Effective connectivity predicts cognitive empathy in cocaine addiction: a spectral dynamic causal modeling study

Abu-Akel, A., & Shamay-Tsoory, S. (2011). Neuroanatomical and neurochemical bases of theory of mind. Neuropsychologia, 49(11), 2971–2984. https://doi.org/10.1016/j.neuropsychologia.2011.07.012 Banziger, T., Grandjean, D., & Scherer, K. R. (2009). Emotion recognition from expressions in face, voice, and body: the Multimodal Emotion Recognition Test (MERT). Emotion, 9(5), 691–704. https://doi.org/10.1037/a0017088 Behzadi, Y., Restom, K., Liau, J., & Liu, T. T. (2007). A component based noise correction method (CompCor) for BOLD and perfusion based fMRI. Neuroimage, 37(1), 90–101. https://doi.org/10.1016/j.neuroimage.2007.04.042 Blair, R. J. R. (2003). Facial expressions, their communicatory functions and neuro-cognitive substrates. Philosophical Transactions Biological Sciences, 358(1431), 561–572. Bonci, A., Bernardi, G., Grillner, P., & Mercuri, N. B. (2003). The dopamine-containing neuron: maestro or simple musician in the orchestra of addiction? Trends in Pharmacological Sciences, 24(4), 172–177. https://doi.org/10.1016/S0165-6147(03)00068-3 Bracht, T., Horn, H., Strik, W., Federspiel, A., Razavi, N., Stegmayer, K., et al. (2014). White matter pathway organization of the reward system is related to positive and negative symptoms in schizophrenia. Schizophrenia Research, 153(1–3), 136–142. https://doi.org/10.1016/j.schres.2014.01.015 Chang, L., Alicata, D., Ernst, T., & Volkow, N. (2007). Structural and metabolic brain changes in the striatum associated with methamphetamine abuse. Addiction, 102, 16–32. https://doi.org/10.1111/j.1360-0443.2006.01782.x Childress, A. R., Mozley, P. D., McElgin, W., Fitzgerald, J., Reivich, M., & O’Brien, C. P. (1999). Limbic activation during cue-induced cocaine craving. The American Journal of Psychiatry, 156(1), 11–18. https://doi.org/10.1176/ajp.156.1.11 Chrysikou, E. G., & Thompson, W. J. (2016). Assessing cognitive and affective empathy through the interpersonal reactivity index: An argument against a two-factor model (vol 23, pg 769, 2016). Assessment, 23(6), 778–778. https://doi.org/10.1177/1073191115607974 Colnat-Coulbois, S., Mok, K., Klein, D., Penicaud, S., Tanriverdi, T., & Olivier, A. (2010). Tractography of the amygdala and hippocampus: anatomical study and application to selective amygdalohippocampectomy. Journal of Neurosurgery, 113(6), 1135–1143. https://doi.org/10.3171/2010.3.JNS091832 Davis, M. H. (1980). A multidimensional approach to individual differences in empathy. JSAS Catalog of Selected Documents in Psychology, 10, 85. Davis, M. H. (1983). Measuring individual differences in empathy: Evidence for a multidimensional approach. Journal of Personality and Social Psychology, 44(1), 113–126. https://doi.org/10.1037/0022-3514.44.1.113 Decety, J. (2015). The neural pathways, development and functions of empathy. Current Opinion in Behavioral Sciences, 3, 1–6. https://doi.org/10.1016/j.cobeha.2014.12.001 Dziobek, I., Rogers, K., Fleck, S., Bahnemann, M., Heekeren, H. R., Wolf, O. T., et al. (2008). Dissociation of Cognitive and Emotional Empathy in Adults with Asperger Syndrome Using the Multifaceted Empathy Test (MET). Journal of Autism and Developmental Disorders, 38(3), 464–473. https://doi.org/10.1007/s10803-007-0486-x Ersche, K. D., Hagan, C. C., Smith, D. G., Jones, P. S., Calder, A. J., & Williams, G. B. (2015). In the face of threat: neural and endocrine correlates of impaired facial emotion recognition in cocaine dependence. Translational Psychiatry, 5, e57010.1038/tp.2015.58. Fernandez-Serrano, M. J., Lozano, O., Perez-Garcia, M., & Verdejo-Garcia, A. (2010). Impact of severity of drug use on discrete emotions recognition in polysubstance abusers. Drug and Alcohol Dependence, 109(1–3), 57–64. https://doi.org/10.1016/j.drugalcdep.2009.12.007 