Striato-cortical tracts predict 12-h abstinence-induced lapse in smokers

Striatal circuit dysfunction is implicated in smoking behaviors and lapses during abstinence attempts. However, little is known about whether the structural connectivity of striatal tracts can be used to predict abstinence-induced craving and lapses. The tract strengths of striatal circuits were compared in 53 male nicotine-dependent cigarette smokers and 58 matched nonsmokers, using seed-based classification by diffusion tensor imaging (DTI) probabilistic tractography with 10 a priori target masks. A 12-h abstinence procedure was then employed, after which 31 individuals abstained and 22 lapsed. Linear regression and binary logistic regression was conducted to test whether the tract strength of frontostriatal circuits was associated with craving changes in abstainers and predicted lapse in smokers. Compared with nonsmokers, in the left hemisphere, smokers showed weaker tract strength in striatum-medial orbitofrontal cortex (mOFC), striatum-ventral lateral prefrontal cortex (vlPFC), striatum-inferior frontal gyrus (IFG) and striatum-posterior cingulate cortex (PCC) (Bonferroni corrected, p < 0.05/20 = 0.0025). In abstainers, the abstinence-induced increases in craving were associated with the tract strength of the left striatum-mOFC and striatum-vlPFC. The tract strength of left striatum-dorsolateral PFC (dlPFC) predicted lapse in smokers with an accuracy of 68.3%. These results provide system-level insights into the weaker tract strength of frontostriatal circuits in male smokers and their potential roles as neuroimaging markers for abstinence-induced craving and risk of lapse. Future studies in female smokers are needed to determine if this generalizes across genders.

[1]  K. Yuan,et al.  White matter integrity in young smokers: a tract‐based spatial statistics study , 2016, Addiction biology.

[2]  Sharon Morein-Zamir,et al.  Fronto-striatal circuits in response-inhibition: Relevance to addiction , 2015, Brain Research.

[3]  Matthijs Vink,et al.  Frontostriatal activity and connectivity increase during proactive inhibition across adolescence and early adulthood , 2014, Human brain mapping.

[4]  D. Ghahremani,et al.  Sex differences in striatal dopamine D2/D3 receptor availability in smokers and non-smokers. , 2012, The international journal of neuropsychopharmacology.

[5]  Heidi Johansen-Berg,et al.  Ventral Striatum/Nucleus Accumbens Activation to Smoking-Related Pictorial Cues in Smokers and Nonsmokers: A Functional Magnetic Resonance Imaging Study , 2005, Biological Psychiatry.

[6]  J. Weber,et al.  Prefrontal–striatal pathway underlies cognitive regulation of craving , 2010, Proceedings of the National Academy of Sciences.

[7]  Gary Glover,et al.  Frontostriatal connectivity and its role in cognitive control in parent-child dyads with ADHD. , 2007, The American journal of psychiatry.

[8]  Chenwang Jin,et al.  Core brain networks interactions and cognitive control in internet gaming disorder individuals in late adolescence/early adulthood , 2015, Brain Structure and Function.

[9]  S. Leh,et al.  Fronto-striatal connections in the human brain: A probabilistic diffusion tractography study , 2007, Neuroscience Letters.

[10]  Dick J Veltman,et al.  Brain activation patterns associated with cue reactivity and craving in abstinent problem gamblers, heavy smokers and healthy controls: an fMRI study , 2010, Addiction biology.

[11]  Yangding Li,et al.  The implication of frontostriatal circuits in young smokers: A resting‐state study , 2016, Human brain mapping.

[12]  K. Yuan,et al.  Frontostriatal circuits, resting state functional connectivity and cognitive control in internet gaming disorder , 2017, Addiction biology.

[13]  N. Volkow,et al.  Dysfunction of the prefrontal cortex in addiction: neuroimaging findings and clinical implications , 2011, Nature Reviews Neuroscience.

[14]  Jeffrey H. Meyer,et al.  Smoking-induced ventral striatum dopamine release. , 2004, The American journal of psychiatry.

[15]  Yihong Yang,et al.  Altered White Matter Integrity in Smokers Is Associated with Smoking Cessation Outcomes , 2017, Front. Hum. Neurosci..

[16]  Rachel Kozink,et al.  Association Between Baseline Corticothalamic-Mediated Inhibitory Control and Smoking Relapse Vulnerability , 2017, JAMA psychiatry.

[17]  Christian A. Rodriguez,et al.  Connectivity Strength of Dissociable Striatal Tracts Predict Individual Differences in Temporal Discounting , 2014, The Journal of Neuroscience.

[18]  Yangding Li,et al.  Abnormal brain white matter network in young smokers: a graph theory analysis study , 2018, Brain Imaging and Behavior.

[19]  S. Houle,et al.  Theta burst stimulation‐induced inhibition of dorsolateral prefrontal cortex reveals hemispheric asymmetry in striatal dopamine release during a set‐shifting task – a TMS–[11C]raclopride PET study , 2008, The European journal of neuroscience.

