Psilocybin-induced spiritual experiences and insightfulness are associated with synchronization of neuronal oscillations

Psychopharmacology

Volumn 232, Issue 19, 2015, Pages 3663-3676

  Kometer, Michael ^a   Pokorny, Thomas ^a   Seifritz, Erich ^a   Volleinweider, Franz X ^a  

^a University Hospital of Psychiatry Zurich   (Switzerland)

Author keywords

ACC; Consciousness; Delta; EEG; Oscillations; PCC; Psilocybin; Resting State; Serotonin; Spirituality

Indexed keywords

BUSPIRONE; ERGOTAMINE; KETANSERIN; PLACEBO; PSILOCYBINE; PSYCHEDELIC AGENT; SEROTONIN AGONIST;

ADULT; ANTERIOR CINGULATE; ARTICLE; CONSCIOUSNESS; CONTROLLED STUDY; DOUBLE BLIND PROCEDURE; DRUG DOSE COMPARISON; ELECTROENCEPHALOGRAM; EYES CLOSED RESTING STATE; EYES OPEN RESTING STATE; FEMALE; HUMAN; INTROSPECTION; LATERAL ORBITOFRONTAL CORTEX; MALE; MENTAL HEALTH; NERVE CELL NETWORK; NEURONAL OSCILLATION; NORMAL HUMAN; OSCILLATION; PARAHIPPOCAMPAL GYRUS; POSTERIOR CINGULATE; PRIORITY JOURNAL; RANDOMIZED CONTROLLED TRIAL; RETROSPLENIAL CORTEX; SPIRITUALISM; STEADY STATE; WELLBEING; BRAIN CORTEX; DRUG EFFECTS; ELECTROENCEPHALOGRAPHY; PHYSIOLOGY; PROCEDURES; YOUNG ADULT;

ADULT; CEREBRAL CORTEX; DOUBLE-BLIND METHOD; ELECTROENCEPHALOGRAPHY; FEMALE; HALLUCINOGENS; HUMANS; MALE; NERVE NET; PARAHIPPOCAMPAL GYRUS; PSILOCYBINE; SEROTONIN RECEPTOR AGONISTS; YOUNG ADULT;

EID: 84941260790     PISSN: 00333158     EISSN: 14322072     Source Type: Journal    
DOI: 10.1007/s00213-015-4026-7     Document Type: Article

References (97)