Fotros, A., Casey, K. F., Larcher, K., Verhaeghe, J. A. J., Cox, S. M. L., Gravel, P., et al. (2013). Cocaine Cue-Induced Dopamine Release in Amygdala and Hippocampus: A High-Resolution PET [18F]Fallypride Study in Cocaine Dependent Participants [Original Article]. Neuropsychopharmacology, 38, 1780. https://doi.org/10.1038/npp.2013.77 Fowler, J. S., Volkow, N. D., Kassed, C. A., & Chang, L. (2007). Imaging the addicted human brain. Science and Practice Perspectives, 3(2), 4–16. Fox, H. C., Axelrod, S. R., Paliwal, P., Sleeper, J., & Sinha, R. (2007). Difficulties in emotion regulation and impulse control during cocaine abstinence. Drug and Alcohol Dependence, 89(2–3), 298–301. https://doi.org/10.1016/j.drugalcdep.2006.12.026 Fox, H. C., Bergquist, K. L., Casey, J., Hong, K. A., & Sinha, R. (2011). Selective cocaine-related difficulties in emotional intelligence: relationship to stress and impulse control. The American Journal on Addictions, 20(2), 151–160. https://doi.org/10.1111/j.1521-0391.2010.00108.x Friston, K. J., Harrison, L., & Penny, W. (2003). Dynamic causal modelling. Neuroimage, 19(4), 1273–1302. Friston, K. J., Kahan, J., Biswal, B., & Razi, A. (2014). A DCM for resting state fMRI. Neuroimage, 94, 396–407. https://doi.org/10.1016/j.neuroimage.2013.12.009 Friston, K. J., & Penny, W. (2011). Post hoc Bayesian model selection. Neuroimage, 56(4), 2089–2099. https://doi.org/10.1016/j.neuroimage.2011.03.062 Frith, C. D., Wolpert, D. M., & Blair, R. J. R. (2003). Facial expressions, their communicatory functions and neuro-cognitive substrates. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences, 358(1431), 561–572. https://doi.org/10.1098/rstb.2002.1220 Gu, H., Salmeron, B. J., Ross, T. J., Geng, X., Zhan, W., Stein, E. A., et al. (2010). Mesocorticolimbic circuits are impaired in chronic cocaine users as demonstrated by resting-state functional connectivity. Neuroimage, 53(2), 593–601. https://doi.org/10.1016/j.neuroimage.2010.06.066 Haut, K. M., Dodell-Feder, D., Guty, E., Nahum, M., & Hooker, C. I. (2019). Change in Objective Measure of Empathic Accuracy Following Social Cognitive Training. Frontiers in Psychiatry, 10, 89410.3389/Fpsyt.2019.00894. Homer, B. D., Solomon, T. M., Moeller, R. W., Mascia, A., DeRaleau, L., & Halkitis, P. N. (2008). Methamphetamine abuse and impairment of social functioning: A review of the underlying neurophysiological causes and Behavioral implications. Psychological Bulletin, 134(2), 301–310. https://doi.org/10.1037/0033-2909.134.2.301 Hu, Y., Salmeron, B. J., Gu, H., Stein, E. A., & Yang, Y. (2015). Impaired functional connectivity within and between frontostriatal circuits and its association with compulsive drug use and trait impulsivity in cocaine addiction. JAMA Psychiatry, 72(6), 584–592. Hulka, L. M., Preller, K. H., Vonmoos, M., Broicher, S. D., & Quednow, B. B. (2013). Cocaine users manifest impaired prosodic and cross-modal emotion processing. Frontiers in Psychiatry, 4, 98. https://doi.org/10.3389/fpsyt.2013.00098 Jackson, M. E., & Moghaddam, B. (2001). Amygdala regulation of nucleus accumbens dopamine output is governed by the prefrontal cortex. Journal of Neuroscience, 21(2), 676–681. https://doi.org/10.1523/Jneurosci.21-02-00676.2001 Jasinska, A. J., Stein, E. A., Kaiser, J., Naumer, M. J., & Yalachkov, Y. (2014). Factors modulating neural reactivity to drug cues in addiction: a survey of human neuroimaging studies. Neuroscience & Biobehavioral Reviews, 38, 1–16. https://doi.org/10.1016/j.neubiorev.2013.10.013 Ji, G. J., Liao, W., Chen, F. F., Zhang, L., & Wang, K. (2017). Low-frequency blood oxygen level-dependent fluctuations in the brain white matter: more than just noise. Science Bulletin, 62(9), 656–657. https://doi.org/10.1016/j.scib.2017.03.021 Karila, L., Gorelick, D., Weinstein, A., Noble, F., Benyamina, A., Coscas, S., et al. (2008). New treatments for cocaine