The effect of acutely administered MDMA on subjective and BOLD-fMRI responses to favourite and worst autobiographical memories

International Journal of Neuropsychopharmacology

Volumn 17, Issue 4, 2014, Pages 527-540

  Carhart Harris, R L ^a   Wall, M B ^b   Erritzoe, D ^a   Kaelen, M ^a   Ferguson, B ^c   De Meer, I ^d   Tanner, M ^d   Bloomfield, M ^a   Williams, T M ^a   Bolstridge, M ^a   Stewart, L ^c   Morgan, C J ^c   Newbould, R D ^d   Feilding, A ^e   Curran, H V ^c   Nutt, D J ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c UNIVERSITY COLLEGE LONDON   (United Kingdom)

^d Imanova Ltd   (United Kingdom)

^e THE BECKLEY FOUNDATION   (United Kingdom)

Author keywords

5 HT; 5 HT2A; Autobiographical memory; emotion; episodic memory; fMRI; MDMA; psychotherapy; serotonin

Indexed keywords

3,4 METHYLENEDIOXYMETHAMPHETAMINE; ASCORBIC ACID; PLACEBO; SEROTONIN RECEPTOR AFFECTING AGENT;

ADULT; ARTICLE; ASSOCIATION; AUTOBIOGRAPHICAL MEMORY; BILATERAL FUSIFORM GYRUS; BOLD SIGNAL; BRAIN REGION; CONTROLLED STUDY; DOUBLE BLIND PROCEDURE; DRUG EFFECT; EXECUTIVE FUNCTION; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; FUSIFORM GYRUS; HIPPOCAMPUS; HUMAN; HUMAN EXPERIMENT; LEFT ANTERIOR TEMPORAL CORTEX; MALE; NORMAL HUMAN; PRIORITY JOURNAL; PSYCHOPHARMACOLOGY; RANDOMIZED CONTROLLED TRIAL; RECALL; SOMATOSENSORY CORTEX; TEMPORAL CORTEX; BRAIN CORTEX; DEVICES; DRUG EFFECTS; EMOTION; EPISODIC MEMORY; FUNCTIONAL NEUROIMAGING; NUCLEAR MAGNETIC RESONANCE IMAGING; PROCEDURES;

ADULT; CEREBRAL CORTEX; DOUBLE-BLIND METHOD; EMOTIONS; FEMALE; FUNCTIONAL NEUROIMAGING; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; MEMORY, EPISODIC; MENTAL RECALL; N-METHYL-3,4-METHYLENEDIOXYAMPHETAMINE; PLACEBOS; SEROTONIN AGENTS;

EID: 84896393968     PISSN: 14611457     EISSN: 14695111     Source Type: Journal    
DOI: 10.1017/S1461145713001405     Document Type: Article

References (65)

