognition memory.
        Pharmacol Biochem Behav. 1977; 7: 99-103
        • Ballard M.E.
        • Gallo D.A.
        • de Wit H.
        Psychoactive drugs and false memory: Comparison of dextroamphetamine and delta-9-tetrahydrocannabinol on false recognition.
        Psychopharmacology (Berl). 2012; 219: 15-24
        • Ballard M.E.
        • Gallo D.A.
        • de Wit H.
        Pre-encoding administration of amphetamine or THC preferentially modulates emotional memory in humans.
        Psychopharmacology (Berl). 2013; 226: 515-529
        • Ranganathan M.
        • Radhakrishnan R.
        • Addy P.H.
        • Schnakenberg-Martin A.M.
        • Williams A.H.
        • Carbuto M.
        • et al.
        Tetrahydrocannabinol (THC) impairs encoding but not retrieval of verbal information.
        Prog Neuropsychopharmacol Biol Psychiatry. 2017; 79: 176-183
        • Ballard M.E.
        • Bedi G.
        • de Wit H.
        Effects of delta-9-tetrahydrocannabinol on evaluation of emotional images.
        J Psychopharmacol. 2012; 26: 1289-1298
        • Hindocha C.
        • Freeman T.P.
        • Schafer G.
        • Gardener C.
        • Das R.K.
        • Morgan C.J.A.
        • Curran H.V.
        Acute effects of delta-9-tetrahydrocannabinol, cannabidiol and their combination on facial emotion recognition: A randomised, double-blind, placebo-controlled study in cannabis users.
        Eur Neuropsychopharmacol. 2015; 25: 325-334
        • Phan K.L.
        • Angstadt M.
        • Golden J.
        • Onyewuenyi I.
        • Popovska A.
        • de Wit H.
        Cannabinoid modulation of amygdala reactivity to social signals of threat in humans.
        J Neurosci. 2008; 28: 2313-2319
        • Rubin D.C.
        • Berntsen D.
        • Bohni M.K.
        A memory-based model of posttraumatic stress disorder: Evaluating basic assumptions underlying the PTSD diagnosis.
        Psychol Rev. 2008; 115: 985-1011
        • Grant S.
        • Pedersen E.R.
        • Neighbors C.
        Associations of posttraumatic stress disorder symptoms with marijuana and synthetic cannabis use among young adult U.S. veterans: A pilot investigation.
        J Stud Alcohol Drugs. 2016; 77: 509-514
        • Kevorkian S.
        • Bonn-Miller M.O.
        • Belendiuk K.
        • Carney D.M.
        • Roberson-Nay R.
        • Berenz E.C.
        Associations among trauma, posttraumatic stress disorder, cannabis use, and cannabis use disorder in a nationally representative epidemiologic sample.
        Psychol Addict Behav. 2015; 29: 633-638
        • Bossong M.G.
        • Jager G.
        • van Hell H.H.
        • Zuurman L.
        • Jansma J.M.
        • Mehta M.A.
        • et al.
        Effects of Δ9-tetrahydrocannabinol administration on human encoding and recall memory function: A pharmacological fMRI study.
        J Cogn Neurosci. 2012; 24: 588-599
        • Bossong M.G.
        • Jansma J.M.
        • van Hell H.H.
        • Jager G.
        • Oudman E.
        • Saliasi E.
        • et al.
        Effects of Δ9-tetrahydrocannabinol on human working memory function.
        Biol Psychiatry. 2012; 71: 693-699
        • Gallo D.A.
        Associative Illusions of Memory: False Memory Research in DRM and Related Tasks.
        Psychology Press, New York, NY2006
        • Yager L.M.
        • Garcia A.F.
        • Wunsch A.M.
        • Ferguson S.M.
        The ins and outs of the striatum: Role in drug addiction.
        Neuroscience. 2015; 301: 529-541
        • Scimeca J.M.
        • Badre D.
        Striatal contributions to declarative memory retrieval.
        Neuron. 2012; 75: 380-392
        • King D.R.
        • Chastelaine M.
        • Elward R.L.
        • Wang T.H.
        • Rugg M.D.
        Dissociation between the neural correlates of recollection and familiarity in the striatum and hippocampus: Across-study convergence.
        Behav Brain Res. 2018; 354: 1-7
        • Speer M.E.
        • Bhanji J.P.
        • Delgado M.R.
        Savoring the past: Positive memories evoke value representations in the striatum.
        Neuron. 2014; 84: 847-856
        • Abe N.
        • Okuda J.
        • Suzuki M.
        • Sasaki H.
        • Matsuda T.
        • Mori E.
        • et al.
        Neural correlates of true memory, false memory, and deception.
        Cereb Cortex. 2008; 18: 2811-2819
        • Ballard M.E.
        • Gallo D.A.
        • de Wit H.
        Amphetamine increases errors during episodic memory retrieval.
        J Clin Psychopharmacol. 2014; 34: 85-92
        • Doss M.K.
        • Weafer J.
        • Gallo D.A.
        • de Wit H.
        MDMA impairs both the encoding and retrieval of emotional recollections.
        Neuropsychopharmacology. 2018; 43: 791-800
        • Gallo D.A.
        False memories and fantastic beliefs: 15 years of the DRM illusion.
        Mem Cognit. 2010; 38: 833-848
        • White T.L.
        • Justice A.J.
        • de Wit H.
        Differential subjective effects of D-amphetamine by gender, hormone levels and menstrual cycle phase.
        Pharmacol Biochem Behav. 2002; 73: 729-741
        • Lang P.J.
