Re‐appraisal of negative emotions in cocaine dependence: dysfunctional corticolimbic activation and connectivity

Cocaine dependence is associated with pronounced elevations of negative affect and deficient regulation of negative emotions. We aimed to investigate the neural substrates of negative emotion regulation in cocaine‐dependent individuals (CDI), as compared to non‐drug‐using controls, using functional magnetic resonance imaging (fMRI) during a re‐appraisal task. Seventeen CDI abstinent for at least 15 days and without other psychiatric co‐morbidities and 18 intelligence quotient‐matched non‐drug‐using controls participated in the study. Participants performed the re‐appraisal task during fMRI scanning: they were exposed to 24 blocks of negative affective or neutral pictures that they should Observe (neutral pictures), Maintain (sustain the emotion elicited by negative pictures) or Suppress (regulate the emotion elicited by negative pictures through previously trained re‐appraisal techniques). Task‐related activations during two conditions of interest (Maintain>Observe and Suppress>Maintain) were analyzed using the general linear model in SPM8 software. We also performed psychophysiological interaction (PPI) seed‐based analyses based on one region from each condition: the dorsolateral prefrontal cortex (dlPFC—Maintain>Observe) and the inferior frontal gyrus (IFG—Suppress>Maintain). Results showed that cocaine users had increased right dlPFC and bilateral temporoparietal junction activations during Maintain>Observe, whereas they showed decreased right IFG, posterior cingulate cortex, insula and fusiform gyrus activations during Suppress>Maintain. PPI analyses showed that cocaine users had increased functional coupling between the dlPFC and emotion‐related regions during Maintain>Observe, whereas they showed decreased functional coupling between the right IFG and the amygdala during Suppress>Maintain. These findings indicate that CDI have dysfunctional corticolimbic activation and connectivity during negative emotion experience and re‐appraisal.

[1]  J. Monterosso,et al.  Different Forms of Self-Control Share a Neurocognitive Substrate , 2011, The Journal of Neuroscience.

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

[3]  D. Epstein,et al.  Daily life hour by hour, with and without cocaine: an ecological momentary assessment study , 2010, Psychopharmacology.

[4]  Helen Young,et al.  Society for the study of addiction. , 1999, Addiction biology.

[5]  A. Aleman,et al.  Bidirectional information flow in frontoamygdalar circuits in humans: a dynamic causal modeling study of emotional associative learning. , 2012, Cerebral cortex.

[6]  Nora D Volkow,et al.  Neurocircuitry of Addiction , 2010, Neuropsychopharmacology.

[7]  J. Uslaner,et al.  Association of depressive symptoms during abstinence with the subjective high produced by cocaine. , 1999, The American journal of psychiatry.

[8]  A. Sanfey,et al.  Reappraising the ultimatum: an fMRI study of emotion regulation and decision making. , 2013, Cerebral cortex.

[9]  Javier Moltó.  Un nuevo método para el estudio experimental de las emociones: el International Affective Picture System (IAPS). Adaptación española. Baremos nacionales , 2000 .

[10]  Kevin N. Ochsner,et al.  The Neural Bases of Distraction and Reappraisal , 2010, Journal of Cognitive Neuroscience.

[11]  Sang Hee Kim,et al.  The effect of cognitive reappraisal on physiological reactivity and emotional memory. , 2012, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[12]  Peter Falkai,et al.  Fear is only as deep as the mind allows A coordinate-based meta-analysis of neuroimaging studies on the regulation of negative affect , 2011, NeuroImage.

[13]  K. Phan,et al.  Neural substrates for voluntary suppression of negative affect: A functional magnetic resonance imaging study , 2005, Biological Psychiatry.

[14]  E. Walker,et al.  Diagnostic and Statistical Manual of Mental Disorders , 2013 .

[15]  Jeffrey S. Maxwell,et al.  Right Dorsolateral Prefrontal Cortical Activity and Behavioral Inhibition , 2009, Psychological science.

[16]  Andrés Catena,et al.  Trait impulsivity and prefrontal gray matter reductions in cocaine dependent individuals. , 2012, Drug and alcohol dependence.

