Altered functional connectivity of the insular cortex across prefrontal networks in cocaine addiction

Interoception is theorized to be an important process mediating substance use disorders, and the insular cortex is recognized as a core neural region supporting interoception. The purpose of this study was to compare the integration of the insular cortex into prefrontal-related resting-state networks between individuals with cocaine dependence and healthy controls. Participants comprised 41 patients with cocaine dependence and 19 controls who underwent a resting-state 3-T functional magnetic resonance imaging scan. Individuals with cocaine dependence demonstrated altered functional connectivity of the insular cortex, predominantly the right insular cortex, with all eight prefrontal-related resting-state networks identified through Independent Component Analysis (ICA). A conjunction analysis demonstrated that the right insular cortex was the neural region with the highest number of common group differences across the networks. There was no evidence that insular cortex connectivity commonly differed between groups for non-prefrontal-related networks. Further, seed-based functional connectivity analyses extended the network analyses and indicated that cocaine dependence was associated with greater connectivity of the right insula with the dorsomedial prefrontal cortex, inferior frontal gyrus, and bilateral dorsolateral prefrontal cortex. These data support the hypothesis that cocaine dependence is related to altered functional interactions of the insular cortex with prefrontal networks. The results suggest possible neural mechanisms by which the insular cortex and interoceptive information influence cognitive control and decision-making processes presumably mediated by prefrontal networks in the cocaine dependence process.

[1]  Brent G. Nelson,et al.  Frontal Hyperconnectivity Related to Discounting and Reversal Learning in Cocaine Subjects , 2011, Biological Psychiatry.

[2]  Yihong Yang,et al.  Mesocorticolimbic circuits are impaired in chronic cocaine users as demonstrated by resting-state functional connectivity , 2010, NeuroImage.

[3]  Jonathan D. Cohen,et al.  Anterior Cingulate Conflict Monitoring and Adjustments in Control , 2004, Science.

[4]  Edward E. Smith,et al.  The Role of Parietal Cortex in Verbal Working Memory , 1998, The Journal of Neuroscience.

[5]  V. Menon,et al.  A critical role for the right fronto-insular cortex in switching between central-executive and default-mode networks , 2008, Proceedings of the National Academy of Sciences.

[6]  Heather L. Urry,et al.  Failure to Regulate: Counterproductive Recruitment of Top-Down Prefrontal-Subcortical Circuitry in Major Depression , 2007, The Journal of Neuroscience.

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

[8]  John Duncan,et al.  The role of the right inferior frontal gyrus: inhibition and attentional control , 2010, NeuroImage.

[9]  K. Berridge,et al.  The psychology and neurobiology of addiction: an incentive-sensitization view. , 2000, Addiction.

[10]  E. Miller,et al.  An integrative theory of prefrontal cortex function. , 2001, Annual review of neuroscience.

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

[12]  Remco J. Renken,et al.  Group analyses of connectivity-based cortical parcellation using repeated k-means clustering , 2009, NeuroImage.

[13]  M. Botvinick,et al.  Conflict monitoring and cognitive control. , 2001, Psychological review.

[14]  J. Anthony,et al.  From First Drug Use to Drug Dependence: Developmental Periods of Risk for Dependence upon Marijuana, Cocaine, and Alcohol , 2002, Neuropsychopharmacology.

[15]  V. Menon,et al.  Saliency, switching, attention and control: a network model of insula function , 2010, Brain Structure and Function.

[16]  H. Critchley,et al.  Conjoint activity of anterior insular and anterior cingulate cortex: awareness and response , 2010, Brain Structure and Function.

[17]  R W Cox,et al.  AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. , 1996, Computers and biomedical research, an international journal.

[18]  B. Wetering,et al.  Error-processing deficits in patients with cocaine dependence , 2007, Biological Psychology.

[19]  E. Stein,et al.  Cue-induced cocaine craving: neuroanatomical specificity for drug users and drug stimuli. , 2000, The American journal of psychiatry.

[20]  Peter Bossaerts,et al.  Risk and risk prediction error signals in anterior insula , 2010, Brain Structure and Function.

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

[22]  J. R. Augustine.  Circuitry and functional aspects of the insular lobe in primates including humans , 1996, Brain Research Reviews.