[20]  Alain Dagher,et al.  The hedonic response to cigarette smoking is proportional to dopamine release in the human striatum as measured by positron emission tomography and [11C]raclopride , 2004, Synapse.

[21]  Jason D. Robinson,et al.  Prequit fMRI responses to pleasant cues and cigarette-related cues predict smoking cessation outcome. , 2014, Nicotine & tobacco research : official journal of the Society for Research on Nicotine and Tobacco.

[22]  Paul J Laurienti,et al.  The association between frontal-striatal connectivity and sensorimotor control in cocaine users. , 2011, Drug and alcohol dependence.

[23]  N. Volkow,et al.  Addiction: Beyond dopamine reward circuitry , 2011, Proceedings of the National Academy of Sciences.

[24]  Amy C Janes,et al.  Striatal Morphology is Associated with Tobacco Cigarette Craving , 2015, Neuropsychopharmacology.

[25]  Michael X. Cohen,et al.  Connectivity-based segregation of the human striatum predicts personality characteristics , 2009, Nature Neuroscience.

[26]  S S Smith,et al.  Predicting smoking cessation. Who will quit with and without the nicotine patch. , 1994, JAMA.

[27]  Kristine M. McGlennen,et al.  Neural Correlates of Response Inhibition and Cigarette Smoking in Late Adolescence , 2011, Neuropsychopharmacology.

[28]  Nora D. Volkow,et al.  Cognitive control of drug craving inhibits brain reward regions in cocaine abusers , 2010, NeuroImage.

[29]  Richard De La Garza,et al.  Characterizing white matter changes in cigarette smokers via diffusion tensor imaging. , 2014, Drug and alcohol dependence.

[30]  Lawrence H. Sweet,et al.  Neural correlates of graphic cigarette warning labels predict smoking cessation relapse , 2017, Psychiatry Research: Neuroimaging.

[31]  Nora D. Volkow,et al.  The Brain on Drugs: From Reward to Addiction , 2015, Cell.

[32]  Jenna M. Sullivan,et al.  Sex Differences in the Brain's Dopamine Signature of Cigarette Smoking , 2014, The Journal of Neuroscience.

[33]  Matthew L. Ho,et al.  Brain metabolic changes during cigarette craving. , 2002, Archives of general psychiatry.

[34]  J. Detre,et al.  Neural Substrates of Abstinence-Induced Cigarette Cravings in Chronic Smokers , 2007, The Journal of Neuroscience.

[35]  R. Austin,et al.  Emergence of antibiotic resistance from multinucleated bacterial filaments , 2014, Proceedings of the National Academy of Sciences.

[36]  Yu-Shin Ding,et al.  Behavioral / Systems / Cognitive Activation of Orbital and Medial Prefrontal Cortex by Methylphenidate in Cocaine-Addicted Subjects But Not in Controls : Relevance to Addiction , 2005 .

[37]  Yangding Li,et al.  The left dorsolateral prefrontal cortex and caudate pathway: New evidence for cue‐induced craving of smokers , 2017, Human brain mapping.

[38]  Paul M. Cinciripini,et al.  Neural substrates of smoking cue reactivity: A meta-analysis of fMRI studies , 2012, NeuroImage.

[39]  D. Ghahremani,et al.  Behavioral and neural markers of cigarette-craving regulation in young-adult smokers during abstinence and after smoking , 2018, Neuropsychopharmacology.

[40]  N. Volkow,et al.  Neurobiologic Advances from the Brain Disease Model of Addiction. , 2016, The New England journal of medicine.

[41]  C. Liston,et al.  Frontostriatal microstructure modulates efficient recruitment of cognitive control. , 2006, Cerebral cortex.

[42]  H. Damasio,et al.  Damage to the Insula Disrupts Addiction to Cigarette Smoking , 2007, Science.

[43]  Christian A. Rodriguez,et al.  Adolescent impatience decreases with increased frontostriatal connectivity , 2015, Proceedings of the National Academy of Sciences.

[44]  A. Louilot,et al.  Lateralized interdependence between limbicotemporal and ventrostriatal dopaminergic transmission , 1994, Neuroscience.

[45]  A. Turken,et al.  Left inferior frontal gyrus is critical for response inhibition , 2008, BMC Neuroscience.

[46]  Shenmin Zhang,et al.  Hemispheric lateralization of resting-state functional connectivity of the ventral striatum: an exploratory study , 2017, Brain Structure and Function.

[47]  F. J. McClernon,et al.  Smoking Abstinence-Induced Changes in Resting State Functional Connectivity with Ventral Striatum Predict Lapse During a Quit Attempt , 2016, Neuropsychopharmacology.

[48]  Mark S. Cohen,et al.  Neural Substrates of Resisting Craving During Cigarette Cue Exposure , 2007, Biological Psychiatry.

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

[50]  Kathleen M. Gates,et al.  The first day is always the hardest: Functional connectivity during cue exposure and the ability to resist smoking in the initial hours of a quit attempt , 2017, NeuroImage.

[51]  H. Groenewegen,et al.  The prefrontal cortex and the integration of sensory, limbic and autonomic information. , 2000, Progress in brain research.