1. Alkire MT, Hudetz AG, Tononi G (2008) Consciousness and anesthesia. Science 322:876-880
2. Babiloni C, Lizio R, Carducci F, Vecchio F, Redolfi A, Marino S, Tedeschi G, Montella P, Guizzaro A, Esposito F (2011) Resting state cortical electroencephalographic rhythms and white matter vascular lesions in subjects with Alzheimer's disease: an Italian multicenter study. J Alzheimers Dis 26:331-346
3. Babiloni C, Carducci F, Lizio R, Vecchio F, Baglieri A, Bernardini S, Cavedo E, Bozzao A, Buttinelli C, Esposito F (2013) Resting state cortical electroencephalographic rhythms are related to gray matter volume in subjects with mild cognitive impairment and Alzheimer's disease. Hum Brain Mapp 34:1427-1446
4. Bar M, Aminoff E (2003) Cortical analysis of visual context. Neuron 38:347-358
5. Bell AJ, Sejnowski TJ (1995) An information-maximization approach to blind separation and blind deconvolution. Neural Comput 7:1129-1159
6. Boly M, Phillips C, Tshibanda L, Vanhaudenhuyse A, Schabus M, Dang-Vu TT, Moonen G, Hustinx R, Maquet P, Laureys S (2008) Intrinsic brain activity in altered states of consciousness: how conscious is the default mode of brain function? Ann N Y Acad Sci 1129:119-129
7. Brewer JA, Worhunsky PD, Gray JR, Tang Y-Y, Weber J, Kober H (2011) Meditation experience is associated with differences in default mode network activity and connectivity. Proc Natl Acad Sci 108:20254-20259
8. Busch NA, Dubois J, VanRullen R (2009) The phase of ongoing EEG oscillations predicts visual perception. J Neurosci 29:7869-7876
9. Buschman TJ, Denovellis EL, Diogo C, Bullock D, Miller EK (2012) Synchronous oscillatory neural ensembles for rules in the prefrontal cortex. Neuron 76:838-846
10. Buzsáki G, Draguhn A (2004) Neuronal oscillations in cortical networks. Science 304:1926-1929
11. Buzsáki G, Anastassiou CA, Koch C (2012) The origin of extracellular fields and currents - EEG, ECoG, LFP and spikes. Nat Rev Neurosci 13:407-420
12. Canuet L, Ishii R, Pascual-Marqui RD, Iwase M, Kurimoto R, Aoki Y, Ikeda S, Takahashi H, Nakahachi T, Takeda M (2011) Resting-state EEG source localization and functional connectivity in schizophrenia-like psychosis of epilepsy. PLoS ONE 6:e27863
13. Canuet L, Tellado I, Couceiro V, Fraile C, Fernandez-Novoa L, Ishii R, Takeda M, Cacabelos R (2012) Resting-state network disruption and APOE genotype in Alzheimer's disease: a lagged functional connectivity study. PLoS ONE 7, e46289
14. Carhart-Harris RL, Erritzoe D, Williams T, Stone JM, Reed LJ, Colasanti A, Tyacke RJ, Leech R, Malizia AL, Murphy K, Hobden P, Evans J, Feilding A, Wise RG, Nutt DJ (2012) Neural correlates of the psychedelic state as determined by fMRI studies with psilocybin. Proc Natl Acad Sci U S A 109:2138-2143
15. Celada P, Puig MV, Díaz-Mataix L, Artigas F (2008) The hallucinogen DOI reduces low-frequency oscillations in rat prefrontal cortex: reversal by antipsychotic drugs. Biol Psychiatry 64:392-400
16. Ching S, Cimenser A, Purdon PL, Brown EN, Kopell NJ (2010) Thalamocortical model for a propofol-induced alpha-rhythm associated with loss of consciousness. Proc Natl Acad Sci U S A 107:22665-22670
17. Cott C, Rock A (2008) Phenomenology of N,N-dimethyltryptamine use: a thematic analysis. J Scientific Exploration 22:359-370
18. Dehaene S, Changeux JP (2011) Experimental and theoretical approaches to conscious processing. Neuron 70:200-227
19. Derogatis L (1994) SCL-90-R: Symptom Checklist-90-R. Administration, scoring and procedures manual. National Computer Systems Inc, Minneapolis
20. Dittrich A (1998) The standardized psychometric assessment of altered states of consciousness (ASCs) in humans. Pharmacopsychiatry 31:80-84