dependence: a focused review. The International Journal of Neuropsychopharmacology, 11(3), 425–438. https://doi.org/10.1017/S1461145707008097 Kelly, C., Zuo, X. N., Gotimer, K., Cox, C. L., Lynch, L., Brock, D., et al. (2011). Reduced interhemispheric resting state functional connectivity in cocaine addiction. Biological Psychiatry, 69(7), 684–692. https://doi.org/10.1016/j.biopsych.2010.11.022 Kemmis, L., Hall, J. K., Kingston, R., & Morgan, M. J. (2007). Impaired fear recognition in regular recreational cocaine users. Psychopharmacology (Berl), 194(2), 151–159. https://doi.org/10.1007/s00213-007-0829-5 Konova, A. B., Moeller, S. J., Tomasi, D., Volkow, N. D., & Goldstein, R. Z. (2013). Effects of methylphenidate on resting-state functional connectivity of the mesocorticolimbic dopamine pathways in cocaine addiction. JAMA Psychiatry, 70(8), 857–868. https://doi.org/10.1001/jamapsychiatry.2013.1129 Koob, G., & Bloom, F. (1988). Cellular and molecular mechanisms of drug dependence. Science, 242(4879), 715–723. https://doi.org/10.1126/science.2903550 Koob, G. F., & Volkow, N. D. (2010). Neurocircuitry of addiction. Neuropsychopharmacology: official publication of the American College of Neuropsychopharmacology, 35(1), 217–238. https://doi.org/10.1038/npp.2009.110 Koob, G. F., & Volkow, N. D. (2016). Neurobiology of addiction: a neurocircuitry analysis. Lancet Psychiatry, 3(8), 760–773. Kral, T. R. A., Stodola, D. E., Birn, R. M., Mumford, J. A., Solis, E., Flook, L., et al. (2018). Neural correlates of video game empathy training in adolescents: a randomized trial. NPJ Science of Learning, 3, 13. https://doi.org/10.1038/s41539-018-0029-6 Lee, H. J., Wheeler, D. S., & Holland, P. C. (2011). Interactions between amygdala central nucleus and the ventral tegmental area in the acquisition of conditioned cue-directed behavior in rats. European Journal of Neuroscience, 33(10), 1876–1884. https://doi.org/10.1111/j.1460-9568.2011.07680.x Makris, N., Gasic, G. P., Seidman, L. J., Goldstein, J. M., Gastfriend, D. R., Elman, I., et al. (2004). Decreased absolute amygdala volume in cocaine addicts. Neuron, 44(4), 729–740, doi:DOI. https://doi.org/10.1016/j.neuron.2004.10.027 Martinez, D., Carpenter, K. M., Liu, F., Slifstein, M., Broft, A., Friedman, A. C., et al. (2011). Imaging dopamine transmission in cocaine dependence: Link between neurochemistry and response to treatment. American Journal of Psychiatry, 168(6), 634–641. https://doi.org/10.1176/appi.ajp.2010.10050748 Marussich, L., Lu, K. H., Wen, H. G., & Liu, Z. M. (2017). Mapping white-matter functional organization at rest and during naturalistic visual perception. Neuroimage, 146, 1128–1141. https://doi.org/10.1016/j.neuroimage.2016.10.005 Maurage, P., Grynberg, D., Noel, X., Joassin, F., Philippot, P., Hanak, C., et al. (2011). Dissociation between affective and cognitive empathy in alcoholism: A specific deficit for the emotional dimension. Alcoholism-Clinical and Experimental Research, 35(9), 1662–1668. https://doi.org/10.1111/j.1530-0277.2011.01512.x Moeller, S. J., & Paulus, M. P. (2018). Toward biomarkers of the addicted human brain: Using neuroimaging to predict relapse and sustained abstinence in substance use disorder. Progress in Neuro-Psychopharmacology & Biological Psychiatry, 80, 143–154. https://doi.org/10.1016/j.pnpbp.2017.03.003 Morgan, M. J., & Marshall, J. P. (2013). Deficient fear recognition in regular cocaine users is not attributable to elevated impulsivity or conduct disorder prior to cocaine use. Journal of Psychopharmacology, 27(6), 526–532. https://doi.org/10.1177/0269881113477708 Mutschler, J., Eifler, S., Dirican, G., Grosshans, M., Kiefer, F., Rossler, W., et al. (2013). Functional social support within a medical supervised outpatient treatment program. American Journal of Drug and Alcohol Abuse, 39(1), 44–49. https://doi.org/10.3109/00952990.2012.677889 