Evidence for involvement of the insula in the psychotropic effects of THC in humans: a double-blind, randomized pharmacological MRI study.

The main reason for recreational use of cannabis is the 'high', the primary psychotropic effect of Δ9-tetrahydrocannabinol (THC). This psychoactive compound of cannabis induces a range of subjective, physical and mental reactions. The effect on heart rate is pronounced and complicates bloodflow-based neuroimaging of psychotropic effects of THC. In this study we investigated the effects of THC on baseline brain perfusion and activity in association with the induction of 'feeling high'. Twenty-three subjects participated in a pharmacological MRI study, where we applied arterial spin labelling (ASL) to measure perfusion, and resting-state functional MRI to assess blood oxygen level-dependent signal fluctuation as a measure of baseline brain activity. Feeling high was assessed with a visual analogue scale and was compared to the imaging measures. THC increased perfusion in the anterior cingulate cortex, superior frontal cortex, and insula, and reduced perfusion in the post-central and occipital gyrus. Baseline brain activity was altered, indicated by increased amplitude of fluctuations in resting-state functional MRI signal after THC administration in the insula, substantia nigra and cerebellum. Perfusion changes in frontal cortex were negatively correlated with ratings of feeling high, suggesting an interaction between cognitive control and subjective effects of THC. In conclusion, an acute THC challenge altered baseline brain perfusion and activity, especially in frontal brain areas involved in cognitive and emotional processes, and the insula, associated with interoceptive awareness. These changes may represent the THC-induced neurophysiological correlates of feeling high. The alterations in baseline brain perfusion and activity also have relevance for studies on task-related effects of THC on brain function.

[1]  A. Craig,et al.  How do you feel — now? The anterior insula and human awareness , 2009, Nature Reviews Neuroscience.

[2]  T G Turkington,et al.  Marijuana intoxication and brain activation in marijuana smokers. , 1997, Life sciences.

[3]  H. Critchley,et al.  Neural systems supporting interoceptive awareness , 2004, Nature Neuroscience.

[4]  S. Rombouts,et al.  Consistent resting-state networks across healthy subjects , 2006, Proceedings of the National Academy of Sciences.

[5]  J. Detre,et al.  A theoretical and experimental investigation of the tagging efficiency of pseudocontinuous arterial spin labeling , 2007, Magnetic resonance in medicine.

[6]  Erno J. Hermans,et al.  Enhanced sensitivity with fast three‐dimensional blood‐oxygen‐level‐dependent functional MRI: comparison of SENSE–PRESTO and 2D‐EPI at 3 T , 2008, NMR in biomedicine.

[7]  L. F. Barrett,et al.  Handbook of Emotions , 1993 .

[8]  M. van Buchem,et al.  Can arterial spin labeling detect white matter perfusion signal? , 2009, Magnetic resonance in medicine.

[9]  A. Bowdle,et al.  Psychedelic Effects of Ketamine in Healthy Volunteers: Relationship to Steady‐state Plasma Concentrations , 1998, Anesthesiology.

[10]  T G Turkington,et al.  Regional cerebral blood flow and depersonalization after tetrahydrocannabinol adrninistration , 1999, Acta psychiatrica Scandinavica.

[11]  A. Craig,et al.  Ecstatic epileptic seizures: A potential window on the neural basis for human self-awareness , 2009, Epilepsy & Behavior.

[12]  M. Posner,et al.  Cognitive and emotional influences in anterior cingulate cortex , 2000, Trends in Cognitive Sciences.

[13]  A. Bond,et al.  The use of analogue scales in rating subjective feelings , 1974 .

[14]  D. Piomelli The molecular logic of endocannabinoid signalling , 2003, Nature Reviews Neuroscience.

[15]  L. Parsons,et al.  Endocannabinoid signaling in neurotoxicity and neuroprotection. , 2010, Neurotoxicology.

[16]  J. Detre,et al.  Perfusion magnetic resonance imaging with continuous arterial spin labeling: methods and clinical applications in the central nervous system. , 1999, European journal of radiology.

[17]  D. Kavanagh,et al.  Being stoned: a review of self-reported cannabis effects. , 2003, Drug and alcohol review.

[18]  Philip K. McGuire,et al.  Neural Basis of Δ-9-Tetrahydrocannabinol and Cannabidiol: Effects During Response Inhibition , 2008, Biological Psychiatry.

[19]  M. P. van den Heuvel,et al.  Normalized Cut Group Clustering of Resting-State fMRI Data , 2008, PloS one.

[20]  X Golay,et al.  Non-invasive Measurement of Perfusion: a Critical Review of Arterial Spin Labelling Techniques , 2022 .

[21]  A. Craig,et al.  Interoception and Emotion : a Neuroanatomical Perspective , 2007 .

[22]  Antoine Bechara,et al.  The hidden island of addiction: the insula , 2009, Trends in Neurosciences.

[23]  Chaozhe Zhu,et al.  Amplitude of low frequency fluctuation within visual areas revealed by resting-state functional MRI , 2007, NeuroImage.

[24]  S. Batkai,et al.  Hemodynamic effects of cannabinoids: coronary and cerebral vasodilation mediated by cannabinoid CB(1) receptors. , 2001, European journal of pharmacology.

[25]  P. McGuire,et al.  Distinct effects of {delta}9-tetrahydrocannabinol and cannabidiol on neural activation during emotional processing. , 2009, Archives of general psychiatry.