21. Elmer S, Rogenmoser L, Kühnis J, Jäncke L (2015) Bridging the gap between perceptual and cognitive perspectives on absolute pitch. J Neurosci 35:366-371
22. Fahrenfort JJ, Snijders TM, Heinen K, van Gaal S, Scholte HS, Lamme VA (2012) Neuronal integration in visual cortex elevates face category tuning to conscious face perception. Proc Natl Acad Sci U S A 109:21504-21509
23. Fell J, Axmacher N (2011) The role of phase synchronization in memory processes. Nat Rev Neurosci 12:105-118
24. Foster BL, Kaveh A, Dastjerdi M, Miller KJ, Parvizi J (2013) Human retrosplenial cortex displays transient theta phase locking with medial temporal cortex prior to activation during autobiographical memory retrieval. J Neurosci 33:10439-10446
25. Goda SA, Piasecka J, Olszewski M, Kasicki S, Hunt MJ (2013) Serotonergic hallucinogens differentially modify gamma and high frequency oscillations in the rat nucleus accumbens. Psychopharmacology (Berl) 228:271-282
26. Gouzoulis-Mayfrank E, Schreckenberger M, Sabri O, Arning C, Thelen B, Spitzer M, Kovar KA, Hermle L, Büll U, Sass H (1999) Neurometabolic effects of psilocybin, 3,4-methylenedioxyethylamphetamine (MDE) and d-methamphetamine in healthy volunteers. A double-blind, placebo-controlled PET study with [18F]FDG. Neuropsychopharmacology 20:565-581
27. 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 (Berl) 187:268-283, discussion 284-292
28. 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
29. Grob C, S., Bossis A, P., Griffiths R, R. (2013) Use of the classic hallucinogen psilocybin for treatment of existential distress associated with cancer. In: Carr BI, Steel J (eds) Psychological Aspects of Cancer. Springer, USA
30. 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 68:71-8
31. Guggisberg AG, Rizk S, Ptak R, Di Pietro M, Saj A, Lazeyras F, Lovblad K-O, Schnider A, Pignat J-M (2014) Two intrinsic coupling types for resting-state integration in the human brain. Brain Topogr 1-12
32. Gusnard DA, Akbudak E, Shulman GL, Raichle ME (2001) Medial prefrontal cortex and self-referential mental activity: relation to a default mode of brain function. Proc Natl Acad Sci U S A 98:4259-4264
33. Haegens S, Nácher V, Luna R, Romo R, Jensen O (2011) α-Oscillations in the monkey sensorimotor network influence discrimination performance by rhythmical inhibition of neuronal spiking. Proc Natl Acad Sci U S A 108:19377-19382
34. Hanslmayr S, Volberg G, Wimber M, Dalal SS, Greenlee MW (2013) Prestimulus Oscillatory Phase at 7 Hz Gates Cortical Information Flow and Visual Perception. Curr Biol 23(22):2273-8
35. Hilty L, Langer N, Pascual-Marqui R, Boutellier U, Lutz K (2011) Fatigue-induced increase in intracortical communication between mid/anterior insular and motor cortex during cycling exercise. Eur J Neurosci 34:2035-2042
36. Hipp JF, Engel AK, Siegel M (2011) Oscillatory synchronization in large-scale cortical networks predicts perception. Neuron 69:387-396
37. Horacek J, Brunovsky M, Novak T, Skrdlantova L, Klirova M, Bubenikova-Valesova V, Krajca V, Tislerova B, Kopecek M, Spaniel F (2007) Effect of low-frequency rTMS on electromagnetic tomography (LORETA) and regional brain metabolism (PET) in schizophrenia patients with auditory hallucinations. Neuropsychobiology 55:132-142
38. Jatoi MA, Kamel N, Malik AS, Faye I (2014) EEG based brain source localization comparison of sLORETA and eLORETA. Australas Phys Eng Sci Med 37:713-721
39. Klimesch W, Sauseng P, Hanslmayr S (2007) EEG alpha oscillations: the inhibition-timing hypothesis. Brain Res Rev 53:63-88
40. 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
