Manipulating brain connectivity with δ9-tetrahydrocannabinol: A pharmacological resting state FMRI study

NeuroImage

Volumn 63, Issue 3, 2012, Pages 1701-1711

  Klumpers, Linda E ^a   Cole, David M ^b,c,d   Khalili Mahani, Najmeh ^b,c   Soeter, Roelof P ^b,c   te Beek, Erik T ^a   Rombouts, Serge A R B ^b,c   van Gerven, Joop M A ^a  

^a CENTRE FOR HUMAN DRUG RESEARCH   (Netherlands)

^b LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^c LEIDEN UNIVERSITY   (Netherlands)

^d IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

Brain connectivity; CNS effects; Pharmacodynamics; Pharmacokinetics; Resting state FMRI; THC

Indexed keywords

CANNABINOID 1 RECEPTOR; DRONABINOL; HYDROCORTISONE; PLACEBO; PROLACTIN;

ADULT; ANXIETY; AREA UNDER THE CURVE; ARTICLE; BODY POSTURE; BRAIN FUNCTION; BRAIN REGION; CEREBELLUM; COMPUTER PROGRAM; CONTROLLED STUDY; CROSSOVER PROCEDURE; DOUBLE BLIND PROCEDURE; DRUG BLOOD LEVEL; DRUG CLEARANCE; DRUG DOSE COMPARISON; DRUG HALF LIFE; DRUG WITHDRAWAL; FEMALE; FRONTAL CORTEX; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HALLUCINATION; HEART RATE; HEMISPHERIC DOMINANCE; HUMAN; HUMAN EXPERIMENT; IMAGE ANALYSIS; MALE; MAXIMUM PLASMA CONCENTRATION; NAUSEA; NORMAL HUMAN; PERCEPTION; PRIORITY JOURNAL; RANDOMIZED CONTROLLED TRIAL; RECEPTOR DENSITY; REGRESSION ANALYSIS; REST; SENSORIMOTOR CORTEX; SIDE EFFECT; STATISTICAL SIGNIFICANCE; TIME PERCEPTION; TIME TO MAXIMUM PLASMA CONCENTRATION; VISUAL ANALOG SCALE; VISUAL CORTEX; VOLUNTEER; VOXEL BASED MORPHOMETRY;

ADOLESCENT; ADULT; BRAIN; BRAIN MAPPING; CANNABINOID RECEPTOR AGONISTS; DOUBLE-BLIND METHOD; FEMALE; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; MIDDLE AGED; NEURAL PATHWAYS; REST; TETRAHYDROCANNABINOL; YOUNG ADULT;

EID: 84866285509     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2012.07.051     Document Type: Article

References (71)

