The left dorsolateral prefrontal cortex and caudate pathway: New evidence for cue‐induced craving of smokers

Although the activation of the prefrontal cortex (PFC) and the striatum had been found in smoking cue induced craving task, whether and how the functional interactions and white matter integrity between these brain regions contribute to craving processing during smoking cue exposure remains unknown. Twenty‐five young male smokers and 26 age‐ and gender‐matched nonsmokers participated in the smoking cue‐reactivity task. Craving related brain activation was extracted and psychophysiological interactions (PPI) analysis was used to specify the PFC‐efferent pathways contributed to smoking cue‐induced craving. Diffusion tensor imaging (DTI) and probabilistic tractography was used to explore whether the fiber connectivity strength facilitated functional coupling of the circuit with the smoking cue‐induced craving. The PPI analysis revealed the negative functional coupling of the left dorsolateral prefrontal cortex (DLPFC) and the caudate during smoking cue induced craving task, which positively correlated with the craving score. Neither significant activation nor functional connectivity in smoking cue exposure task was detected in nonsmokers. DTI analyses revealed that fiber tract integrity negatively correlated with functional coupling in the DLPFC‐caudate pathway and activation of the caudate induced by smoking cue in smokers. Moreover, the relationship between the fiber connectivity integrity of the left DLPFC‐caudate and smoking cue induced caudate activation can be fully mediated by functional coupling strength of this circuit in smokers. The present study highlighted the left DLPFC‐caudate pathway in smoking cue‐induced craving in smokers, which may reflect top‐down prefrontal modulation of striatal reward processing in smoking cue induced craving processing. Hum Brain Mapp 38:4644–4656, 2017. © 2017 Wiley Periodicals, Inc.

[1]  J. Palca Nicotine addiction , 1988, Nature.

[2]  M. Roesch,et al.  Orbitofrontal cortex, decision-making and drug addiction , 2006, Trends in Neurosciences.

[3]  Jonathan Downar,et al.  Noninvasive brain stimulation treatments for addiction and major depression , 2016, Annals of the New York Academy of Sciences.

[4]  R. C. Oldfield The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

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

[6]  Cyril Poupon,et al.  Microstructure of a three-way anatomical network predicts individual differences in response inhibition: A tractography study , 2012, NeuroImage.

[7]  C. Chen,et al.  A Memory Retrieval-Extinction Procedure to Prevent Drug Craving and Relapse , 2012, Science.

[8]  Sterling C. Johnson,et al.  Medial prefrontal functional connectivity—Relation to memory self-appraisal accuracy in older adults with and without memory disorders , 2012, Neuropsychologia.

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

[10]  J. Monterosso,et al.  Increased functional coupling between the left fronto‐parietal network and anterior insula predicts steeper delay discounting in smokers , 2014, Human brain mapping.

[11]  Nicholas B. Allen,et al.  Arrested development? Reconsidering dual-systems models of brain function in adolescence and disorders , 2012, Trends in Cognitive Sciences.

[12]  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.

[13]  Margaret Munro The hijacked brain , 2015, Nature.

[14]  J. Fiez,et al.  Prefrontal responses to drug cues: a neurocognitive analysis , 2004, Nature Neuroscience.

[15]  L. Kozlowski,et al.  The Fagerström Test for Nicotine Dependence: a revision of the Fagerström Tolerance Questionnaire. , 1991, British journal of addiction.

[16]  Edythe D London,et al.  Gene variants of brain dopamine pathways and smoking-induced dopamine release in the ventral caudate/nucleus accumbens. , 2006, Archives of general psychiatry.

[17]  K. Yuan,et al.  Functional Connectivity Abnormalities of Brain Regions with Structural Deficits in Young Adult Male Smokers , 2016, Front. Hum. Neurosci..

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

[19]  Filip Van Droogenbroeck,et al.  To Stop or Not to Stop , 2014, Research on aging.

[20]  M. Delgado,et al.  Toward a cumulative science of functional integration: A meta‐analysis of psychophysiological interactions , 2016, Human brain mapping.

[21]  K. Kiehl,et al.  Neural correlates of substance abuse: Reduced functional connectivity between areas underlying reward and cognitive control , 2014, Human brain mapping.

[22]  Sterling C. Johnson,et al.  A generalized form of context-dependent psychophysiological interactions (gPPI): A comparison to standard approaches , 2012, NeuroImage.

[23]  L. Nystrom,et al.  Tracking the hemodynamic responses to reward and punishment in the striatum. , 2000, Journal of neurophysiology.

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

[25]  F. Joseph McClernon,et al.  24-h smoking abstinence potentiates fMRI-BOLD activation to smoking cues in cerebral cortex and dorsal striatum , 2009, Psychopharmacology.

[26]  Chenwang Jin,et al.  Reduced frontal cortical thickness and increased caudate volume within fronto-striatal circuits in young adult smokers. , 2015, Drug and alcohol dependence.