41. Kometer M, Schmidt A, Jäncke L, Vollenweider FX (2013) Activation of serotonin 2A receptors underlies the psilocybin-induced effects on α oscillations, N170 visual-evoked potentials, and visual hallucinations. J Neurosci 33:10544-10551
42. Kühnis J, Elmer S, Jäncke L (2014) Auditory evoked responses in musicians during passive vowel listening are modulated by functional connectivity between bilateral auditory-related brain regions. J Cogn Neurosci 26:2750-2761
43. Lee TW, Girolami M, Sejnowski TJ (1999) Independent component analysis using an extended infomax algorithm for mixed subgaussian and supergaussian sources. Neural Comput 11:417-441
44. Levin JS (1993) Age differences in mystical experience. Gerontologist 33:507-513
45. Lu H, Zuo Y, Gu H, Waltz JA, Zhan W, Scholl CA, Rea W, Yang Y, Stein EA (2007) Synchronized delta oscillations correlate with the resting-state functional MRI signal. Proc Natl Acad Sci U S A 104:18265-18269
46. Maselko J, Kubzansky LD (2006) Gender differences in religious practices, spiritual experiences and health: results from the US General Social Survey. Soc Sci Med 62:2848-2860
47. McClain CS, Rosenfeld B, Breitbart W (2003) Effect of spiritual well-being on end-of-life despair in terminally-ill cancer patients. Lancet 361:1603-1607
48. Melloni L, Molina C, Pena M, Torres D, Singer W, Rodriguez E (2007) Synchronization of neural activity across cortical areas correlates with conscious perception. J Neurosci 27:2858-2865
49. Merker B (2013) Cortical gamma oscillations: the functional key is activation, not cognition. Neurosci Biobehav Rev 37:401-417
50. Miller L, Bansal R, Wickramaratne P, Hao X, Tenke CE, Weissman MM, Peterson BS (2014) Neuroanatomical correlates of religiosity and spirituality: a study in adults at high and low familial risk for depression. JAMA Psychiatry 71:128-135
51. Mulert C, Jäger L, Schmitt R, Bussfeld P, Pogarell O, Möller HJ, Juckel G, Hegerl U (2004) Integration of fMRI and simultaneous EEG: towards a comprehensive understanding of localization and time-course of brain activity in target detection. Neuroimage 22:83-94
52. Mulert C, Jäger L, Propp S, Karch S, Störmann S, Pogarell O, Möller H-J, Juckel G, Hegerl U (2005) Sound level dependence of the primary auditory cortex: simultaneous measurement with 61-channel EEG and fMRI. Neuroimage 28:49-58
53. Murphy M, Bruno MA, Riedner BA, Boveroux P, Noirhomme Q, Landsness EC, Brichant JF, Phillips C, Massimini M, Laureys S, Tononi G, Boly M (2011) Propofol anesthesia and sleep: a high-density EEG study. Sleep 34:283-291A
54. Muthukumaraswamy SD, Carhart-Harris RL, Moran RJ, Brookes MJ, Williams TM, Errtizoe D, Sessa B, Papadopoulos A, Bolstridge M, Singh KD, Feilding A, Friston KJ, Nutt DJ (2013) Broadband cortical desynchronization underlies the human psychedelic state. J Neurosci 33:15171-15183
55. Neuner I, Arrubla J, Werner CJ, Hitz K, Boers F, Kawohl W, Shah NJ (2014) The default mode network and EEG regional spectral power: a simultaneous fMRI-EEG study. PLoS ONE 9:e88214
56. Nichols DE (2004) Hallucinogens. Pharmacol Ther 101:131-181
57. Nichols TE (2012) Multiple testing corrections, nonparametric methods, and random field theory. Neuroimage 62:811-815
58. Nichols TE, Holmes AP (2002) Nonparametric permutation tests for functional neuroimaging: a primer with examples. Hum Brain Mapp 15:1-25
59. Nolte G, Bai O, Wheaton L, Mari Z, Vorbach S, Hallett M (2004) Identifying true brain interaction from EEG data using the imaginary part of coherency. Clin Neurophysiol 115:2292-2307