Nazari-Serenjeh, F., & Rezayof, A. (2013). Cooperative interaction between the basolateral amygdala and ventral tegmental area modulates the consolidation of inhibitory avoidance memory. Progress in Neuro-Psychopharmacology & Biological Psychiatry, 40, 54–61. https://doi.org/10.1016/j.pnpbp.2012.10.003 Nomura, K., & Akai, S. (2012). Empathy with fictional stories: Reconsideration of the fantasy scale of the interpersonal reactivity index. Psychological Reports, 110(1), 304–314. https://doi.org/10.2466/02.07.09.11.PR0.110.1.304-314 Nooner, K. B., Colcombe, S. J., Tobe, R. H., Mennes, M., Benedict, M. M., Moreno, A. L., et al. (2012). The NKI-Rockland sample: a model for accelerating the pace of discovery science in psychiatry. Frontiers in Neuroscience, 6, 15210.3389/fnins.2012.00152. O’Brien, C. P. (2005). Anticraving medications for relapse prevention: a possible new class of psychoactive medications. The American Journal of Psychiatry, 162(8), 1423–1431. https://doi.org/10.1176/appi.ajp.162.8.1423 Ostlund, S. B., & Halbout, B. (2017). Mesolimbic Dopamine Signaling in Cocaine Addiction. In V. R. Preedy (Ed.), The Neuroscience of Cocaine (pp. 287–295). San Diego: Academic. Parkes, L., Tiego, J., Aquino, K., Braganza, L., Chamberlain, S. R., Fontenelle, L. F., et al. (2019). Transdiagnostic variations in impulsivity and compulsivity in obsessive-compulsive disorder and gambling disorder correlate with effective connectivity in cortical-striatal-thalamic-cortical circuits. Neuroimage. 202,. https://doi.org/10.1016/j.neuroimage.2019.116070 Parkinson, C., & Wheatley, T. (2014). Relating anatomical and social connectivity: White Matter microstructure predicts emotional empathy. Cerebral Cortex, 24(3), 614–625. https://doi.org/10.1093/cercor/bhs347 Patel, A. X., Kundu, P., Rubinov, M., Jones, P. S., Vertes, P. E., Ersche, K. D., et al. (2014). A wavelet method for modeling and despiking motion artifacts from resting-state fMRI time series. Neuroimage, 95, 287–304. https://doi.org/10.1016/j.neuroimage.2014.03.012 Phillips, A. G., Ahn, S., & Howland, J. G. (2003). Amygdalar control of the mesocorticolimbic dopamine system: parallel pathways to motivated behavior. Neuroscience and Biobehavioral Reviews, 27(6), 543–554. https://doi.org/10.1016/j.neubiorev.2003.09.002 Preller, K. H., Herdener, M., Schilbach, L., Stampfli, P., Hulka, L. M., Vonmoos, M., et al. (2014b). Functional changes of the reward system underlie blunted response to social gaze in cocaine users. Proceedings of the National Academy of Sciences of the United States of America, 111(7), 2842–2847. https://doi.org/10.1073/pnas.1317090111 Preller, K. H., Hulka, L. M., Vonmoos, M., Jenni, D., Baumgartner, M. R., Seifritz, E., et al. (2014a). Impaired emotional empathy and related social network deficits in cocaine users. Addiction Biology, 19(3), 452–466. https://doi.org/10.1111/adb.12070 Pulos, S., Elison, J., & Lennon, R. (2004). The hierarchical structure of the interpersonal reactivity index. Social Behavior and Personality, 32(4), 355–359. https://doi.org/10.2224/sbp.2004.32.4.355 Quednow, B. B. (2017). Social cognition and interaction in stimulant use disorders. Current Opinion in Behavioral Sciences, 13, 55–62. https://doi.org/10.1016/j.cobeha.2016.10.001 Rando, K., Tuit, K., Hannestad, J., Guarnaccia, J., & Sinha, R. (2013). Sex differences in decreased limbic and cortical grey matter volume in cocaine dependence: a voxel-based morphometric study. Addiction Biology, 18(1), 147–160. https://doi.org/10.1111/adb.12008 Ray, S., Di, X., & Biswal, B. B. (2016). Effective connectivity within the mesocorticolimbic system during resting-state in cocaine users. Frontiers in Human Neuroscience, 10, 563. https://doi.org/10.3389/fnhum.2016.00563 Razi, A., Kahan, J., Rees, G., & Friston, K. J. (2015). Construct validation of a DCM for resting state fMRI. Neuroimage, 