[27]  Rita Z. Goldstein,et al.  Drug addiction and its underlying neurobiological basis: neuroimaging evidence for the involvement of the frontal cortex. , 2002, The American journal of psychiatry.

[28]  N. Volkow,et al.  Cocaine Cues and Dopamine in Dorsal Striatum: Mechanism of Craving in Cocaine Addiction , 2006, The Journal of Neuroscience.

[29]  D. Madden,et al.  Disconnected aging: Cerebral white matter integrity and age-related differences in cognition , 2014, Neuroscience.

[30]  S. Mori,et al.  Principles of Diffusion Tensor Imaging and Its Applications to Basic Neuroscience Research , 2006, Neuron.

[31]  M. Kaufman,et al.  Prefrontal and limbic resting state brain network functional connectivity differs between nicotine-dependent smokers and non-smoking controls. , 2012, Drug and alcohol dependence.

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

[33]  S. Shiffman,et al.  Prediction of lapse from associations between smoking and situational antecedents assessed by ecological momentary assessment. , 2007, Drug and alcohol dependence.

[34]  Charlene C. Wu,et al.  White-Matter Tract Connecting Anterior Insula to Nucleus Accumbens Correlates with Reduced Preference for Positively Skewed Gambles , 2016, Neuron.

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

[36]  C. Lamm,et al.  Transcranial Magnetic Stimulation of the Left Dorsolateral Prefrontal Cortex Decreases Cue-induced Nicotine Craving and EEG Delta Power , 2014, Brain Stimulation.

[37]  S. Thorpe,et al.  Responses of striatal neurons in the behaving monkey. 1. Head of the caudate nucleus , 1983, Behavioural Brain Research.

[38]  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.

[39]  S. Lukas,et al.  Insula–Dorsal Anterior Cingulate Cortex Coupling is Associated with Enhanced Brain Reactivity to Smoking Cues , 2015, Neuropsychopharmacology.

[40]  A. Bechara Decision making, impulse control and loss of willpower to resist drugs: a neurocognitive perspective , 2005, Nature Neuroscience.

[41]  Hans-Georg Buchholz,et al.  Association of low striatal dopamine d2 receptor availability with nicotine dependence similar to that seen with other drugs of abuse. , 2008, The American journal of psychiatry.

[42]  Tomáš Paus,et al.  Growth of white matter in the adolescent brain: Myelin or axon? , 2010, Brain and Cognition.

[43]  Samuel M. McClure,et al.  Annals of the New York Academy of Sciences a Dual-systems Perspective on Addiction: Contributions from Neuroimaging and Cognitive Training , 2022 .

[44]  Diana Martinez,et al.  Brain Stimulation in Addiction , 2016, Neuropsychopharmacology.

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

[46]  Alain Dagher,et al.  Dorsolateral prefrontal and orbitofrontal cortex interactions during self-control of cigarette craving , 2013, Proceedings of the National Academy of Sciences.

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

[48]  Lutz Jäncke,et al.  Structural and functional connectivity in healthy aging: Associations for cognition and motor behavior , 2016, Human brain mapping.

[49]  Kristopher J Preacher,et al.  SPSS and SAS procedures for estimating indirect effects in simple mediation models , 2004, Behavior research methods, instruments, & computers : a journal of the Psychonomic Society, Inc.

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

[51]  Naoaki Tanaka,et al.  Altered anterior‐posterior connectivity through the arcuate fasciculus in temporal lobe epilepsy , 2016, Human brain mapping.

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

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

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

[55]  T. Yuan,et al.  Transcranial direct current stimulation of the frontal-parietal-temporal area attenuates cue-induced craving for heroin. , 2016, Journal of Psychiatric Research.

[56]  D. Rubin,et al.  Activation in mesolimbic and visuospatial neural circuits elicited by smoking cues: evidence from functional magnetic resonance imaging. , 2002, The American journal of psychiatry.

[57]  Caryn Lerman,et al.  Dopamine Transporter Binding in Smokers and Nonsmokers , 2007, Clinical nuclear medicine.

[58]  N. Volkow,et al.  Striatocortical pathway dysfunction in addiction and obesity: differences and similarities , 2013, Critical reviews in biochemistry and molecular biology.

[59]  B. D. Bunday,et al.  To Stop or Not to Stop , 1975 .

[60]  K. Yuan,et al.  Neural correlates of 12-h abstinence-induced craving in young adult smokers: a resting-state study , 2017, Brain Imaging and Behavior.

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

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

[63]  Intra-regional and inter-regional abnormalities and cognitive control deficits in young adult smokers , 2016, Brain Imaging and Behavior.

[64]  Ti-Fei Yuan,et al.  10-Hz Repetitive Transcranial Magnetic Stimulation of the Left Dorsolateral Prefrontal Cortex Reduces Heroin Cue Craving in Long-Term Addicts , 2016, Biological Psychiatry.

[65]  K. Yuan,et al.  Striatum morphometry is associated with cognitive control deficits and symptom severity in internet gaming disorder , 2015, Brain Imaging and Behavior.