60. Olbrich S, Mulert C, Karch S, Trenner M, Leicht G, Pogarell O, Hegerl U (2009) EEG-vigilance and BOLD effect during simultaneous EEG/fMRI measurement. Neuroimage 45:319-332
61. Olbrich S, Tränkner A, Chittka T, Hegerl U, Schönknecht P (2014) Functional connectivity in major depression: increased phase synchronization between frontal cortical EEG-source estimates. Psychiatry Res Neuroimaging 222:91-99
62. Pascual-Marqui RD (2002) Standardized low-resolution brain electromagnetic tomography (sLORETA): technical details. Methods Find Exp Clin Pharmacol 24(Suppl D):5-12
63. Pascual-Marqui RD, Michel CM, Lehmann D (1994) Low resolution electromagnetic tomography: a new method for localizing electrical activity in the brain. Int J Psychophysiol 18:49-65
64. Pascual-Marqui RD, Lehmann D, Koukkou M, Kochi K, Anderer P, Saletu B, Tanaka H, Hirata K, John ER, Prichep L, Biscay-Lirio R, Kinoshita T (2011) Assessing interactions in the brain with exact low-resolution electromagnetic tomography. Philos Trans A Math Phys Eng Sci 369:3768-3784
65. Pascual-Marqui RD, Biscay RJ, Bosch-Bayard J, Lehmann D, Kochi K, Kinoshita T, Yamada N, Sadato N (2014) Assessing direct paths of intracortical causal information flow of oscillatory activity with the isolated effective coherence (iCoh). Front Hum Neurosci 8
66. Perrin F, Pernier J, Bertrand O, Echallier JF (1989) Spherical splines for scalp potential and current density mapping. Electroencephalogr Clin Neurophysiol 72:184-187
67. Pizzagalli DA, Oakes TR, Fox AS, Chung MK, Larson CL, Abercrombie HC, Schaefer SM, Benca RM, Davidson RJ (2004) Functional but not structural subgenual prefrontal cortex abnormalities in melancholia. Mol Psychiatry 9(325):393-405
68. Puig MV, Watakabe A, Ushimaru M, Yamamori T, Kawaguchi Y (2010) Serotonin modulates fast-spiking interneuron and synchronous activity in the rat prefrontal cortex through 5-HT1A and 5-HT2A receptors. J Neurosci 30:2211-2222
69. Ramyead A, Kometer M, Studerus E, Koranyi S, Ittig S, Gschwandtner U, Fuhr P, Riecher-Rössler A (2014) Aberrant current source-density and lagged phase synchronization of neural oscillations as markers for emerging psychosis. Schizophr Bull 41(4):919-929
70. Riba J, Anderer P, Morte A, Urbano G, Jané F, Saletu B, Barbanoj MJ (2002) Topographic pharmaco-EEG mapping of the effects of the South American psychoactive beverage ayahuasca in healthy volunteers. Br J Clin Pharmacol 53:613-628
71. Riba J, Anderer P, Jané F, Saletu B, Barbanoj MJ (2004) Effects of the South American psychoactive beverage ayahuasca on regional brain electrical activity in humans: a functional neuroimaging study using low-resolution electromagnetic tomography. Neuropsychobiology 50:89-101
72. Schoffelen JM, Gross J (2009) Source connectivity analysis with MEG and EEG. Hum Brain Mapp 30:1857-1865
73. Schroeder CE, Lakatos P (2009) Low-frequency neuronal oscillations as instruments of sensory selection. Trends Neurosci 32:9-18
74. Sheehan D, Lecrubier Y, Sheehan K, Amorim P, Janavs J, Weiller E, Hergueta T, Baker R, Dunbar G (1998) The Mini-International Neuropsychiatric Interview (MINI): the development and validation of a structured diagnostic psychiatric interview for DSM-IV and ICD-10. J Clin Psychiatry 59:22-33
75. Shushruth S (2013) Exploring the neural basis of consciousness through anesthesia. J Neurosci 33:1757-1758
76. Siegel M, Donner TH, Engel AK (2012) Spectral fingerprints of large-scale neuronal interactions. Nat Rev Neurosci 13:121-134
77. Southwick SM, Charney DS (2012) The science of resilience: implications for the prevention and treatment of depression. Science 338:79-82