1. Anderson IM, Juhasz G, Thomas E, Downey D, McKie S, Deakin JF, Elliott R (2011) The effect of acute citalopram on face emotion processing in remitted depression: a pharmacoMRI study. Eur Neuropsychopharmacol 21:140-148.
2. Anderson MC, Ochsner KN, Kuhl B, Cooper J, Robertson E, Gabrieli SW, Glover GH, Gabrieli JD (2004) Neural systems underlying the suppression of unwanted memories. Science 303:232-235.
3. Bach DR, Behrens TE, Garrido L, Weiskopf N, Dolan RJ (2011) Deep and superficial amygdala nuclei projections revealed in vivo by probabilistic tractography. J Neurosci 31:618-623.
4. Bedi G, Phan KL, Angstadt M, de Wit H (2009) Effects of MDMA on sociability and neural response to social threat and social reward. Psychopharmacology 207:73-83.
5. Bedi G, Hyman D, de Wit H (2010) Is ecstasy an "empathogen"? Effects of±3, 4-methylenedioxymethamphetamine on prosocial feelings and identification of emotional states in others. Biol Psychiatry 68:1134-1140.
6. Beringer K, Tunstall B, Broadbear JH (2009) Oxytocin as a mediator of the unique interoceptive effects of 3, 4-Methylenedioxymethamphetamine (MDMA, "Ecstasy") in the rat. Neuropsychobiology 60:217-217.
7. Bickart KC, Hollenbeck MC, Barrett LF, Dickerson BC (2012) Intrinsic amygdala-cortical functional connectivity predicts social network size in humans. J Neurosci 32:14729-14741.
8. Brewin CR (2006) Understanding cognitive behaviour therapy: a retrieval competition account. Behav Res Ther 44:765-784.
9. Broadbear JH, Tunstall B, Beringer K (2011) Examining the role of oxytocin in the interoceptive effects of 3, 4-methylenedioxymethamphetamine (MDMA, 'ecstasy') using a drug discrimination paradigm in the rat. Addict Biol 16:202-214.
10. Button KS, Ioannidis JP, Mokrysz C, Nosek BA, Flint J, Robinson ES, Munafo MR (2013) Power failure: why small sample size undermines the reliability of neuroscience. Nat Rev Neurosci 14:365-376.
11. Cahir M, Ardis T, Reynolds GP, Cooper SJ (2007) Acute and chronic tryptophan depletion differentially regulate central 5-HT1A and 5-HT 2A receptor binding in the rat. Psychopharmacology 190:497-506.
12. Carhart-Harris RL, Leech R, Williams TM, Erritzoe D, Abbasi N, Bargiotas T, Hobden P, Sharp DJ, Evans J, Feilding A, Wise RG, Nutt DJ (2012) Implications for psychedelic-assisted psychotherapy: functional magnetic resonance imaging study with psilocybin. Br J Psychiatry 200:238-244.
13. Cowen PJ (2008) Serotonin and depression: pathophysiological mechanism or marketing myth? Trends Pharmacol Sci 29:433-436.
14. Daselaar SM, Rice HJ, Greenberg DL, Cabeza R, LaBar KS, Rubin DC (2008) The spatiotemporal dynamics of autobiographical memory: neural correlates of recall, emotional intensity, and reliving. Cereb Cortex 18:217-229.
15. de la Torre R, Farre M, Roset PN, Pizarro N, Abanades S, Segura M, Segura J, Cami J (2004) Human pharmacology of MDMA: pharmacokinetics, metabolism, and disposition. Ther Drug Monit 26:137-144.
16. Diukova A, Ware J, Smith JE, Evans CJ, Murphy K, Rogers PJ, Wise RG (2012) Separating neural and vascular effects of caffeine using simultaneous EEG-FMRI: differential effects of caffeine on cognitive and sensorimotor brain responses. NeuroImage 62:239-249.
17. Duman RS, Aghajanian GK (2012) Synaptic dysfunction in depression: potential therapeutic targets. Science 338:68-72.
18. Erritzoe D, Frokjaer VG, Holst KK, Christoffersen M, Johansen SS, Svarer C, Madsen J, Rasmussen PM, Ramsoy T, Jernigan TL, Knudsen GM (2011) In vivo imaging of cerebral serotonin transporter and serotonin(2A) receptor binding in 3, 4-methylenedioxymethamphetamine (MDMA or "ecstasy") and hallucinogen users. Arch Gen Psychiatry 68:562-576.
19. Friston KJ, Buechel C, Fink GR, Morris J, Rolls E, Dolan RJ (1997) Psychophysiological and modulatory interactions in neuroimaging. NeuroImage 6:218-229.
20. Friston KJ, Harrison L, Penny W (2003) Dynamic causal modelling. NeuroImage 19:1273-1302.
21. Frokjaer VG, Mortensen EL, Nielsen FA, Haugbol S, Pinborg LH, Adams KH, Svarer C, Hasselbalch SG, Holm S, Paulson OB, Knudsen GM (2008) Frontolimbic serotonin 2A receptor binding in healthy subjects is associated with personality risk factors for affective disorder. Biol Psychiatry 63:569-576.
22. Gallagher M, Chiba AA (1996) The amygdala and emotion. Curr Opin Neurobiol 6:221-227.
