Chronic non-medical prescription opioid use and empathy for pain: Does pain make the difference?
Corresponding Author
Sara L. Kroll
Experimental and Clinical Pharmacopsychology, Department of Psychiatry, Psychotherapy, and Psychosomatics, Psychiatric Hospital, University of Zurich, Zurich, Switzerland
Center for Social and Affective Neuroscience, Department of Biomedical and Clinical Sciences, Linköping University, Linköping, Sweden
Correspondence
Sara L. Kroll, Experimental and Clinical Pharmacopsychology, Department of Psychiatry, Psychotherapy and Psychosomatics, Psychiatric Hospital, University of Zurich, Lenggstrasse 31, PO Box 1931, Zurich 8008, Switzerland.
Email: [email protected], [email protected]
Contribution: Conceptualization, Data curation, Formal analysis, Investigation, Methodology, Project administration, Visualization, Writing - original draft, Writing - review & editing
Search for more papers by this authorJulian F. Thayer
Department of Psychological Science, University of California, Irvine, CA, USA
Contribution: Data curation, Formal analysis, Methodology, Software, Supervision, Validation, Writing - review & editing
Search for more papers by this authorDeWayne P. Williams
Department of Psychological Science, University of California, Irvine, CA, USA
Contribution: Data curation, Formal analysis, Methodology, Software, Supervision, Validation, Writing - review & editing
Search for more papers by this authorDaniela M. Pfabigan
Institute of Basic Medical Sciences, Faculty of Medicine, University of Oslo, Oslo, Norway
Contribution: Data curation, Formal analysis, Methodology, Software, Supervision, Validation, Writing - review & editing
Search for more papers by this authorMarkus R. Baumgartner
Center for Forensic Hair Analysis, Institute of Forensic Medicine, University of Zurich, Zurich, Switzerland
Contribution: Data curation, Formal analysis, Resources
Search for more papers by this authorClaus Lamm
Social, Cognitive and Affective Neuroscience Unit, Department of Cognition, Emotion, and Methods in Psychology, Faculty of Psychology, University of Vienna, Vienna, Austria
Contribution: Resources, Supervision, Validation, Writing - original draft
Search for more papers by this authorBoris B. Quednow
Experimental and Clinical Pharmacopsychology, Department of Psychiatry, Psychotherapy, and Psychosomatics, Psychiatric Hospital, University of Zurich, Zurich, Switzerland
Neuroscience Center Zurich, University of Zurich and Swiss Federal Institute of Technology Zurich, Zurich, Switzerland
Contribution: Conceptualization, Formal analysis, Funding acquisition, Methodology, Project administration, Resources, Software, Supervision, Validation, Visualization, Writing - original draft, Writing - review & editing
Search for more papers by this authorCorresponding Author
Sara L. Kroll
Experimental and Clinical Pharmacopsychology, Department of Psychiatry, Psychotherapy, and Psychosomatics, Psychiatric Hospital, University of Zurich, Zurich, Switzerland
Center for Social and Affective Neuroscience, Department of Biomedical and Clinical Sciences, Linköping University, Linköping, Sweden
Correspondence
Sara L. Kroll, Experimental and Clinical Pharmacopsychology, Department of Psychiatry, Psychotherapy and Psychosomatics, Psychiatric Hospital, University of Zurich, Lenggstrasse 31, PO Box 1931, Zurich 8008, Switzerland.
Email: [email protected], [email protected]
Contribution: Conceptualization, Data curation, Formal analysis, Investigation, Methodology, Project administration, Visualization, Writing - original draft, Writing - review & editing
Search for more papers by this authorJulian F. Thayer
Department of Psychological Science, University of California, Irvine, CA, USA
Contribution: Data curation, Formal analysis, Methodology, Software, Supervision, Validation, Writing - review & editing
Search for more papers by this authorDeWayne P. Williams
Department of Psychological Science, University of California, Irvine, CA, USA
Contribution: Data curation, Formal analysis, Methodology, Software, Supervision, Validation, Writing - review & editing
Search for more papers by this authorDaniela M. Pfabigan
Institute of Basic Medical Sciences, Faculty of Medicine, University of Oslo, Oslo, Norway
Contribution: Data curation, Formal analysis, Methodology, Software, Supervision, Validation, Writing - review & editing
Search for more papers by this authorMarkus R. Baumgartner
Center for Forensic Hair Analysis, Institute of Forensic Medicine, University of Zurich, Zurich, Switzerland
Contribution: Data curation, Formal analysis, Resources
Search for more papers by this authorClaus Lamm
Social, Cognitive and Affective Neuroscience Unit, Department of Cognition, Emotion, and Methods in Psychology, Faculty of Psychology, University of Vienna, Vienna, Austria
Contribution: Resources, Supervision, Validation, Writing - original draft
Search for more papers by this authorBoris B. Quednow
Experimental and Clinical Pharmacopsychology, Department of Psychiatry, Psychotherapy, and Psychosomatics, Psychiatric Hospital, University of Zurich, Zurich, Switzerland
Neuroscience Center Zurich, University of Zurich and Swiss Federal Institute of Technology Zurich, Zurich, Switzerland