78. Stam CJ, Nolte G, Daffertshofer A (2007) Phase lag index: assessment of functional connectivity from multi channel EEG and MEG with diminished bias from common sources. Hum Brain Mapp 28:1178-1193
79. Steinmann S, Leicht G, Ertl M, Andreou C, Polomac N, Westerhausen R, Friederici AD, Mulert C (2014) Conscious auditory perception related to long-range synchrony of gamma oscillations. Neuroimage 100:435-443
80. Studerus E, Gamma A, Vollenweider FX (2010) Psychometric evaluation of the altered states of consciousness rating scale (OAV). PLoS ONE 5, e12412
81. Studerus E, Kometer M, Hasler F, Vollenweider FX (2011) Acute, subacute and long-term subjective effects of psilocybin in healthy humans: a pooled analysis of experimental studies. J Psychopharmacol 25:1434-1452
82. Tenke CE, Kayser J, Miller L, Warner V, Wickramaratne P, Weissman MM, Bruder GE (2013) Neuronal generators of posterior EEG alpha reflect individual differences in prioritizing personal spirituality. Biol Psychol 94:426-432
83. Thatcher RW, North DM, Biver CJ (2012) Diffusion spectral imaging modules correlate with EEG LORETA neuroimaging modules. Hum Brain Mapp 33:1062-1075
84. Towle VL, Bolaños J, Suarez D, Tan K, Grzeszczuk R, Levin DN, Cakmur R, Frank SA, Spire JP (1993) The spatial location of EEG electrodes: locating the best-fitting sphere relative to cortical anatomy. Electroencephalogr Clin Neurophysiol 86:1-6
85. Urgesi C, Aglioti SM, Skrap M, Fabbro F (2010) The spiritual brain: selective cortical lesions modulate human self-transcendence. Neuron 65:309-319
86. Vann SD, Aggleton JP, Maguire EA (2009) What does the retrosplenial cortex do? Nat Rev Neurosci 10:792-802
87. VanRullen R, Koch C (2003) Is perception discrete or continuous? Trends Cogn Sci 7:207-213
88. Varela F, Lachaux JP, Rodriguez E, Martinerie J (2001) The brainweb: phase synchronization and large-scale integration. Nat Rev Neurosci 2:229-239
89. Vecchio F, Miraglia F, Curcio G, Altavilla R, Scrascia F, Giambattistelli F, Quattrocchi CC, Bramanti P, Vernieri F, Rossini PM (2015) Cortical brain connectivity evaluated by graph theory in dementia: a correlation study between functional and structural data. J Alzheimers Dis 45(3):745-756
90. Vitacco D, Brandeis D, Pascual-Marqui R, Martin E (2002) Correspondence of event-related potential tomography and functional magnetic resonance imaging during language processing. Hum Brain Mapp 17:4-12
91. Vollenweider FX, Kometer M (2010) The neurobiology of psychedelic drugs: implications for the treatment of mood disorders. Nat Rev Neurosci 11:642-651
92. Vollenweider FX, Leenders KL, Scharfetter C, Maguire P, Stadelmann O, Angst J (1997) Positron emission tomography and fluorodeoxyglucose studies of metabolic hyperfrontality and psychopathology in the psilocybin model of psychosis. Neuropsychopharmacology 16:357-372
93. Vollenweider FX, Vollenweider-Scherpenhuyzen MF, Bäbler A, Vogel H, Hell D (1998) Psilocybin induces schizophrenia-like psychosis in humans via a serotonin-2 agonist action. Neuroreport 9:3897-3902
94. Wallis JD (2007) Orbitofrontal cortex and its contribution to decision-making. Annu Rev Neurosci 30:31-56
95. Wittchen H-U, Pfister H (1997) DIA-X-Interviews: Manual für Screening-Verfahren und Interview. Swets & Zeitlinger, Frankfurt, Hesse
96. Womelsdorf T, Schoffelen JM, Oostenveld R, Singer W, Desimone R, Engel AK, Fries P (2007) Modulation of neuronal interactions through neuronal synchronization. Science 316:1609-1612
97. Worrell GA, Lagerlund TD, Sharbrough FW, Brinkmann BH, Busacker NE, Cicora KM, O'Brien TJ (2000) Localization of the epileptic focus by low-resolution electromagnetic tomography in patients with a lesion demonstrated by MRI. Brain Topogr 12:273-282