106, 1–14. https://doi.org/10.1016/j.neuroimage.2014.11.027 Snoek, L., Miletic, S., & Scholte, H. S. (2019). How to control for confounds in decoding analyses of neuroimaging data. Perception, 48, 204–204. Takeuchi, H., Taki, Y., Thyreau, B., Sassa, Y., Hashizume, H., Sekiguchi, A., et al. (2013). White matter structures associated with empathizing and systemizing in young adults. Neuroimage, 77, 222–236. https://doi.org/10.1016/j.neuroimage.2013.04.004 Tomei, A., Besson, J., Reber, N., Rougemont-Bucking, A., & Grivel, J. (2017). Personal distress and empathic concern in methadone-maintained patients. Journal of Substance Use, 22(1), 37–41. https://doi.org/10.3109/14659891.2016.1140238 Tsvetanov, K. A., Henson, R. N. A., Tyler, L. K., Razi, A., Geerligs, L., Ham, T. E., et al. (2016). Extrinsic and intrinsic brain network connectivity maintains cognition across the lifespan despite accelerated decay of regional brain activation. Journal of Neuroscience, 36(11), 3115–3126. https://doi.org/10.1523/Jneurosci.2733-15.2016 van Huijstee, A. N., & Mansvelder, H. D. (2014). Glutamatergic synaptic plasticity in the mesocorticolimbic system in addiction. Frontiers in Cellular Neuroscience, 8, 466. https://doi.org/10.3389/fncel.2014.00466 Verdejo-Garcia, A. (2014). Social cognition in cocaine addiction. Proceedings of the National Academy of Sciences of the United States of America, 111(7), 2406–2407. https://doi.org/10.1073/pnas.1324287111 Volkow, N. D., Baler, R. D., & Goldstein, R. Z. (2011a). Addiction: Pulling at the Neural Threads of Social Behaviors. Neuron, 69(4), 599–602. https://doi.org/10.1016/j.neuron.2011.01.027 Volkow, N. D., Wang, G. J., Fowler, J. S., Tomasi, D., & Telang, F. (2011b). Addiction: beyond dopamine reward circuitry. Proceedings of the National Academy of Sciences of the United States of America, 108(37), 15037–15042. https://doi.org/10.1073/pnas.1010654108 Volkow, N. D., Fowler, J. S., & Wang, G. J. (2003). The addicted human brain: insights from imaging studies. Journal of Clinical Investigation, 111(10), 1444–1451. https://doi.org/10.1172/JCI18533 Volkow, N. D., Fowler, J. S., & Wang, G. J. (2004). The addicted human brain viewed in the light of imaging studies: brain circuits and treatment strategies. Neuropharmacology, 47(Suppl 1), 3–13. https://doi.org/10.1016/j.neuropharm.2004.07.019 Volkow, N. D., Fowler, J. S., Wang, G. J., Hitzemann, R., Logan, J., Schlyer, D. J., et al. (1993). Decreased dopamine D2 receptor availability is associated with reduced frontal metabolism in cocaine abusers. Synapse (New York, N. Y.), 14(2), 169–177. https://doi.org/10.1002/syn.890140210 Volkow, N. D., & Morales, M. (2015). The brain on drugs: From reward to addiction. Cell, 162(4), 712–725. https://doi.org/10.1016/j.cell.2015.07.046 Volkow, N. D., Wang, G. J., Fowler, J. S., & Tomasi, D. (2012). Addiction circuitry in the human brain. The Annual Review of Pharmacology and Toxicology, 52, 321–336. https://doi.org/10.1146/annurev-pharmtox-010611-134625 Vonmoos, M., Hulka, L. M., Preller, K. H., Minder, F., Baumgartner, M. R., & Quednow, B. B. (2014). Cognitive impairment in cocaine users is drug-induced but partially reversible: Evidence from a longitudinal study. Neuropsychopharmacology: official publication of the American College of Neuropsychopharmacology, 39(9), 2200–2210. https://doi.org/10.1038/npp.2014.71 Wiers, C. E., Cabrera, E., Skarda, E., Volkow, N. D., & Wang, G. J. (2016). PET imaging for addiction medicine: From neural mechanisms to clinical considerations. Progress in Brain Research, 224, 175–201. https://doi.org/10.1016/bs.pbr.2015.07.016 Wilcox, C. E., Teshiba, T. M., Merideth, F., Ling, J., & Mayer, A. R. (2011). Enhanced cue reactivity and fronto-striatal functional connectivity in cocaine use disorders. Drug and Alcohol Dependence, 115(1–2), 137–144. https://doi.org/10.1016/j.drugalcdep.2011.01.009