The effects of psilocybin and MDMA on between-network resting state functional connectivity in healthy volunteers

Frontiers in Human Neuroscience

Volumn 8, Issue MAY, 2014, Pages

  Roseman, Leor ^a   Leech, Robert ^a   Feilding, Amanda ^b   Nutt, David J ^a   Carhart Harris, Robin L ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b THE BECKLEY FOUNDATION   (United Kingdom)

Author keywords

5HT2A; Brain networks; Functional connectivity; MDMA; Psilocybin; Psychedelic; Resting state; Serotonin

Indexed keywords

3,4 METHYLENEDIOXYMETHAMPHETAMINE; PSILOCYBINE;

ADULT; ARTICLE; BRAIN FUNCTION; CONSCIOUSNESS LEVEL; CONTROLLED STUDY; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HEAD MOVEMENT; HUMAN; HUMAN EXPERIMENT; MALE; MOOD CHANGE; NORMAL HUMAN; PHARMACOLOGICAL BLOCKING; RESTING STATE NETWORK; SENSORIMOTOR FUNCTION; VISUAL HALLUCINATION;

EID: 84901639454     PISSN: None     EISSN: 16625161     Source Type: Journal    
DOI: 10.3389/fnhum.2014.00204     Document Type: Article

References (50)

1. Beckmann, C. F., Deluca, M., Devlin, J. T., and Smith, S. M. (2005). Investigations into resting-state connectivity using independent component analysis. Philos. Trans. R. Soc. B Biol. Sci. 360, 1001-1013. doi: 10.1098/rstb.2005.1634
2. Beckmann, C. F., Mackay, C. E., Filippini, N., and Smith, S. M. (2009). Group comparison of resting-state FMRI data using multi-subject ICA and dual regression. Neuroimage 47, S148. doi: 10.1016/S1053-8119(09)71511-3
3. Biswal, B., Yetkin, F. Z., Haughton, V. M., and Hyde, J. S. (1995). Functional connectivity in the motor cortex of resting human brain using echo-planar MRI. Magn. Reson. Med. 34, 537-541. doi: 10.1002/mrm.1910340409
4. Carhart-Harris, R. L., Erritzoe, D., Williams, T., Stone, J. M., Reed, L. J., Colasanti, A., et al. (2012a). Neural correlates of the psychedelic state as determined by fMRI studies with psilocybin. Proc. Natl. Acad. Sci. U.S.A. 109, 2138-2143. doi: 10.1073/pnas.1119598109
5. Carhart-Harris, R. L., Leech, R., Erritzoe, D., Williams, T. M., Stone, J. M., Evans, J., et al. (2012b). Functional connectivity measures after psilocybin inform a novel hypothesis of early psychosis. Schizophr. Bull. 39, 1343-1351. doi: 10.1093/schbul/sbs117
6. Carhart-Harris, R. L., Leech, R., Tagliazucchi, E., Hellyer, P. J., Chialvo, D. R., Feilding, A., et al. (2014a). The entropic brain: A theory of conscious states informed by neuroimaging research with psychedelic drugs. Front. Hum. Neurosci. 8:20. doi: 10.3389/fnhum.2014.00020
7. Carhart-Harris, R. L., Murphy, K., Leech, R., Erritzoe, D., Wall, M. B., Bart, F., et al. (2014b). The effects of acutely administered 3, 4-methylenedioxymethamphetamine on spontaneous brain function in healthy volunteers measured with arterial spin labelling and blood oxygen level-dependent resting-state functional connectivity. Biol. Psychiatry. doi: 10.1016/j.biopsych.2013.12.015. [Epub ahead of print].
8. Carhart-Harris, R. L., Williams, T. M., Sessa, B., Tyacke, R. J., Rich, A. S., Feilding, A., et al. (2011). The administration of psilocybin to healthy, hallucinogen-experienced volunteers in a mock-functional magnetic resonance imaging environment: a preliminary investigation of tolerability. J. Psychopharmacol. 25, 1562-1567. doi: 10.1177/0269881110367445
9. Chialvo, D. R. (2010). Emergent complex neural dynamics. Nat. Phys. 6, 744-750. doi: 10.1038/nphys1803
10. Damoiseaux, J. S., and Greicius, M. D. (2009). Greater than the sum of its parts: a review of studies combining structural connectivity and resting-state functional connectivity. Brain Struct. Funct. 213, 525-533. doi: 10.1007/s00429-009-0208-6
11. De Araujo, D. B., Ribeiro, S., Cecchi, G. A., Carvalho, F. M., Sanchez, T. A., Pinto, J. P., et al. (2012). Seeing with the eyes shut: neural basis of enhanced imagery following ayahuasca ingestion. Hum. Brain Mapp. 33, 2550-2560. doi: 10.1002/hbm.21381
12. Deco, G., Rolls, E. T., and Romo, R. (2009). Stochastic dynamics as a principle of brain function. Prog. Neurobiol. 88, 1-16. doi: 10.1016/j.pneurobio.2009.01.006