1. Beckmann C.F., Smith S.M. Tensorial extensions of independent component analysis for multisubject FMRI analysis. NeuroImage 2005, 25:294-311.
2. Beckmann C.F., DeLuca M., Devlin J.T., Smith S.M. Investigations into resting-state connectivity using independent component analysis. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 2005, 360:1001-1013.
3. Benowitz N.L., Jones R.T., Lerner C.B. Depression of growth hormone and cortisol response to insulin-induced hypoglycemia after prolonged oral delta-9-tetrahydrocannabinol administration in man. J. Clin. Endocrinol. Metab. 1976, 42:938-941.
4. Bhattacharyya S., Fusar-Poli P., Borgwardt S., Martin-Santos R., Nosarti C., O'Carroll C., Allen P., Seal M.L., Fletcher P.C., Crippa J.A., Giampietro V., Mechelli A., Atakan Z., McGuire P. Modulation of mediotemporal and ventrostriatal function in humans by Delta9-tetrahydrocannabinol: a neural basis for the effects of Cannabis sativa on learning and psychosis. Arch. Gen. Psychiatry 2009, 66:442-451.
5. Birn R.M. The role of physiological noise in resting-state functional connectivity. NeuroImage 2012, 62(2):864-870. (Epub 2012 Jan 8).
6. Birn R.M., Smith M.A., Jones T.B., Bandettini P.A. The respiration response function: the temporal dynamics of fMRI signal fluctuations related to changes in respiration. NeuroImage 2008, 40:644-654.
7. Biswal B.B., Mennes M., Zuo X.N., Gohel S., Kelly C., Smith S.M., Beckmann C.F., Adelstein J.S., Buckner R.L., Colcombe S., Dogonowski A.M., Ernst M., Fair D., Hampson M., Hoptman M.J., Hyde J.S., Kiviniemi V.J., Kotter R., Li S.J., Lin C.P., Lowe M.J., Mackay C., Madden D.J., Madsen K.H., Margulies D.S., Mayberg H.S., McMahon K., Monk C.S., Mostofsky S.H., Nagel B.J., Pekar J.J., Peltier S.J., Petersen S.E., Riedl V., Rombouts S.A., Rypma B., Schlaggar B.L., Schmidt S., Seidler R.D., Siegle G.J., Sorg C., Teng G.J., Veijola J., Villringer A., Walter M., Wang L., Weng X.C., Whitfield-Gabrieli S., Williamson P., Windischberger C., Zang Y.F., Zhang H.Y., Castellanos F.X., Milham M.P. Toward discovery science of human brain function. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:4734-4739.
8. Bocker K.B., Hunault C.C., Gerritsen J., Kruidenier M., Mensinga T.T., Kenemans J.L. Cannabinoid modulations of resting state EEG theta power and working memory are correlated in humans. J. Cogn. Neurosci. 2010, 22:1906-1916.
9. Bond A., Lader M. The use of analogue scales in rating subjective feelings. Br. J. Med. Psychol. 1974, 47:211-218.
10. Borgwardt S.J., Allen P., Bhattacharyya S., Fusar-Poli P., Crippa J.A., Seal M.L., Fraccaro V., Atakan Z., Martin-Santos R., O'Carroll C., Rubia K., McGuire P.K. Neural basis of delta-9-tetrahydrocannabinol and cannabidiol: effects during response inhibition. Biol. Psychiatry 2008, 64:966-973.
11. Bowdle T.A., Radant A.D., Cowley D.S., Kharasch E.D., Strassman R.J., Roy-Byrne P.P. Psychedelic effects of ketamine in healthy volunteers: relationship to steady-state plasma concentrations. Anesthesiology 1998, 88:82-88.
12. Carter R.M., O'Doherty J.P., Seymour B., Koch C., Dolan R.J. Contingency awareness in human aversive conditioning involves the middle frontal gyrus. NeuroImage 2006, 29:1007-1012.
13. Chang C., Cunningham J.P., Glover G.H. Influence of heart rate on the BOLD signal: the cardiac response function. NeuroImage 2009, 44:857-869.
14. Chen C.L., Willis B.A., Mooney L., Ong G.K., Lim C.N., Lowe S.L., Tauscher-Wisniewski S., Cutler G.B., Wiss S.D. Cortisol response to individualised graded insulin infusions: a reproducible biomarker for CNS compounds inhibiting HPA activation. Br. J. Clin. Pharmacol. 2010, 70:886-894.
15. Cole D.M., Beckmann C.F., Long C.J., Matthews P.M., Durcan M.J., Beaver J.D. Nicotine replacement in abstinent smokers improves cognitive withdrawal symptoms with modulation of resting brain network dynamics. NeuroImage 2010, 52:590-599.
