Cannabis, cigarettes, and their co-occurring use: Disentangling differences in default mode network functional connectivity.

BACKGROUND Resting-state functional connectivity is a noninvasive, neuroimaging method for assessing neural network function. Altered functional connectivity among regions of the default-mode network have been associated with both nicotine and cannabis use; however, less is known about co-occurring cannabis and tobacco use. METHODS We used posterior cingulate cortex (PCC) seed-based resting-state functional connectivity analyses to examine default mode network (DMN) connectivity strength differences between four groups: (1) individuals diagnosed with cannabis dependence who do not smoke tobacco (n=19; ages 20-50), (2) cannabis-dependent individuals who smoke tobacco (n=23, ages 21-52), (3) cannabis-naïve, nicotine-dependent individuals who smoke tobacco (n=24, ages 21-57), and (4) cannabis- and tobacco-naïve healthy controls (n=21, ages 21-50), controlling for age, sex, and alcohol use. We also explored associations between connectivity strength and measures of cannabis and tobacco use. RESULTS PCC seed-based analyses identified the core nodes of the DMN (i.e., PCC, medial prefrontal cortex, inferior parietal cortex, and temporal cortex). In general, the cannabis-dependent, nicotine-dependent, and co-occurring use groups showed lower DMN connectivity strengths than controls, with unique group differences in connectivity strength between the PCC and the cerebellum, medial prefrontal cortex, parahippocampus, and anterior insula. In cannabis-dependent individuals, PCC-right anterior insula connectivity strength correlated with duration of cannabis use. CONCLUSIONS This study extends previous research that independently examined the differences in resting-state functional connectivity among individuals who smoke cannabis and tobacco by including an examination of co-occurring cannabis and tobacco use and provides further evidence that cannabis and tobacco exposure is associated with alterations in DMN connectivity.

[1]  K. Davis,et al.  Connectivity-based parcellation of the human frontal polar cortex , 2014, Brain Structure and Function.

[2]  Jeremy D. Schmahmann,et al.  Functional topography in the human cerebellum: A meta-analysis of neuroimaging studies , 2009, NeuroImage.

[3]  B. Biswal,et al.  Functional connectivity in the motor cortex of resting human brain using echo‐planar mri , 1995, Magnetic resonance in medicine.

[4]  Joel M. Mumma,et al.  The Effects of Chronic Cigarette Smoking on Gray Matter Volume: Influence of Sex , 2014, PloS one.

[5]  Karl Fagerstrom,et al.  Measuring nicotine dependence: A review of the Fagerstrom Tolerance Questionnaire , 1989, Journal of Behavioral Medicine.

[6]  Koene R. A. Van Dijk,et al.  The parahippocampal gyrus links the default‐mode cortical network with the medial temporal lobe memory system , 2014, Human brain mapping.

[7]  Jesse J. Suh,et al.  Neural responses to subliminally presented cannabis and other emotionally evocative cues in cannabis-dependent individuals , 2013, Psychopharmacology.

[8]  Daniel S. Margulies,et al.  Mapping the functional connectivity of anterior cingulate cortex , 2007, NeuroImage.

[9]  Katherine E. Prater,et al.  Distinct Cerebellar Contributions to Intrinsic Connectivity Networks , 2009, NeuroImage.

[10]  Seong-Whan Lee,et al.  Cocaine addiction related reproducible brain regions of abnormal default-mode network functional connectivity: A group ICA study with different model orders , 2013, Neuroscience Letters.

[11]  Nick F Ramsey,et al.  Evidence for involvement of the insula in the psychotropic effects of THC in humans: a double-blind, randomized pharmacological MRI study. , 2011, The international journal of neuropsychopharmacology.

[12]  A. Scallet.  Neurotoxicology of cannabis and THC: A review of chronic exposure studies in animals , 1991, Pharmacology Biochemistry and Behavior.

[13]  R. Buckner,et al.  Functional-Anatomic Fractionation of the Brain's Default Network , 2010, Neuron.

[14]  Kaustubh Supekar,et al.  Dynamic Reconfiguration of Structural and Functional Connectivity Across Core Neurocognitive Brain Networks with Development , 2011, The Journal of Neuroscience.

[15]  M. Fox,et al.  Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging , 2007, Nature Reviews Neuroscience.

[16]  Brian A. King,et al.  Current Cigarette Smoking Among Adults — United States, 2005–2012 , 2014, MMWR. Morbidity and mortality weekly report.

[17]  S. Heishman,et al.  Meta-analysis of the acute effects of nicotine and smoking on human performance , 2010, Psychopharmacology.

[18]  R. Mechoulam,et al.  The isolation and structure of delta-1-tetrahydrocannabinol and other neutral cannabinoids from hashish. , 1971, Journal of the American Chemical Society.

[19]  H. Gu,et al.  Association of nicotine addiction and nicotine's actions with separate cingulate cortex functional circuits. , 2009, Archives of general psychiatry.

[20]  Abraham Z. Snyder,et al.  A default mode of brain function: A brief history of an evolving idea , 2007, NeuroImage.

[21]  D. Metzger,et al.  The Fifth Edition of the Addiction Severity Index. , 1992, Journal of substance abuse treatment.

[22]  G. Glover,et al.  Dissociable Intrinsic Connectivity Networks for Salience Processing and Executive Control , 2007, The Journal of Neuroscience.

[23]  John K. Robinson,et al.  Changes in hippocampal morphology following chronic treatment with the synthetic cannabinoid WIN 55,212-2 , 2000, Brain Research.