        • Bradley M.M.
        • Cuthbert B.N.
        International Affective Picture System (IAPS): Technical Manual and Affective Ratings.
        National Institute of Mental Health Center for the Study of Emotion and Attention, Gainesville, FL1997
        • Marchewka A.
        • Żurawski Ł.
        • Jednoróg K.
        • Grabowska A.
        The Nencki Affective Picture System (NAPS): Introduction to a novel, standardized, wide-range, high-quality, realistic picture database.
        Behav Res Methods. 2014; 46: 596-610
        • Gallo D.A.
        • Foster K.T.
        • Johnson E.L.
        Elevated false recollection of emotional pictures in younger and older adults.
        Psychol Aging. 2009; 24: 981-988
        • Wachtel S.R.
        • ElSohly M.A.
        • Ross S.A.
        • Ambre J.
        • de Wit H.
        Comparison of the subjective effects of delta-9-tetrahydrocannabinol and marijuana in humans.
        Psychopharmacology (Berl). 2002; 161: 331-339
        • Yonelinas A.P.
        The nature of recollection and familiarity: A review of 30 years of research.
        J Mem Lang. 2002; 46: 441-517
        • Martin W.R.
        • Sloan J.W.
        • Sapira J.D.
        • Jasinski D.R.
        Physiologic, subjective, and behavioral effects of amphetamine, methamphetamine, ephedrine, phenmetrazine, and methylphenidate in man.
        Clin Pharmacol Ther. 1971; 12: 245-258
        • Folstein M.F.
        • Luria R.
        Reliability, validity, and clinical application of the Visual Analogue Mood Scale.
        Psychol Med. 1973; 3: 479-486
        • Morean M.E.
        • de Wit H.
        • King A.C.
        • Sofuoglu M.
        • Rueger S.Y.
        • O’Malley S.S.
        The Drug Effects Questionnaire: Psychometric support across three drug types.
        Psychopharmacology (Berl). 2013; 227: 177-192
        • Doss M.K.
        THC at retrieval drives false recollection of neutral and emotional episodic memories [dataset]. Open Science Framework.
        (Available at:) (Accessed May 20, 2018)
        • Hart C.L.
        • Ilan A.B.
        • Gevins A.
        • Gunderson E.W.
        • Role K.
        • Colley J.
        • Foltin R.W.
        Neurophysiological and cognitive effects of smoked marijuana in frequent users.
        Pharmacol Biochem Behav. 2010; 96: 333-341
        • Miller L.
        • Cornett T.
        • McFarland D.
        Marijuana: An analysis of storage and retrieval deficits in memory with the technique of restricted reminding.
        Pharmacol Biochem Behav. 1978; 8: 327-332
        • Ames F.
        A clinical and metabolic study of acute intoxication with cannabis sativa and its role in the model psychoses.
        J Ment Sci. 1958; 104: 972-999
        • Tart C.T.
        Marijuana intoxication: Common experiences.
        Nature. 1970; 226: 701-704
        • Morgan C.J.
        • Rothwell E.
        • Atkinson H.
        • Mason O.
        • Curran H.V.
        Hyper-priming in cannabis users: A naturalistic study of the effects of cannabis on semantic memory function.
        Psychiatry Res. 2010; 176: 213-218
        • Schafer G.
        • Feilding A.
        • Morgan C.J.
        • Agathangelou M.
        • Freeman T.P.
        • Curran H.V.
        Investigating the interaction between schizotypy, divergent thinking and cannabis use.
        Conscious Cogn. 2012; 21: 292-298
        • Doss M.K.
        • Bluestone M.R.
        • Gallo D.A.
        Two mechanisms of constructive recollection: Perceptual recombination and conceptual fluency.
        J Exp Psychol Learn Mem Cogn. 2016; 42: 1747-1758
        • Bohn A.
        • Berntsen D.
        Pleasantness bias in flashbulb memories: Positive and negative flashbulb memories of the fall of the Berlin Wall among East and West Germans.
        Mem Cognit. 2007; 35: 565-577
        • Kensinger E.A.
        • Schacter D.L.
        When the Red Sox shocked the Yankees: Comparing negative and positive memories.
        Psychon Bull Rev. 2006; 13: 757-763
        • Levine L.J.
        • Bluck S.
        Painting with broad strokes: Happiness and the malleability of event memory.
        Cogn Emot. 2004; 18: 559-574
        • Radhakrishnan R.
        • Wilkinson S.T.
        • D’Souza D.C.
        Gone to pot – A review of the association between cannabis and psychosis.
        Front Psychiatry. 2014; 5: 54
        • Strange D.
        • Takarangi M.K.T.
        Memory distortion for traumatic events: The role of mental imagery.
        Front Psychiatry. 2015; 6: 27
        • McNally R.J.
        Recovering memories of trauma.
        Curr Dir Psychol Sci. 2003; 12: 32-35
        • Piper A.
        "Truth serum" and "recovered memories" of sexual abuse: A review of the evidence.
        J Psychiatry Law. 1993; 21: 447-471
        • Tull M.T.
        • McDermott M.J.
        • Gratz K.L.
        Marijuana dependence moderate the effect of posttraumatic stress disorder on trauma cue reactivity in substance dependent patients.
        Drug Alcohol Depend. 2016; 159: 219-226
        • Yarnell S.
        The use of medicinal marijuana for posttraumatic stress disorder: A review of the current literature.
        Prim Care Companion CNS Disord. 2015; 17: 15r01786