16. Corchero J., Fuentes J.A., Manzanares J. Chronic treatment with CP-55,940 regulates corticotropin releasing factor and proopiomelanocortin gene expression in the hypothalamus and pituitary gland of the rat. Life Sci. 1999, 64:905-911.
17. Crockett D., Klonoff H., Clark C. The effects of marijuana on verbalization and thought processes. J. Pers. Assess. 1976, 40:582-587.
18. Damoiseaux J.S., Rombouts S.A., Barkhof F., Scheltens P., Stam C.J., Smith S.M., Beckmann C.F. Consistent resting-state networks across healthy subjects. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:13848-13853.
19. Daw N.D., O'Doherty J.P., Dayan P., Seymour B., Dolan R.J. Cortical substrates for exploratory decisions in humans. Nature 2006, 441:876-879.
20. De Luca M., Beckmann C.F., De Stefano N., Matthews P.M., Smith S.M. fMRI resting state networks define distinct modes of long-distance interactions in the human brain. NeuroImage 2006, 29:1359-1367.
21. de Visser S.J., van der Post J., Pieters M.S., Cohen A.F., van Gerven J.M. Biomarkers for the effects of antipsychotic drugs in healthy volunteers. Br. J. Clin. Pharmacol. 2001, 51:119-132.
22. Desmond J.E., Glover G.H. Estimating sample size in functional MRI (fMRI) neuroimaging studies: statistical power analyses. J. Neurosci. Methods 2002, 118:115-128.
23. Dewey W.L., Peng T.C., Harris L.S. The effect of 1-trans-delta 9-tetrahydrocannabinol on the hypothalamo-hypophyseal-adrenal axis of rats. Eur. J. Pharmacol. 1970, 12:382-384.
24. du Boisgueheneuc F., Levy R., Volle E., Seassau M., Duffau H., Kinkingnehun S., Samson Y., Zhang S., Dubois B. Functions of the left superior frontal gyrus in humans: a lesion study. Brain 2006, 129:3315-3328.
25. Eggan S.M., Lewis D.A. Immunocytochemical distribution of the cannabinoid CB1 receptor in the primate neocortex: a regional and laminar analysis. Cereb. Cortex 2007, 17:175-191.
26. Emrich H.M., Weber M.M., Wendl A., Zihl J., von M.L., Hanisch W. Reduced binocular depth inversion as an indicator of cannabis-induced censorship impairment. Pharmacol. Biochem. Behav. 1991, 40:689-690.
27. Filippini N., MacIntosh B.J., Hough M.G., Goodwin G.M., Frisoni G.B., Smith S.M., Matthews P.M., Beckmann C.F., Mackay C.E. Distinct patterns of brain activity in young carriers of the APOE-epsilon4 allele. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:7209-7214.
28. Foltin R.W., Fischman M.W., Brady J.V., Bernstein D.J., Capriotti R.M., Nellis M.J., Kelly T.H. Motivational effects of smoked marijuana: behavioral contingencies and low-probability activities. J. Exp. Anal. Behav. 1990, 53:5-19.
29. Fox M.D., Snyder A.Z., Vincent J.L., Raichle M.E. Intrinsic fluctuations within cortical systems account for intertrial variability in human behavior. Neuron 2007, 56:171-184.
30. Goodwin R.S., Baumann M.H., Gorelick D.A., Schwilke E., Schwope D.M., Darwin W.D., Kelly D.L., Schroeder J.R., Ortemann-Renon C., Bonnet D., Huestis M.A. CB1 - cannabinoid receptor antagonist effects on cortisol in cannabis-dependent men. Am. J. Drug Alcohol Abuse 2011, 38(1):114-119. (Epub 2011 Jul 29).
31. Greicius M.D., Srivastava G., Reiss A.L., Menon V. Default-mode network activity distinguishes Alzheimer's disease from healthy aging: evidence from functional MRI. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:4637-4642.
32. Herkenham M. Cannabinoid receptor localization in brain: relationship to motor and reward systems. Ann. N. Y. Acad. Sci. 1992, 654:19-32.
33. Hine M.L. The recovery of fields of vision in concussion injuries of the occipital cortex. Br. J. Ophthalmol. 1918, 2:12-25.
34. Jha A.P., Ranucci M.B., Giuliani N.R. Organization of mnemonic and response operations within prefrontal cortex. Brain Res. 2006, 1097:133-141.
35. Khalili-Mahani N., Zoethout R.M., Beckmann C.F., Baerends E., de Kam M.L., Soeter R.P., Dahan A., van Buchem M.A., van Gerven J.M., Rombouts S.A. Effects of morphine and alcohol on functional brain connectivity during "resting state": a placebo-controlled crossover study in healthy young men. Hum. Brain Mapp 2011, 33(5):1003-10018. (Epub 2011 Mar 9). 10.1002/hbm.21265.