13. Dovern, A., Fink, G. R., Fromme, A. C., Wohlschlager, A. M., Weiss, P. H., and Riedl, V. (2012). Intrinsic network connectivity reflects consistency of synesthetic experiences. J. Neurosci. 32, 7614-7621. doi: 10.1523/JNEUROSCI.5401-11.2012
14. Erritzoe, D., Frokjaer, V. G., Haahr, M. T., Kalbitzer, J., Svarer, C., Holst, K. K., et al. (2010). Cerebral serotonin transporter binding is inversely related to body mass index. Neuroimage 52, 284-289. doi: 10.1016/j.neuroimage.2010.03.086
15. Fox, M. D., Snyder, A. Z., Vincent, J. L., Corbetta, M., Van Essen, D. C., and Raichle, M. E. (2005). The human brain is intrinsically organized into dynamic, anticorrelated functional networks. Proc. Natl. Acad. Sci. U.S.A. 102, 9673-9678. doi: 10.1073/pnas.0504136102
16. Friston, K. J., Harrison, L., and Penny, W. (2003). Dynamic causal modelling. Neuroimage 19, 1273-1302. doi: 10.1016/S1053-8119(03)00202-7
17. Gouzoulis-Mayfrank, E., Hermle, L., Kovar, K., and Sass, H. (1996). Entactogenic drugs "ecstasy"(MDMA), "eve"(MDE) and other ring-substituted methamphetamine derivatives. A new class of substances among illegal designer drugs?. Nervenarzt 67, 369.
18. Green, A. R., Mechan, A. O., Elliott, J. M., O'shea, E., and Colado, M. I. (2003). The pharmacology and clinical pharmacology of 3, 4-methylenedioxymethamphetamine (MDMA, "ecstasy"). Pharmacol. Rev. 55, 463-508. doi: 10.1124/pr.55.3.3
19. Hellyer, P. J., Shanahan, M., Scott, G., Wise, R. J., Sharp, D., and Leech, R. (2014). The control of global brain dynamics: opposing actions of frontoparietal control and default mode networks on attention. J. Neurosci. 34, 451-461. doi: 10.1523/JNEUROSCI.1853-13.2014
20. Huxley, A. (1959). The Doors of Perception and Heaven and Hell. Harmondsworth: Penguin Books.
21. Jenkinson, M., Bannister, P., Brady, M., and Smith, S. (2002). Improved optimization for the robust and accurate linear registration and motion correction of brain images. Neuroimage 17, 825-841. doi: 10.1006/nimg.2002.1132
22. Kanamaru, T., Fujii, H., and Aihara, K. (2013). Deformation of attractor landscape via cholinergic presynaptic modulations: a computational study using a phase neuron model. PLoS ONE 8:e53854. doi: 10.1371/journal.pone.0053854
23. Kolbrich, E. A., Goodwin, R. S., Gorelick, D. A., Hayes, R. J., Stein, E. A., and Huestis, M. A. (2008). Plasma pharmacokinetics of 3,4-methylenedioxymethamphetamine after controlled oral administration to young adults. Ther. Drug Monit. 30, 320-332. doi: 10.1097/FTD.0b013e3181684fa0
24. Laureys, S. (2005). The neural correlate of (un)awareness: lessons from the vegetative state. Trends Cogn. Sci. 9, 556-559. doi: 10.1016/j.tics.2005.10.010
25. Laureys, S., Owen, A., and Schiff, N. (2009). Coma science: clinical and ethical implications. Preface. Prog. Brain Res. 177, xiii-xiv. doi: 10.1016/S0079-6123(09)17736-1
26. Liechti, M. E., and Vollenweider, F. X. (2001). Which neuroreceptors mediate the subjective effects of MDMA in humans? A summary of mechanistic studies. Hum. Psychopharmacol. 16, 589-598. doi: 10.1002/hup.348
27. Luke, D. P., and Terhune, D. B. (2013). The induction of synaesthesia with chemical agents: a systematic review. Front. Psychol. 4:753. doi: 10.3389/fpsyg.2013.00753
28. Mamah, D., Barch, D. M., and Repovs, G. (2013). Resting state functional connectivity of five neural networks in bipolar disorder and schizophrenia. J. Affect. Disord. 150, 601-609. doi: 10.1016/j.jad.2013.01.051
29. Muthukumaraswamy, S. D., Carhart-Harris, R. L., Moran, R. J., Brookes, M. J., Williams, T. M., Errtizoe, D., et al. (2013). Broadband cortical desynchronization underlies the human psychedelic state. J. Neurosci. 33, 15171-15183. doi: 10.1523/JNEUROSCI.2063-13.2013
30. Nutt, D. J., King, L. A., and Nichols, D. E. (2013). Effects of Schedule I drug laws on neuroscience research and treatment innovation. Nat. Rev. Neurosci. 14, 577-585. doi: 10.1038/nrn3530
31. Power, J. D., Barnes, K. A., Snyder, A. Z., Schlaggar, B. L., and Petersen, S. E. (2012). Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion. Neuroimage 59, 2142-2154. doi: 10.1016/j.neuroimage.2011.10.018
