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Joint effects of stress and chronic cannabis use on prospective memory

  • Carrie CuttlerEmail author
  • Alexander Spradlin
  • Amy T. Nusbaum
  • Paul Whitney
  • John M. Hinson
  • Ryan J. McLaughlin
Original Investigation

Abstract

Rationale

Prospective memory pervades our daily lives and failures can have detrimental consequences. This ability to execute delayed intentions may be impacted by stress, yet few studies have examined these effects. Moreover, as many cannabis users report using cannabis to cope with stress, it is important to understand how stress impacts memory in cannabis users.

Objectives

We assessed the effects of acute and chronic stress on prospective memory to examine whether stress differentially impacts prospective memory in cannabis users vs. non-users.

Methods

Forty cannabis users and 42 non-users were assigned an episodic and a habitual prospective memory test before completing either the stress or no stress condition of the Maastricht Acute Stress Test (MAST). Participants were instructed to execute the habitual test during the MAST and the episodic test shortly after the MAST. Chronic stress was measured using the Perceived Stress Scale, and acute stress was measured using subjective ratings and cortisol.

Results

There was a main effect of acute stress indicating that stress detrimentally impacted habitual prospective memory performance. Although there was not a significant stress x cannabis interaction, further planned comparisons indicated the habitual prospective memory impairment was selective to cannabis users. There were also significant negative correlations between (i) episodic prospective memory and both subjective stress as well as chronic stress, and (ii) habitual prospective memory and change in subjective stress.

Conclusions

This study is the first to reveal detrimental effects of acute stress on prospective memory performance, which may be exacerbated in cannabis users.