36. Kim W., Doyle M.E., Liu Z., Lao Q., Shin Y.K., Carlson O.D., Kim H.S., Thomas S., Napora J.K., Lee E.K., Moaddel R., Wang Y., Maudsley S., Martin B., Kulkarni R.N., Egan J.M. Cannabinoids inhibit insulin receptor signaling in pancreatic beta-cells. Diabetes 2011, 60:1198-1209.
37. Koechlin E., Basso G., Pietrini P., Panzer S., Grafman J. The role of the anterior prefrontal cortex in human cognition. Nature 1999, 399:148-151.
38. Koethe D., Gerth C.W., Neatby M.A., Haensel A., Thies M., Schneider U., Emrich H.M., Klosterkotter J., Schultze-Lutter F., Leweke F.M. Disturbances of visual information processing in early states of psychosis and experimental delta-9-tetrahydrocannabinol altered states of consciousness. Schizophr. Res. 2006, 88:142-150.
39. Kolmel H.W. Pure homonymous hemiachromatopsia. Findings with neuro-ophthalmologic examination and imaging procedures. Eur. Arch. Psychiatry Neurol. Sci. 1988, 237:237-243.
40. Laird A.R., Fox P.M., Eickhoff S.B., Turner J.A., Ray K.L., McKay D.R., Glahn D.C., Beckmann C.F., Smith S.M., Fox P.T. Behavioral interpretations of intrinsic connectivity networks. J. Cogn. Neurosci. 2011, 23:4022-4037.
41. Mathew R.J., Wilson W.H., Turkington T.G., Coleman R.E. Cerebellar activity and disturbed time sense after THC. Brain Res 1998, 797:183-189.
42. Mathew R.J., Wilson W.H., Chiu N.Y., Turkington T.G., DeGrado T.R., Coleman R.E. Regional cerebral blood flow and depersonalization after tetrahydrocannabinol administration. Acta Psychiatr. Scand. 1999, 100:67-75.
43. Mathew R.J., Wilson W.H., Turkington T.G., Hawk T.C., Coleman R.E., DeGrado T.R., Provenzale J. Time course of tetrahydrocannabinol-induced changes in regional cerebral blood flow measured with positron emission tomography. Psychiatry Res. 2002, 116:173-185.
44. McDonald J., Schleifer L., Richards J.B., de W.H. Effects of THC on behavioral measures of impulsivity in humans. Neuropsychopharmacology 2003, 28:1356-1365.
45. Mennes M., Kelly C., Zuo X.N., Di M.A., Biswal B.B., Castellanos F.X., Milham M.P. Inter-individual differences in resting-state functional connectivity predict task-induced BOLD activity. NeuroImage 2010, 50:1690-1701.
46. Miller E.K., Cohen J.D. An integrative theory of prefrontal cortex function. Annu. Rev. Neurosci. 2001, 24:167-202.
47. Morrison P.D., Zois V., McKeown D.A., Lee T.D., Holt D.W., Powell J.F., Kapur S., Murray R.M. The acute effects of synthetic intravenous delta9-tetrahydrocannabinol on psychosis, mood and cognitive functioning. Psychol. Med. 2009, 39:1607-1616.
48. Nichols T.E., Holmes A.P. Nonparametric permutation tests for functional neuroimaging: a primer with examples. Hum. Brain Mapp. 2002, 15:1-25.
49. Nyberg L., Kim A.S., Habib R., Levine B., Tulving E. Consciousness of subjective time in the brain. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:22356-22359.
50. Quigley M., Cordes D., Turski P., Moritz C., Haughton V., Seth R., Meyerand M.E. Role of the corpus callosum in functional connectivity. AJNR Am. J. Neuroradiol. 2003, 24:208-212.
51. Ramaekers J.G., Kauert G., Theunissen E.L., Toennes S.W., Moeller M.R. Neurocognitive performance during acute THC intoxication in heavy and occasional cannabis users. J. Psychopharmacol. 2009, 23:266-277.
52. Ranganathan M., Braley G., Pittman B., Cooper T., Perry E., Krystal J., D'Souza D.C. The effects of cannabinoids on serum cortisol and prolactin in humans. Psychopharmacology. (Berl) 2009, 203:737-744.
53. Romero J., Hillard C.J., Calero M., Rabano A. Fatty acid amide hydrolase localization in the human central nervous system: an immunohistochemical study. Brain Res. Mol. Brain Res. 2002, 100:85-93.
54. Rose J.E., McClernon F.J., Froeliger B., Behm F.M., Preud'homme X., Krystal A.D. Repetitive transcranial magnetic stimulation of the superior frontal gyrus modulates craving for cigarettes. Biol. Psychiatry 2011, 70(8):794-799. (Epub 2011 Jul 18).