Contribution: Conceptualization, Formal analysis, Funding acquisition, Methodology, Project administration, Resources, Software, Supervision, Validation, Visualization, Writing - original draft, Writing - review & editing
Search for more papers by this authorFunding information
This work was supported by the Theodor and Ida Herzog-Egli Foundation and starting grants of the Medical Faculty of the University of Zurich and of the Psychiatric Hospital of the University of Zurich to BBQ. SLK was financed by a grant of the Swiss National Science Foundation (105319_162639/1) to BBQ
Abstract
Non-medical prescription opioid use (NMPOU) is at the heart of the opioid epidemic in the United States. Although chronic opioid use is commonly accompanied by deficits in social functioning, little is known about the impact of chronic NMPOU on social cognitive functions. Social neuroscience models suggest that empathy activates similar or even equivalent neural structures as those underpinning the first-hand experience in that emotional state (e.g., pain). Therefore, we measured subjective and psychophysiological responses during an empathy-for-pain task in 23 individuals with NMPOU, objectively confirmed by hair and urine testing, and compared them with 29 opioid-naïve healthy controls. NMPOU individuals showed lower other-related and self-related unpleasantness ratings when seeing others in pain than controls. No differences between the control and NMPOU group were found in skin conductance responses and heart rate variability (HRV) assessed by root mean square of successive differences (RMSSD) in response to the task. However, RMSSD-HRV was strongly negatively correlated with self-related unpleasantness and craving in the NMPOU group. A subsequent mediation analysis showed a total effect of RMSSD-HRV on self-related unpleasantness with no mediation of craving. This indicates that stronger emotion regulation indexed by high RMSSD-HRV might have downregulating effects on sharing others’ pain in NMPOU individuals but not in healthy controls, which was further accompanied by decreased ratings of personal distress and empathetic concern. These results contribute to a better understanding of social functioning in chronic opioid users, suggesting adequate emotion regulation and empathy trainings as therapeutic targets for future interventions of opioid use disorders and long-term pain treatment with opioids.
CONFLICT OF INTEREST
The authors have no conflict of interest to declare.
Supporting Information
| Filename | Description |
|---|---|
| psyp13776-sup-0001-Supinfo.docxWord document, 59.6 KB |
Supplementary Material Table S1 Motives of opioid use Table S2 Frequency table of opioid use Table S3 Independent t-tests of the questionnaires (means and standard deviations) Table S4 Correlation analyses of drug use variables within the NMPOU group Figure S1 Mediation analysis Figure S2 Validation check for cognitive and affective empathy for pain |
Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.
REFERENCES
- Batson, C. D., Early, S., & Salvarini, G. (1997). Perspective taking: Imagining how another feels versus imagining how you would feel. Personality and Social Psychology Bulletin, 23, 751–758.
- Baumgärtner, U., Buchholz, H.-G., Bellosevich, A., Magerl, W., Siessmeier, T., Rolke, R., Höhnemann, S., Piel, M., Rösch, F., Wester, H.-J., Henriksen, G., Stoeter, P., Bartenstein, P., Treede, R.-D., & Schreckenberger, M. (2006). High opiate receptor binding potential in the human lateral pain system. NeuroImage, 30(3), 692–699. https://doi.org/10.1016/j.neuroimage.2005.10.033
- Beck, A. T., Ward, C. H., Mendelson, M., Mock, J., & Erbaugh, J. (1961). An inventory for measuring depression. Archives of General Psychiatry, 4, 561–571. https://doi.org/10.1001/archpsyc.1961.01710120031004
- Benedek, M., & Kaernbach, C. (2010). A continuous measure of phasic electrodermal activity. Journal of Neuroscience Methods, 190(1), 80–91. https://doi.org/10.1016/j.jneumeth.2010.04.028
- Benjamini, Y., & Hochberg, Y. (1995). Controlling the false discovery rate: A practical and powerful approach to multiple testing. Journal of the Royal Statistical Society, 57(1), 289–300.
10.1111/j.2517-6161.1995.tb02031.x Google Scholar
- Bernhardt, B. C., & Singer, T. (2012). The neural basis of empathy. Annual Review of Neuroscience, 35, 1–23. https://doi.org/10.1146/annurev-neuro-062111-150536
- Byrd, D. A., Robinson-Papp, J., Mindt, M. R., Mintz, L., Elliott, K., Lighty, Q., & Manhattan, H. I. V. B. B. (2013). Isolating cognitive and neurologic HIV effects in substance-dependent, confounded cohorts: A pilot study. Journal of the International Neuropsychological Society, 19(4), 463–473. https://doi.org/10.1017/S1355617712001634
- Carlyle, M., Rowley, M., Stevens, T., Karl, A., & Morgan, C. J. A. (2020). Impaired empathy and increased anger following social exclusion in non-intoxicated opioid users. Psychopharmacology, 237(2), 419–430. https://doi.org/10.1007/s00213-019-05378-x
- Cohen, J. (1988). Statistical power analysis for the bevavioral sciences (Hillsdale Ed, 2nd ed.) Lawrence Erlbaum Associates.