23. Godlewska BR, Norbury R, Selvaraj S, Cowen PJ, Harmer CJ (2012) Short-term SSRI treatment normalises amygdala hyperactivity in depressed patients. Psychol Med 42:2609-2617.
24. Greer GR, Tolbert R (1998) A method of conducting therapeutic sessions with MDMA. J Psychoactive Drugs 30:371-379.
25. Griffiths R, Richards W, Johnson M, McCann U, Jesse R (2008) Mystical-type experiences occasioned by psilocybin mediate the attribution of personal meaning and spiritual significance 14 months later. J Psychopharmacol 22:621-632.
26. Griffiths RR, Richards WA, McCann U, Jesse R (2006) Psilocybin can occasion mystical-type experiences having substantial and sustained personal meaning and spiritual significance. Psychopharmacology 187:268-283; discussion 284-292.
27. Grob CS, Danforth AL, Chopra GS, Hagerty M, McKay CR, Halberstadt AL, Greer GR (2011) Pilot study of psilocybin treatment for anxiety in patients with advanced-stage cancer. Arch Gen Psychiatry 68:71-78.
28. Harmer CJ (2008) Serotonin and emotional processing: does it help explain antidepressant drug action? Neuropharmacology 55:1023-1028.
29. Harmer CJ, Mackay CE, Reid CB, Cowen PJ, Goodwin GM (2006) Antidepressant drug treatment modifies the neural processing of nonconscious threat cues. Biol Psychiatry 59:816-820.
30. Hofmann SG, Pollack MH, Otto MW (2006) Augmentation treatment of psychotherapy for anxiety disorders with D-cycloserine. CNS Drug Rev 12:208-217.
31. Hysek CM, Domes G, Liechti ME (2012) MDMA enhances "mind reading" of positive emotions and impairs "mind reading" of negative emotions. Psychopharmacology 222:293-302.
32. Iannetti GD, Wise RG (2007) BOLD functional MRI in disease and pharmacological studies: room for improvement? Magn Reson Imaging 25:978-988.
33. Kolbrich EA, Goodwin RS, Gorelick DA, Hayes RJ, Stein EA, Huestis MA (2008) Plasma pharmacokinetics of 3, 4-methylenedioxymethamphetamine after controlled oral administration to young adults. Ther Drug Monit 30:320-332.
34. Kometer M, Schmidt A, Bachmann R, Studerus E, Seifritz E, Vollenweider FX (2012) Psilocybin biases facial recognition, goal-directed behavior, and mood state toward positive relative to negative emotions through different serotonergic subreceptors. Biol Psychiatry 72:898-906.
35. Kuypers KP, Wingen M, Heinecke A, Formisano E, Ramaekers JG (2011) MDMA intoxication and verbal memory performance: a placebo-controlled pharmaco-MRI study. J Psychopharmacol 25:1053-1061.
36. Lanius RA, Bluhm RL, Frewen PA (2011) How understanding the neurobiology of complex post-traumatic stress disorder can inform clinical practice: a social cognitive and affective neuroscience approach. Acta Psychiatr Scand 124:331-348.
37. Lanius RA, Brand B, Vermetten E, Frewen PA, Spiegel D (2012) The dissociative subtype of posttraumatic stress disorder: rationale, clinical and neurobiological evidence, and implications. Depress Anxiety 29:701-708.
38. Lenzi D, Trentini C, Pantano P, Macaluso E, Lenzi GL, Ammaniti M (2013) Attachment models affect brain responses in areas related to emotions and empathy in nulliparous women. Hum Brain Mapp 34:1399-1414.
39. Liechti ME, Vollenweider FX (2001) Which neuroreceptors mediate the subjective effects of MDMA in humans? A summary of mechanistic studies. Hum Psychopharmacol 16:589-598.
40. Liechti ME, Saur MR, Gamma A, Hell D, Vollenweider FX (2000) Psychological and physiological effects of MDMA ("Ecstasy") after pretreatment with the 5-HT(2) antagonist ketanserin in healthy humans. Neuropsychopharmacol: ACNP 23:396-404.
41. MacLean KA, Johnson MW, Griffiths RR (2011) Mystical experiences occasioned by the hallucinogen psilocybin lead to increases in the personality domain of openness. J Psychopharmacol 25:1453-1461.
42. Macleod C (2012) Cognitive bias modification procedures in the management of mental disorders. Curr Opin Psychiatry 25:114-120.
43. Meyer JH, McMain S, Kennedy SH, Korman L, Brown GM, DaSilva JN, Wilson AA, Blak T, Eynan-Harvey R, Goulding VS, Houle S, Links P (2003a) Dysfunctional attitudes and 5-HT2 receptors during depression and self-harm. Am J Psychiatry 160:90-99.
44. Meyer JH, McMain S, Kennedy SH, Korman L, Brown GM, DaSilva JN, Wilson AA, Blak T, Eynan-Harvey R, Goulding VS, Houle S, Links P (2003b) Dysfunctional attitudes and 5-HT2 receptors during depression and self-harm. Am J Psychiatry 160:90-99.