32. Raichle, M. E., Macleod, A. M., Snyder, A. Z., Powers, W. J., Gusnard, D. A., and Shulman, G. L. (2001). A default mode of brain function. Proc. Natl. Acad. Sci. U.S.A. 98, 676-682. doi: 10.1073/pnas.98.2.676
33. Riba, J., Anderer, P., Morte, A., Urbano, G., Jane, F., Saletu, B., et al. (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. doi: 10.1046/j.1365-2125.2002.01609.x
34. Satterthwaite, T. D., Elliott, M. A., Gerraty, R. T., Ruparel, K., Loughead, J., Calkins, M. E., et al. (2013). An improved framework for confound regression and filtering for control of motion artifact in the preprocessing of resting-state functional connectivity data. Neuroimage 64, 240-256. doi: 10.1016/j.neuroimage.2012.08.052
35. Shannon, C. E., and Weaver, W. (1949). The Mathematical Theory of Communication. Urbana, IL: University of Illinois Press.
36. Sinke, C., Neufeld, J., Emrich, H. M., Dillo, W., Bleich, S., Zedler, M., et al. (2012). Inside a synesthete's head: a functional connectivity analysis with grapheme-color synesthetes. Neuropsychologia 50, 3363-3369. doi: 10.1016/j.neuropsychologia.2012.09.015
37. Smith, S. M. (2002). Fast robust automated brain extraction. Hum. Brain Mapp. 17, 143-155. doi: 10.1002/hbm.10062
38. Smith, S. M., and Brady, J. M. (1997). SUSAN-a new approach to low level image processing. Int. J. Comput. Vis. 23, 45-78. doi: 10.1023/A:1007963824710
39. Smith, S. M., Fox, P. T., Miller, K. L., Glahn, D. C., Fox, P. M., Mackay, C. E., et al. (2009). Correspondence of the brain's functional architecture during activation and rest. Proce. Natl. Acad. Sci. U.S.A. 106, 13040-13045. doi: 10.1073/pnas.0905267106
40. Smith, S. M., Jenkinson, M., Woolrich, M. W., Beckmann, C. F., Behrens, T. E., Johansen-Berg, H., et al. (2004). Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage 23, S208-S219. doi: 10.1016/j.neuroimage.2004.07.051
41. Tagliazucchi, E., Balenzuela, P., Fraiman, D., and Chialvo, D. R. (2012). Criticality in large-scale brain FMRI dynamics unveiled by a novel point process analysis. Front. Physiol. 3:15. doi: 10.3389/fphys.2012.00015
42. Tognoli, E., and Kelso, J. (2014). The metastable brain. Neuron 81, 35-48. doi: 10.1016/j.neuron.2013.12.022
43. Tononi, G. (2004). An information integration theory of consciousness. BMC Neurosci. 5:42. doi: 10.1186/1471-2202-5-42
44. Tononi, G. (2012). Integrated information theory of consciousness: an updated account. Arch. Ital. Biol. 150, 56-90. doi: 10.4449/aib.v149i5.1388
45. Van Den Heuvel, M., Mandl, R., and Pol, H. H. (2008). Normalized cut group clustering of resting-state FMRI data. PLoS ONE 3:e2001. doi: 10.1371/journal.pone.0002001
46. Van Wel, J. H., Kuypers, K. P., Theunissen, E. L., Bosker, W. M., Bakker, K., and Ramaekers, J. G. (2011). Blockade of 5-HT2 receptor selectively prevents MDMA-induced verbal memory impairment. Neuropsychopharmacology 36, 1932-1939. doi: 10.1038/npp.2011.80
47. Vollenweider, F. X., Leenders, K. L., Scharfetter, C., Maguire, P., Stadelmann, O., and Angst, J. (1997). Positron emission tomography and fluorodeoxyglucose studies of metabolic hyperfrontality and psychopathology in the psilocybin model of psychosis. Neuropsychopharmacology 16, 357-372. doi: 10.1016/S0893-133X(96)00246-1
48. Wise, S. P., Boussaoud, D., Johnson, P. B., and Caminiti, R. (1997). Premotor and parietal cortex: corticocortical connectivity and combinatorial computations 1. Annu. Rev. Neurosci. 20, 25-42. doi: 10.1146/annurev.neuro.20.1.25
49. Wood, J., Kim, Y., and Moghaddam, B. (2012). Disruption of prefrontal cortex large scale neuronal activity by different classes of psychotomimetic drugs. J. Neurosci. 32, 3022-3031. doi: 10.1523/JNEUROSCI.6377-11.2012
50. Yan, C.-G., Cheung, B., Kelly, C., Colcombe, S., Craddock, R. C., Di Martino, A., et al. (2013). A comprehensive assessment of regional variation in the impact of head micromovements on functional connectomics. Neuroimage76, 183-201. doi: 10.1016/j.neuroimage.2013.03.004