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

[24]  A. Bechara,et al.  The insula and drug addiction: an interoceptive view of pleasure, urges, and decision-making , 2010, Brain Structure and Function.

[25]  K. Berridge,et al.  The incentive sensitization theory of addiction: some current issues , 2008, Philosophical Transactions of the Royal Society B: Biological Sciences.

[26]  A. Mayer,et al.  Enhanced cue reactivity and fronto-striatal functional connectivity in cocaine use disorders. , 2011, Drug and alcohol dependence.

[27]  G. Deco,et al.  Emerging concepts for the dynamical organization of resting-state activity in the brain , 2010, Nature Reviews Neuroscience.

[28]  Hugh Garavan,et al.  The Role of Cognitive Control in Cocaine Dependence , 2007, Neuropsychology Review.

[29]  Katiuscia Sacco,et al.  Functional connectivity of the insula in the resting brain , 2011, NeuroImage.

[30]  Vince D. Calhoun,et al.  A review of group ICA for fMRI data and ICA for joint inference of imaging, genetic, and ERP data , 2009, NeuroImage.

[31]  R. Kahn,et al.  Functionally linked resting‐state networks reflect the underlying structural connectivity architecture of the human brain , 2009, Human brain mapping.

[32]  Mark W. Woolrich,et al.  Advances in functional and structural MR image analysis and implementation as FSL , 2004, NeuroImage.

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

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

[35]  S Makeig,et al.  Spatially independent activity patterns in functional MRI data during the stroop color-naming task. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[36]  S. Quartz,et al.  Human Insula Activation Reflects Risk Prediction Errors As Well As Risk , 2008, The Journal of Neuroscience.

[37]  T. Robbins,et al.  Stop-signal inhibition disrupted by damage to right inferior frontal gyrus in humans , 2003, Nature Neuroscience.

[38]  Naomi B. Pitskel,et al.  Three Systems of Insular Functional Connectivity Identified with Cluster Analysis , 2010, Cerebral cortex.

[39]  Timothy E. J. Behrens,et al.  Choice, uncertainty and value in prefrontal and cingulate cortex , 2008, Nature Neuroscience.

[40]  F. Moeller,et al.  Relationship between attentional bias to cocaine-related stimuli and impulsivity in cocaine-dependent subjects , 2011, The American journal of drug and alcohol abuse.

[41]  Christine L. Cox,et al.  Reduced Interhemispheric Resting State Functional Connectivity in Cocaine Addiction , 2011, Biological Psychiatry.

[42]  E. Kandel,et al.  Resolving Emotional Conflict: A Role for the Rostral Anterior Cingulate Cortex in Modulating Activit , 2006 .

[43]  E. Reiman,et al.  Thermosensory activation of insular cortex , 2000, Nature Neuroscience.

[44]  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.

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

[46]  Paul W. Burgess,et al.  When I think about me and simulate you: Medial rostral prefrontal cortex and self-referential processes , 2010, NeuroImage.

[47]  T. Robbins,et al.  Inhibition and the right inferior frontal cortex , 2004, Trends in Cognitive Sciences.

[48]  L. Fellows,et al.  Dorsal Medial Prefrontal Cortex Plays a Necessary Role in Rapid Error Prediction in Humans , 2008, The Journal of Neuroscience.

[49]  J. Pekar,et al.  A method for making group inferences from functional MRI data using independent component analysis , 2001, Human brain mapping.

[50]  Timothy E. J. Behrens,et al.  Learning the value of information in an uncertain world , 2007, Nature Neuroscience.

[51]  Rita Z. Goldstein,et al.  Disrupted Functional Connectivity with Dopaminergic Midbrain in Cocaine Abusers , 2010, PloS one.

[52]  C. Kilts,et al.  The neural correlates of cue-induced craving in cocaine-dependent women. , 2004, The American journal of psychiatry.

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

[54]  Daniel S. Margulies,et al.  Delineating self-referential processing from episodic memory retrieval: Common and dissociable networks , 2010, NeuroImage.

[55]  Maneesh C. Patel,et al.  Distinct frontal systems for response inhibition, attentional capture, and error processing , 2010, Proceedings of the National Academy of Sciences.

[56]  K. Berridge,et al.  Incentive-sensitization and addiction. , 2001, Addiction.