[26]  Paul W. Burgess,et al.  Distinct functional connectivity associated with lateral versus medial rostral prefrontal cortex: A meta-analysis , 2010, NeuroImage.

[27]  HighWire Press Philosophical Transactions of the Royal Society of London , 1781, The London Medical Journal.

[28]  J. Guelfi,et al.  Hedonic response to sucrose solutions and the fear of weight gain in patients with eating disorders , 2002, Psychiatry Research.

[29]  J. Quickfall,et al.  Brain neuroimaging in cannabis use: a review. , 2006, The Journal of neuropsychiatry and clinical neurosciences.

[30]  R. Mathew,et al.  Acute changes in cerebral blood flow after smoking marijuana. , 1993, Life sciences.

[31]  K. Davis,et al.  Two systems of resting state connectivity between the insula and cingulate cortex , 2009, Human brain mapping.

[32]  A F Cohen,et al.  Effect of intrapulmonary tetrahydrocannabinol administration in humans , 2008, Journal of psychopharmacology.

[33]  D. Alsop,et al.  Continuous flow‐driven inversion for arterial spin labeling using pulsed radio frequency and gradient fields , 2008, Magnetic resonance in medicine.

[34]  Timothy G. Turkington,et al.  Cerebellar activity and disturbed time sense after THC , 1998, Brain Research.

[35]  James Provenzale,et al.  Time course of tetrahydrocannabinol-induced changes in regional cerebral blood flow measured with positron emission tomography , 2002, Psychiatry Research: Neuroimaging.

[36]  P. McGuire,et al.  Neuroimaging in cannabis use: a systematic review of the literature , 2009, Psychological Medicine.

[37]  E. Russo Cannabis and Cannabinoids: Pharmacology, Toxicology, and Therapeutic Potential , 2002 .

[38]  N. Ramsey,et al.  Methods of the Pharmacological Imaging of the Cannabinoid System (PhICS) study: towards understanding the role of the brain endocannabinoid system in human cognition , 2011, International journal of methods in psychiatric research.

[39]  D. S. Williams,et al.  Magnetic resonance imaging of perfusion using spin inversion of arterial water. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[40]  André Aleman,et al.  Activation of Anterior Insula during Self-Reflection , 2009, PloS one.

[41]  Vincent A Magnotta,et al.  Effects of smoking marijuana on focal attention and brain blood flow , 2007, Human psychopharmacology.

[42]  Lineke Zuurman,et al.  Biomarkers for the effects of cannabis and THC in healthy volunteers. , 2009, British journal of clinical pharmacology.

[43]  L. Iversen,et al.  Cannabis and the brain. , 2003, Brain : a journal of neurology.

[44]  R. Kahn,et al.  Central nervous system effects of haloperidol on THC in healthy male volunteers , 2010, Journal of psychopharmacology.

[45]  G H Glover,et al.  Image‐based method for retrospective correction of physiological motion effects in fMRI: RETROICOR , 2000, Magnetic resonance in medicine.

[46]  A. Craig How do you feel? Interoception: the sense of the physiological condition of the body , 2002, Nature Reviews Neuroscience.

[47]  E. Chronicle,et al.  Functional Imaging Studies in Cannabis Users , 2007, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[48]  A. Ameri The effects of cannabinoids on the brain , 1999, Progress in Neurobiology.

[49]  M. D’Esposito,et al.  Empirical Analyses of BOLD fMRI Statistics , 1997, NeuroImage.

[50]  Brian Pittman,et al.  Effects of haloperidol on the behavioral, subjective, cognitive, motor, and neuroendocrine effects of Δ-9-tetrahydrocannabinol in humans , 2008, Psychopharmacology.

[51]  Gregory G. Brown,et al.  Measurement of cerebral perfusion with arterial spin labeling: Part 1. Methods , 2007, Journal of the International Neuropsychological Society.

[52]  M. D’Esposito,et al.  Empirical analyses of BOLD fMRI statistics. I. Spatially unsmoothed data collected under null-hypothesis conditions. , 1997, NeuroImage.

[53]  Lucina Q. Uddin,et al.  The anterior insula in autism: Under-connected and under-examined , 2009, Neuroscience & Biobehavioral Reviews.

[54]  Chaozhe Zhu,et al.  An improved approach to detection of amplitude of low-frequency fluctuation (ALFF) for resting-state fMRI: Fractional ALFF , 2008, Journal of Neuroscience Methods.

[55]  R. Mathew,et al.  Acute changes in cerebral blood flow associated with marijuana smoking , 1989, Acta psychiatrica Scandinavica.

[56]  A. Craig,et al.  Emotional moments across time: a possible neural basis for time perception in the anterior insula , 2009, Philosophical Transactions of the Royal Society B: Biological Sciences.

[57]  H. Critchley Neural mechanisms of autonomic, affective, and cognitive integration , 2005, The Journal of comparative neurology.

[58]  Chiara Nosarti,et al.  Modulation of mediotemporal and ventrostriatal function in humans by Delta9-tetrahydrocannabinol: a neural basis for the effects of Cannabis sativa on learning and psychosis. , 2009, Archives of general psychiatry.

[59]  R. Mathew,et al.  Regional Cerebral Blood Flow after Marijuana Smoking , 1992, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.