Keywords

Prospective memory Cannabis Acute stress Chronic stress Cortisol 

Notes

Funding information

Washington State University’s Dedicated Marijuana Account funded this study using excised tax dollars from the sales of recreational cannabis.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Andreano JM, Cahill L (2006) Glucocorticoid release and memory consolidation in men and women. Psychol Sci 17:466–470.  https://doi.org/10.1111/j.1467-9280.2006.01729.x CrossRefPubMedPubMedCentralGoogle Scholar
  2. Atsak P, Roozendaal B, Campolongo P (2012) Role of the endocannabinoid system in regulating glucocorticoid effects on memory for emotional experiences. Neuroscience 204:104–116.  https://doi.org/10.1016/j.neuroscience.2011.08.047 CrossRefPubMedPubMedCentralGoogle Scholar
  3. Bhattacharyya S, Morrison PD, Fusar-Poli P, Martin-Santos R, Borgwardt S, Winton-Brown T, Nosarti C, O' Carroll CM, Seal M, Allen P, Mehta MA, Stone JM, Tunstall N, Giampietro V, Kapur S, Murray RM, Zuardi AW, Crippa JA, Atakan Z, McGuire PK (2010) Opposite effects of Δ-9-tetrahydrocannabinol and cannabidiol on human brain function and psychopathology. Neuropsychopharmacology 35:764–774.  https://doi.org/10.1038/npp.2009.184 CrossRefPubMedGoogle Scholar
  4. Bhattacharyya S, Egerton A, Kim E, Rosso L, Barros DR, Hammers A, Brammer M, Turkheimer FE, Howes OD, McGuire P (2017) Acute induction of anxiety in humans by delta-9-tetrahydrocannabinol related to amygdalar cannabinoid-1 (CB!) receptors. Sci Rep 7:15025.  https://doi.org/10.1038/s41598-017-14203-4 CrossRefPubMedPubMedCentralGoogle Scholar
  5. Braidwood R, Mansell S, Waldron J, Rendell PG, Kamboj SK, Curran HV (2018) Non-dependent and dependent daily cannabis users differ in mental health but not prospective memory ability. Front Psychiatry 9.  https://doi.org/10.3389/fpsyt.2018.00097
  6. Broyd SJ, van Hell HH, Beale C, Yücel M, Solowij N (2016) Acute and chronic effects of cannabinoids on human cognition – a systematic review. Biol Psychiatry 79:557–567.  https://doi.org/10.1016/j.biopsych.2015.12.002 CrossRefPubMedGoogle Scholar
  7. Childs E, Lutz AA, de Wit H (2017) Dose-related effects of delta-9-THC on emotional responses to acute psychosocial stress. Drug Alcohol Depend 177:136.144–136.144.  https://doi.org/10.1016/j.drugalcdep.2017.03.030 CrossRefPubMedPubMedCentralGoogle Scholar
  8. Cohen S, Williamson G (1988) Perceived stress in a probability sample of the United States. In: Spacapan S, Oskamp S (eds) The social psychology of health: Claremont symposium on applied social psychology. Newbury Park, CaliforniaGoogle Scholar
  9. Crovtiz HF, Daniel WF (1984) Measurements of everyday memory – toward the prevention of forgetting. Bull Psychon Soc 22:413–414.  https://doi.org/10.3758/BF03333861 CrossRefGoogle Scholar
  10. Cuttler C, Spradlin A (2017) Measuring cannabis consumption: psychometric properties of the daily sessions, frequency, age of onset, and quantity of cannabis use inventory (DFAQ-CU). PLoS One 12:e0178194.  https://doi.org/10.1371/journal.pone.0178194 CrossRefPubMedPubMedCentralGoogle Scholar
  11. Cuttler C, McLaughlin RJ, Graf P (2012) Mechanisms underlying the link between cannabis use and prospective memory. PLoS One 7:e36820.  https://doi.org/10.1371/journal.pone.0036820 CrossRefPubMedPubMedCentralGoogle Scholar
  12. Cuttler C, Spradlin A, Nusbaum AT, Whitney P, Hinson JM, McLaughlin RJ (2017) Blunted stress reactivity in chronic cannabis users. Psychopharmacology 234:2299–2309.  https://doi.org/10.1007/s00213-017-4648-z CrossRefPubMedGoogle Scholar
  13. Cuttler C, Spradlin A, McLaughlin RJ (2018) A naturalistic examination of the perceived effects of cannabis on negative affect. J Affect Disord 235:198–205.  https://doi.org/10.1016/j.jad.2018.04.054 CrossRefPubMedGoogle Scholar