[24]  Christian F. Doeller,et al.  Interaction Between Hippocampus and Cerebellum Crus I in Sequence-Based but not Place-Based Navigation. , 2015, Cerebral cortex.

[25]  Y. Sarne,et al.  Cannabinoids: between neuroprotection and neurotoxicity. , 2005, Current drug targets. CNS and neurological disorders.

[26]  Marcel Zeelenberg,et al.  Data analysis 2 , 2016 .

[27]  E. Stein,et al.  Down-Regulation of Amygdala and Insula Functional Circuits by Varenicline and Nicotine in Abstinent Cigarette Smokers , 2013, Biological Psychiatry.

[28]  Domenico Aquino,et al.  Gray Matter Reduction in the Vermis and CRUS-II Is Associated with Social and Interaction Deficits in Low-Functioning Children with Autistic Spectrum Disorders: a VBM-DARTEL Study , 2013, The Cerebellum.

[29]  Vinod Menon,et al.  Functional connectivity in the resting brain: A network analysis of the default mode hypothesis , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[30]  J. Gabrieli,et al.  The frontopolar cortex and human cognition: Evidence for a rostrocaudal hierarchical organization within the human prefrontal cortex , 2000, Psychobiology.

[31]  K. Carroll,et al.  Clinical correlates of co-occurring cannabis and tobacco use: a systematic review. , 2012, Addiction.

[32]  C. Lerman,et al.  Cognitive function during nicotine withdrawal: Implications for nicotine dependence treatment , 2014, Neuropharmacology.

[33]  Wanqing Li,et al.  The default mode network and social understanding of others: what do brain connectivity studies tell us , 2014, Front. Hum. Neurosci..

[34]  Bharat B. Biswal,et al.  Competition between functional brain networks mediates behavioral variability , 2008, NeuroImage.

[35]  Eric Nyberg,et al.  Nicotine effects on default mode network during resting state , 2011, Psychopharmacology.

[36]  A. Childress,et al.  Cannabis, Cigarettes, and Their Co-Occurring Use: Disentangling Differences in Gray Matter Volume , 2015, The international journal of neuropsychopharmacology.

[37]  Elliot A. Stein,et al.  Resting state functional connectivity in addiction: Lessons learned and a road ahead , 2012, NeuroImage.

[38]  Maurizio Corbetta,et al.  The human brain is intrinsically organized into dynamic, anticorrelated functional networks. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[39]  Laura Blanco-Hinojo,et al.  Functional connectivity alterations in brain networks relevant to self-awareness in chronic cannabis users. , 2014, Journal of psychiatric research.

[40]  Kosha Ruparel,et al.  Large-scale brain network coupling predicts acute nicotine abstinence effects on craving and cognitive function. , 2014, JAMA psychiatry.

[41]  Dewen Hu,et al.  Disruptive changes of cerebellar functional connectivity with the default mode network in schizophrenia , 2014, Schizophrenia Research.

[42]  R. Blair.  The amygdala and ventromedial prefrontal cortex in morality and psychopathy , 2007, Trends in Cognitive Sciences.

[43]  Todd B. Parrish,et al.  The posterior cingulate and medial prefrontal cortex mediate the anticipatory allocation of spatial attention , 2003, NeuroImage.

[44]  V. Calhoun,et al.  Reduced executive and default network functional connectivity in cigarette smokers , 2015, Human brain mapping.

[45]  N. Solowij,et al.  The chronic effects of cannabis on memory in humans: a review. , 2008, Current drug abuse reviews.

[46]  Senhua Zhu,et al.  Resting State Brain Function Analysis Using Concurrent BOLD in ASL Perfusion fMRI , 2013, PloS one.

[47]  Fenna M. Krienen,et al.  Segregated Fronto-Cerebellar Circuits Revealed by Intrinsic Functional Connectivity , 2009, Cerebral cortex.

[48]  G. Winterer,et al.  Neuroprotective and neurotoxic effects of nicotine. , 2009, Pharmacopsychiatry.

[49]  Linda C. Sobell,et al.  Timeline Follow-Back A Technique for Assessing Self-Reported Alcohol Consumption , 1992 .

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

[51]  David M. Cole,et al.  Manipulating brain connectivity with δ9-tetrahydrocannabinol: A pharmacological resting state FMRI study , 2012, NeuroImage.

[52]  R. Poulton,et al.  A longitudinal study of the effects of tobacco and cannabis exposure on lung function in young adults. , 2002, Addiction.

[53]  S. Petersen,et al.  The maturing architecture of the brain's default network , 2008, Proceedings of the National Academy of Sciences.

[54]  D. Schacter,et al.  The Brain's Default Network , 2008, Annals of the New York Academy of Sciences.

[55]  Xiaoping Hu,et al.  Abnormal Brain Default-Mode Network Functional Connectivity in Drug Addicts , 2011, PloS one.

[56]  G L Shulman,et al.  INAUGURAL ARTICLE by a Recently Elected Academy Member:A default mode of brain function , 2001 .

[57]  Kevin Murphy,et al.  Anatomical and functional overlap within the insula and anterior cingulate cortex during interoception and phobic symptom provocation , 2013, Human brain mapping.

[58]  Stephen M Smith,et al.  Correspondence of the brain's functional architecture during activation and rest , 2009, Proceedings of the National Academy of Sciences.

[59]  A. Pfefferbaum,et al.  The Resting Brain of Alcoholics. , 2015, Cerebral cortex.