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

[18]  S. Whiteside,et al.  The Five Factor Model and impulsivity: using a structural model of personality to understand impulsivity , 2001 .

[19]  C. Conners,et al.  Clinical use of rating scales in diagnosis and treatment of attention-deficit/hyperactivity disorder. , 1999, Pediatric clinics of North America.

[20]  R. Davidson.  Right Dorsolateral Prefrontal Cortical Activity and Behavioral , 2009 .

[21]  R. Raedt,et al.  The effect of one left-sided dorsolateral prefrontal sham-controlled HF-rTMS session on approach and withdrawal related emotional neuronal processes , 2011, Clinical Neurophysiology.

[22]  Megan E. Piper,et al.  Addiction motivation reformulated: an affective processing model of negative reinforcement. , 2004, Psychological review.

[23]  J. Gross.  Emotion Regulation: Past, Present, Future , 1999 .

[24]  Y. Ono,et al.  The International Personality Disorder Examination. The World Health Organization/Alcohol, Drug Abuse, and Mental Health Administration international pilot study of personality disorders. , 1994, Archives of general psychiatry.

[25]  R. Sinha,et al.  Stress-induced cocaine craving and hypothalamic-pituitary-adrenal responses are predictive of cocaine relapse outcomes. , 2006, Archives of general psychiatry.

[26]  William A. Cunningham,et al.  Tools of the Trade Type I and Type II error concerns in fMRI research : rebalancing the scale , 2009 .

[27]  M. Yücel,et al.  The role of affective dysregulation in drug addiction. , 2010, Clinical psychology review.

[28]  Jane E Joseph,et al.  Neural Correlates of Emotional Reactivity in Sensation Seeking , 2009, Psychological science.

[29]  H. Garavan,et al.  Neural mechanisms underlying drug-related cue distraction in active cocaine users , 2009, Pharmacology Biochemistry and Behavior.

[30]  J C Gore,et al.  Functional magnetic resonance imaging of cocaine craving. , 2001, The American journal of psychiatry.

[31]  B. Levine,et al.  The functional neuroanatomy of autobiographical memory: A meta-analysis , 2006, Neuropsychologia.

[32]  Melissa L. Allen,et al.  Kaufman Brief Intelligence Test , 2021, Encyclopedia of Autism Spectrum Disorders.

[33]  C. Kilts,et al.  Neural activity related to anger in cocaine-dependent men: a possible link to violence and relapse. , 2000, The American journal on addictions.

[34]  Karl J. Friston,et al.  Psychophysiological and Modulatory Interactions in Neuroimaging , 1997, NeuroImage.

[35]  William A. Cunningham,et al.  Type I and Type II error concerns in fMRI research: re-balancing the scale. , 2009, Social cognitive and affective neuroscience.

[36]  P. Lang,et al.  International Affective Picture System (IAPS): Instruction Manual and Affective Ratings (Tech. Rep. No. A-4) , 1999 .

[37]  L. Clark,et al.  Comparison of impulsivity and working memory in cocaine addiction and pathological gambling: Implications for cocaine-induced neurotoxicity. , 2012, Drug and alcohol dependence.

[38]  R. Sinha,et al.  Enhanced Sensitivity to Stress and Drug/Alcohol Craving in Abstinent Cocaine-Dependent Individuals Compared to Social Drinkers , 2008, Neuropsychopharmacology.

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

[40]  P. Boesiger,et al.  Imbalance between Left and Right Dorsolateral Prefrontal Cortex in Major Depression Is Linked to Negative Emotional Judgment: An fMRI Study in Severe Major Depressive Disorder , 2008, Biological Psychiatry.

[41]  D. J. Dickinson.  Test Review: Kaufman, A. S., and Kaufman, N. L. (1985). Kaufman Test of Educational Achievement, Brief Form. Circle Pines, MN: American Guidance Service , 1986 .

[42]  Luke Clark,et al.  The role of interoception in addiction: A critical review , 2012, Neuroscience & Biobehavioral Reviews.