  14. Einstein GO, McDaniel MA (1990) Normal aging and prospective memory. J Exp Psychol Learn Mem Cogn 16:717–726.  https://doi.org/10.1037/0278-7393.16.4.717 CrossRefPubMedGoogle Scholar
  15. Einstein GO, McDaniel MA (1996) Retrieval processes in prospective memory: theoretical approaches and some new empirical findings. In: Brandimonte M, Einstein GO, McDaniel MA (eds) Prospective memory: theory and applications. Lawrence Erlbaum Associates, HillsdaleGoogle Scholar
  16. Elo AL, Leppänen A, Jahkola A (2003) Validity of a single-item measure of stress symptoms. Scand J Work Environ Health 29:444–451.  https://doi.org/10.5271/sjweh.752 CrossRefPubMedGoogle Scholar
  17. Eskildsen A, Andersen LP, Pedersen AD, Vandborg SK, Anderson JH (2015) Work-related stress is associated with impaired neuropsychological test performance: a clinical cross-sectional study. Stress 18:198–207.  https://doi.org/10.3109/1025890.2015.1004629 CrossRefPubMedGoogle Scholar
  18. Gallagher DT, Hadjiefthyvoulou F, Fisk J, Montgomery C, Robinson SJ, Judge J (2013) Prospective memory deficits in illicit polydrug users are associated with the average long-term typical dose of ecstasy typically consumed in a single session. Neuropsychology 28:43–54.  https://doi.org/10.1037/neu0000004 CrossRefPubMedGoogle Scholar
  19. Glienke K, Piefke M (2016) Acute social stress before the planning phase improves memory performance in a complex real life-related prospective memory task. Neurobiol Learn Mem 133:181.  https://doi.org/10.1016/j.nlm.2016.06.025 CrossRefGoogle Scholar
  20. Graf P, Uttl B (2001) Prospective memory: a new focus for research. Conscious Cogn 10:437–450.  https://doi.org/10.1006/ccog.2001.0504 CrossRefPubMedGoogle Scholar
  21. Grant I, Gonzalez R, Carey CL, Natarajan L, Wolfson T (2003) Non-acute (residual) neurocognitive effects of cannabis use. A meta-analytic study. J Int Neuropsychol Soc 9:679–689.  https://doi.org/10.1017/S1355617703950016 CrossRefPubMedGoogle Scholar
  22. Hadjiefthyvoulou F, Fisk JE, Montgomery C, Bridges N (2011) Prospective memory functioning among ecstasy/polydrug users: evidence from the Cambridge Prospective Memory Test (CAMPROMPT). Psychopharmacology 215:761–774.  https://doi.org/10.1007/s00213-011-2174-y CrossRefPubMedGoogle Scholar
  23. Hirvonen J, Goodwin RS, Li CT, Terry GE, Zoghbi SS, Morse C, Pike VW, Volkow ND, Huestis MA, Innis RB (2012) Reversible and regionally selective downregulation of brain cannabinoid CB1 receptors in chronic daily cannabis users. Mol Psychiatry 17:642–649.  https://doi.org/10.1038/mp.2011.82 CrossRefPubMedGoogle Scholar
  24. Hyman SM, Sinha R (2009) Stress-related factors in cannabis use and misuse: implications for prevention and treatment. J Subst Abus Treat 36:400–413.  https://doi.org/10.1016/j.jsat.2008.08.005 CrossRefGoogle Scholar
  25. Ihle A, Schnitzspahn K, Rendell PG, Luong C, Kliegel M (2012) Age benefits in everyday prospective memory: the influence of personal task importance, use of reminders and everyday stress. Aging Neuropsychol Cogn 19:84–101.  https://doi.org/10.1080/13825585.2011.629288 CrossRefGoogle Scholar
  26. Joëls M (2006) Corticosteroid effects in the brain: U-shape it. Trends Pharmacol Sci 27:244–250.  https://doi.org/10.1016/j.tips.2006.03.007 CrossRefPubMedGoogle Scholar
  27. Kirschbaum C, Prike KM, Hellhammer DH (1993) The ‘Trier social stress test’: a tool for investigating psychobiological stress responses in a laboratory setting. Neuropsychobiology 28:76–81.  https://doi.org/10.1159/000119004 CrossRefPubMedGoogle Scholar
  28. Kliegel M, Martin M (2003) Prospective memory research: why is it relevant? Int J Psychol 38:193–194.  https://doi.org/10.1080/00207590344000114 CrossRefGoogle Scholar