55. Starck T., Remes J., Nikkinen J., Tervonen O., Kiviniemi V. Correction of low-frequency physiological noise from the resting state BOLD fMRI--Effect on ICA default mode analysis at 1.5 T. J. Neurosci. Methods 2010, 186(2):179-185.
56. Smith S.M., Nichols T.E. Threshold-free cluster enhancement: addressing problems of smoothing, threshold dependence and localisation in cluster inference. NeuroImage 2009, 44:83-98.
57. Smith S.M., Fox P.T., Miller K.L., Glahn D.C., Fox P.M., Mackay C.E., Filippini N., Watkins K.E., Toro R., Laird A.R., Beckmann C.F. Correspondence of the brain's functional architecture during activation and rest. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:13040-13045.
58. Stokes P.R., Egerton A., Watson B., Reid A., Breen G., Lingford-Hughes A., Nutt D.J., Mehta M.A. Significant decreases in frontal and temporal [11C]-raclopride binding after THC challenge. NeuroImage 2010, 52:1521-1527.
59. Stoodley C.J., Schmahmann J.D. Functional topography in the human cerebellum: a meta-analysis of neuroimaging studies. NeuroImage 2009, 44:489-501.
60. Strougo A., Zuurman L., Roy C., Pinquier J.L., van Gerven J.M., Cohen A.F., Schoemaker R.C. Modelling of the concentration-effect relationship of THC on central nervous system parameters and heart rate - insight into its mechanisms of action and a tool for clinical research and development of cannabinoids. J. Psychopharmacol. 2008, 22:717-726.
61. Tinklenberg J.R., Kopell B.S., Melges F.T., Hollister L.E. Marihuana and alcohol, time production and memory functions. Arch. Gen. Psychiatry 1972, 27:812-815.
62. van Hell H.H., Bossong M.G., Jager G., Kristo G., van Osch M.J., Zelaya F., Kahn R.S., Ramsey N.F. Evidence for involvement of the insula in the psychotropic effects of THC in humans: a double-blind, randomized pharmacological MRI study. Int. J. Neuropsychopharmacol. 2011, 1-12.
63. Venkatraman V., Rosati A.G., Taren A.A., Huettel S.A. Resolving response, decision, and strategic control: evidence for a functional topography in dorsomedial prefrontal cortex. J. Neurosci. 2009, 29:13158-13164.
64. Wenger T., Fernandez-Ruiz J.J., Ramos J.A. Immunocytochemical demonstration of CB1 cannabinoid receptors in the anterior lobe of the pituitary gland. J. Neuroendocrinol. 1999, 11:873-878.
65. Winton-Brown T.T., Allen P., Bhattacharyya S., Borgwardt S.J., Fusar-Poli P., Crippa J.A., Seal M.L., Martin-Santos R., Ffytche D., Zuardi A.W., Atakan Z., McGuire P.K. Modulation of auditory and visual processing by delta-9-tetrahydrocannabinol and cannabidiol: an FMRI study. Neuropsychopharmacology 2011, 36:1340-1348.
66. Wise R.G., Preston C. What is the value of human FMRI in CNS drug development?. Drug Discov. Today 2010, 15:973-980.
67. Zhang Y., Brady M., Smith S. Segmentation of brain MR images through a hidden Markov random field model and the expectation-maximization algorithm. IEEE Trans. Med. Imaging 2001, 20:45-57.
68. Zuurman L., Roy C., Schoemaker R., Hazekamp A., den Hartigh J., Bender J., Verpoorte R., Pinquier J., Cohen A., van Gerven J. Effect of intrapulmonary tetrahydrocannabinol administration in humans. J. Psychopharmacol. 2008, 22:707-716.
69. Zuurman L., Roy C., Schoemaker R.C., Hazekamp A., Den Hartigh J., Bender J.C., Verpoorte R., Pinquier J.L., Cohen A.F., van Gerven J.M. Effect of intrapulmonary tetrahydrocannabinol administration in humans. J. Psychopharmacol. 2008, 22:707-716.
70. Zuurman L., Roy C., Schoemaker R., Amatsaleh A., Guimaeres L., Pinquier J., Cohen A., van Gerven J. Inhibition of THC-induced effects on the central nervous system and heart rate by a novel CB1 receptor antagonist AVE1625. J. Psychopharmacol. 2008, 24(3):363-371. (Epub 2008 Sep 18).
71. Zuurman L., Ippel A.E., Moin E., van Gerven J.M. Biomarkers for the effects of cannabis and THC in healthy volunteers. Br. J. Clin. Pharmacol. 2009, 67:5-21.