45. Meyer ML, Masten CL, Ma Y, Wang C, Shi Z, Eisenberger NI, Han S (2013) Empathy for the social suffering of friends and strangers recruits distinct patterns of brain activation. Social Cog and Affect Neuroscience 8:446-454.
46. Mithoefer MC, Wagner MT, Mithoefer AT, Jerome L, Doblin R (2011) The safety and efficacy of {±}3, 4-methyl-enedioxymethamphetamine-assisted psychotherapy in subjects with chronic, treatment-resistant posttraumatic stress disorder: the first randomized controlled pilot study. J Psychopharmacol 25:439-452.
47. Mithoefer MC, Wagner MT, Mithoefer AT, Jerome L, Martin SF, Yazar-Klosinski B, Michel Y, Brewerton TD, Doblin R (2013) Durability of improvement in post-traumatic stress disorder symptoms and absence of harmful effects or drug dependency after 3, 4-methylenedioxymethamphetamine-assisted psychotherapy: a prospective long-term follow-up study. J Psychopharmacol 27:28-39.
48. Murphy SE, Norbury R, O'Sullivan U, Cowen PJ, Harmer CJ (2009) Effect of a single dose of citalopram on amygdala response to emotional faces. Br J Psychiatry 194:535-540.
49. Musser ED, Kaiser-Laurent H, Ablow JC (2012) The neural correlates of maternal sensitivity: an fMRI study. Develop Cogn Neuroscience 2:428-436.
50. Nichols DE, Brewster WK, Johnson MP, Oberlender R, Riggs RM (1990) Nonneurotoxic tetralin and indan analogues of 3, 4-(methylenedioxy)amphetamine (MDA). J Med Chem 33:703-710.
51. Nutt DJ, King LA, Nichols DE (2013) Effects of Schedule I drug laws on neuroscience research and treatment innovation. Nat Rev Neurosci 14:577-585.
52. Piefke M, Weiss PH, Zilles K, Markowitsch HJ, Fink GR (2003) Differential remoteness and emotional tone modulate the neural correlates of autobiographical memory. Brain 126:650-668.
53. Protopopescu X, Pan H, Tuescher O, Cloitre M, Goldstein M, Engelien W, Epstein J, Yang YH, Gorman J, LeDoux J, Silbersweig D, Stern E (2005) Differential time courses and specificity of amygdala activity in posttraumatic stress disorder subjects and normal control subjects. Biol Psychiatry 57:464-473.
54. Ramaekers JG, Kuypers KP, Wingen M, Heinecke A, Formisano E (2009) Involvement of inferior parietal lobules in prospective memory impairment during acute MDMA (ecstasy) intoxication: an event-related fMRI study. Neuropsychopharmacol: ACNP 34:1641-1648.
55. Rauch SA, Eftekhari A, Ruzek JI (2012) Review of exposure therapy: a gold standard for PTSD treatment. J Rehabil Res Dev 49:679-687.
56. Ressler KJ, Rothbaum BO, Tannenbaum L, Anderson P, Graap K, Zimand E, Hodges L, Davis M (2004) Cognitive enhancers as adjuncts to psychotherapy: use of D-cycloserine in phobic individuals to facilitate extinction of fear. Arch Gen Psychiatry 61:1136-1144.
57. Rothman RB, Baumann MH, Dersch CM, Romero DV, Rice KC, Carroll FI, Partilla JS (2001) Amphetamine-type central nervous system stimulants release norepinephrine more potently than they release dopamine and serotonin. Synapse 39:32-41.
58. Sessa B (2009) Let's not give in to Descartes: we need pharmacology and psychotherapy. J Psychopharmacol 23:227-228.
59. Sharot T, Korn CW, Dolan RJ (2011) How unrealistic optimism is maintained in the face of reality. Nat Neurosci 14:1475-1479.
60. St Jacques PL, Botzung A, Miles A, Rubin DC (2011) Functional neuroimaging of emotionally intense autobiographical memories in post-traumatic stress disorder. J Psychiatry Res 45:630-637.
61. Svoboda E, McKinnon MC, Levine B (2006) The functional neu-roanatomy of autobiographical memory: a meta-analysis. Neuropsychologia 44:2189-2208.
62. Tranter R, Bell D, Gutting P, Harmer C, Healy D, Anderson IM (2009) The effect of serotonergic and noradrenergic antidepressants on face emotion processing in depressed patients. J Affect Disord 118:87-93.
63. Urban NB, Girgis RR, Talbot PS, Kegeles LS, Xu X, Frankle WG, Hart CL, Slifstein M, Abi-Dargham A, Laruelle M (2012) Sustained recreational use of ecstasy is associated with altered pre and postsynaptic markers of serotonin transmission in neocortical areas: a PET study with [(1)(1)C]DASB and [(1)(1) C]MDL 100907. Neuropsychopharmacol: ACNP 37:1465-1473.
64. van Wel JH, Kuypers KP, Theunissen EL, Bosker WM, Bakker K, Ramaekers JG (2012) Effects of acute MDMA intoxication on mood and impulsivity: role of the 5-HT2 and 5-HT1 receptors. PloS ONE 7:e40187.
65. Weiner KS, Grill-Spector K (2012) The improbable simplicity of the fusiform face area. Trends Cog Sciences 16:251-254.