  29. Kliegel M, Martin M, McDaniel MA, Einstein GO (2001) Varying the importance of a prospective memory task: differential effects across time- and event-based prospective memory. Memory 9:1–11.  https://doi.org/10.1080/09658210042000003 CrossRefPubMedGoogle Scholar
  30. Kliegel M, McDaniel MA, Einstein GO (2008) Prospective memory: cognitive, neuroscience, developmental, and applied perspectives. Taylor and Francis Group LLC, New YorkGoogle Scholar
  31. Kvavilashvili L, Ellis J (1996) Varieties of intention: Some distinctions and classifications. In: Brandimonte M, Einstein GO, McDaniel M (eds) Prospective memory: Theory and applications. Lawrence Erlbaum, MahwayGoogle Scholar
  32. Marchant NL, Trawley S, Rusted JM (2008) Prospective memory or prospective attention: physiological and pharmacological support for an attention model. Int J Neuropsychopharmacol 11:401–411.  https://doi.org/10.1017/S146114570700819X CrossRefPubMedGoogle Scholar
  33. McDaniel MA, Einstein GO (2007) Prospective memory: an overview and synthesis of an emerging field. Sage Publications Inc., Thousand OaksGoogle Scholar
  34. McHale S, Hunt N (2008) Executive function deficits in short-term abstinent cannabis users. Hum Psychopharmacology Clin 23:409–415.  https://doi.org/10.1002/hup.941 CrossRefGoogle Scholar
  35. Montgomery C, Seddon AL, Fisk JE, Murphy PN, Jansari A (2012) Cannabis-related deficits in real-world memory. Hum Psychopharmacology Clin 27:217–225.  https://doi.org/10.1002/hup.1273 CrossRefGoogle Scholar
  36. Moreira FA, Wotjak CT (2010) Cannabinoids and anxiety. In: Stein M, Steckler T (eds) Behavioral neurobiology of anxiety and its treatment, vol 2. Springer, BerlinGoogle Scholar
  37. Möschl M, Walser M, Plessow F, Goschke T, Fischer R (2017) Acute stress shifts the balance between controlled and automatic processes in prospective memory. Neurobiol Learn Mem 144:53–67.  https://doi.org/10.1016/j.nlm.2017.06.0002 CrossRefPubMedGoogle Scholar
  38. Nakayama Y, Takahashi T, Radford MH (2005) Cortisol levels and prospective and retrospective memory in humans. Neuro Endocrinol Lett 26:599–602PubMedGoogle Scholar
  39. Nater UM, Okere U, Stallkamp R, Moor C, Ehlert U, Kliegel M (2006) Psychosocial stress enhances time-based prospective memory in healthy young men. Neurobiol Learn Mem 86:344–348.  https://doi.org/10.1016/j.nlm.2006.04.006 CrossRefPubMedGoogle Scholar
  40. National Academies of Sciences, Engineering, and Medicine (2017) The health effects of cannabis and cannabinoids: the current state of evidence and recommendations for research. The National Academies Press, Washington, DC.  https://doi.org/10.17226/24625 CrossRefGoogle Scholar
  41. Phan KL, Angstadt M, Golden J, Onyewuenyi I, Popovska A, de Wit H (2008) Cannabinoid modulation of amygdala reactivity to social signals of threat in humans. J Neurosci 28:2313–2319.  https://doi.org/10.1523/JNEUROSCI.5603-07.2008 CrossRefPubMedPubMedCentralGoogle Scholar
  42. Piefke M, Glienke K (2017) The effects of stress on prospective memory: a systematic review. Psychol Neurosci 10:345–362.  https://doi.org/10.1037/pne0000102 CrossRefGoogle Scholar
  43. Riebe CJ, Wotjak CT (2011) Endocannabinoids and stress. Stress 14(4):384–397.  https://doi.org/10.3109/10253890.2011.586753 CrossRefPubMedGoogle Scholar
  44. Rubino T, Guidali C, Vigano N, Realini M, Massi P, Parolaro D (2008) CB1 receptor stimulation in specific brain areas differently modulate anxiety-related behavior. Neuropharmacology 54:151–160.  https://doi.org/10.1016/j.neuropharm.2007.06.024 CrossRefPubMedGoogle Scholar
  45. Schmitter-Edgecombe M, Woo E, Greeley DR (2009) Characterizing multiple memory deficits and their relation to everyday functioning in individuals with mild cognitive impairment. Neuropsychology 23:168–177.  https://doi.org/10.1037/a0014186 CrossRefPubMedGoogle Scholar
  46. Schoeler T, Kambeitz J, Behlke I, Murray R, Bhattacharyya S (2016) The effects of cannabis on memory function in users with and without a psychotic disorder: findings from a combined meta-analysis. Psychol Med 46:177–188.  https://doi.org/10.1017/S0033291715001646 CrossRefPubMedGoogle Scholar
  47. Schreiner AM, Dunn ME (2012) Residual effects of cannabis use on neurocognitive performance after prolonged abstinence. A meta-analysis. Exp Clin Psychopharmacol 20:420–429.  https://doi.org/10.1037/a0029117 CrossRefPubMedGoogle Scholar
  48. Schwabe L, Haddad L, Schachinger H (2008) HPA axis activation by a socially evaluated cold pressor test. Psychoneuroendocrinology 33:890–895.  https://doi.org/10.1016/j.psyneuen.2008.03.001 CrossRefPubMedGoogle Scholar
  49. Schwabe L, Joëls M, Roozendaal B, Wolf OT, Oitzi MS (2012) Stress effects on memory: an update and integration. Neurosci Biobehav Rev 36:1740–1749.  https://doi.org/10.1016/j.neubiorev.2011.07.002 CrossRefPubMedPubMedCentralGoogle Scholar
  50. Sellen AJ, Louie G, Harris GE, Wilkins AJ (1997) What brings attention to mind? An in situ study of prospective memory. Memory 5:483–507.  https://doi.org/10.1080/741941433 CrossRefPubMedGoogle Scholar
  51. Shields GS, Sazma MA, McCullough AM, Yonelinas AP (2017) The effects of acute stress on episodic memory: a meta-analysis and integrative review. Psychol Bull 143:636–675.  https://doi.org/10.1037/bul0000100 CrossRefPubMedPubMedCentralGoogle Scholar
  52. Smeets T, Cornelisse S, Quaedflieg CW, Meyer T, Jelicic M, Merckelbach H (2012) Introducing the Maastricht acute stress test (MAST): a quick and non-invasive approach to elicit robust autonomic and glucocorticoid stress responses. Psychoneuroendocrinology 37:1998–2008.  https://doi.org/10.1016/j.psyneuen.2012.04.012 CrossRefPubMedGoogle Scholar
  53. Solowij N, Pesa N (2010) Cognitive abnormalities and cannabis use. Rev Bras Psiquiatr 32(Supp 1):S31–S40PubMedGoogle Scholar
  54. Stock L-M, Merz CJ (2018) Memory retrieval of everyday information under stress. Neurobiol Learn Mem 152:32–38.  https://doi.org/10.1016/j.nlm.2018.05.008 CrossRefPubMedGoogle Scholar
  55. Szőllősi Á, Pajkossy P, Demeter G, Kéri S, Racsmány M (2018) Acute stress affects prospective memory functions via associative memory processes. Acta Psychol 182:82–90.  https://doi.org/10.1016/j.actpsy.2017.012 CrossRefGoogle Scholar
  56. Uttl B (2008) Transparent meta-analysis of prospective memory and aging. PLoS One 3:e1568.  https://doi.org/10.1371/journal.pone.0001568 CrossRefPubMedPubMedCentralGoogle Scholar
  57. Vogel S, Schwabe L (2016) Learning and memory under stress: implications for the classroom. Sci Learn 16011.  https://doi.org/10.1038/npjsilearn.2016.11
  58. Walser M, Fischer R, Goschke T, Kirschbaum C, Plessow F (2013) Intention retrieval and deactivation following an acute psychosocial stressor. PLoS One 8:e85685CrossRefGoogle Scholar
  59. Wilson B, Cockburn J, Baddeley A (1985) The Rivermead behavioral memory test manual. Thames Valley Test Company, Bury St. EdmundsGoogle Scholar
  60. Wolf O (2017) Stress and memory retrieval: mechanisms and consequences. Curr Opin Behav Sci 14:40–46.  https://doi.org/10.1016/j.coheha.2016.12.001 CrossRefGoogle Scholar
  61. Woods SP, Weinborn M, Velnoweth A, Rooney A, Bucks RS (2012) Memory for intentions is uniquely associated with instrumental activities of daily living in healthy older adults. J Int Neuropsychol Soc 18:134–138.  https://doi.org/10.1017/S1355617711001263 CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of PsychologyWashington State UniversityPullmanUSA
  2. 2.Translational Addiction Research CenterWashington State UniversityPullmanUSA
  3. 3.Department of Integrative Physiology and NeuroscienceWashington State UniversityPullmanUSA

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