- Cooper, G. A. A., Kronstrand, R., & Kintz, P. & Society of Hair Testing. (2012). Society of Hair Testing guidelines for drug testing in hair. Forensic Science International, 218(1–3), 20–24. https://doi.org/10.1016/j.forsciint.2011.10.024
- Craig, E. D. (1968). Physiological arousal as a function of imagined, vicarious, and direct stress experiences. Journal of Abnormal Psychology, 73(6), 513–520. https://doi.org/10.1037/h0026531
- Darke, S. (2011). The life of the heroin user, typical beginnings, trajectories and outcomes. Cambridge University Press.
10.1017/CBO9780511732249 Google Scholar
- 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., & Jackson, P. L. (2004). The functional architecture of human empathy. Behavioral and Cognitive Neuroscience Reviews, 3(2), 71–100. https://doi.org/10.1177/1534582304267187
- Decety, J., & Sommerville, J. A. (2003). Shared representations between self and other: A social cognitive neuroscience view. Trends in Cognitive Sciences, 7(12), 527–533. https://doi.org/10.1016/j.tics.2003.10.004
- Dziobek, I., Preissler, S., Grozdanovic, Z., Heuser, I., Heekeren, H. R., & Roepke, S. (2011). Neuronal correlates of altered empathy and social cognition in borderline personality disorder. NeuroImage, 57(2), 539–548. https://doi.org/10.1016/j.neuroimage.2011.05.005
- Dziobek, I., Rogers, K., Fleck, S., Bahnemann, M., Heekeren, H. R., Wolf, O. T., & Convit, A. (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
- Fareed, A., Kim, J., Ketchen, B., Kwak, W. J., Wang, D., Shongo-Hiango, H., & Drexler, K. (2017). Effect of heroin use on changes of brain functions as measured by functional magnetic resonance imaging, a systematic review. Journal of Addictive Diseases, 36(2), 105–116. https://doi.org/10.1080/10550887.2017.1280898
- Faul, F., Erdfelder, E., Buchner, A., & Lang, A. G. (2009). Statistical power analyses using G*Power 3.1: Tests for correlation and regression analyses. Behavior Research Methods, 41(4), 1149–1160. https://doi.org/10.3758/BRM.41.4.1149
- Fields, H. L. (2011). Mu opioid receptor mediated analgesia and reward. In G. W. Pasternak (Ed.), The opiate receptors, (Vol. 23, 2nd ed. pp. 239–264). Humana Press.
10.1007/978-1-60761-993-2_10 Google Scholar
- Garland, E. L. (2016). Restructuring reward processing with Mindfulness-Oriented Recovery Enhancement: Novel therapeutic mechanisms to remediate hedonic dysregulation in addiction, stress, and pain. Annals of the New York Academy of Sciences, 1373(1), 25–37. https://doi.org/10.1111/nyas.13034
- Garland, E. L., Hanley, A. W., Kline, A., & Cooperman, N. A. (2019). Mindfulness-Oriented Recovery Enhancement reduces opioid craving among individuals with opioid use disorder and chronic pain in medication assisted treatment: Ecological momentary assessments from a stage 1 randomized controlled trial. Drug and Alcohol Dependence, 203, 61–65. https://doi.org/10.1016/j.drugalcdep.2019.07.007
- Greenberg, D. M., Warrier, V., Allison, C., & Baron-Cohen, S. (2018). Testing the Empathizing-Systemizing theory of sex differences and the Extreme Male Brain theory of autism in half a million people. Proceedings of the National Academy of Sciences of the United States of America, 115(48), 12152–12157. https://doi.org/10.1073/pnas.1811032115
- Handelsman, L., Cochrane, K. J., Aronson, M. J., Ness, R., Rubinstein, K. J., & Kanof, P. D. (1987). Two new rating scales for opiate withdrawal. The American Journal of Drug and Alcohol Abuse, 13(3), 293–308. https://doi.org/10.3109/00952998709001515
- Hayes, A. F. (2018). Introduction to mediation, moderation, and conditional process analysis: A regression-based approach ( 2nd ed.). The Guilford Press.
- Heatherton, T. F., Kozlowski, L. T., Frecker, R. C., & Fagerstrom, K. O. (1991). The Fagerstrom test for nicotine dependence: A revision of the Fagerstrom Tolerance Questionnaire. British Journal of Addiction, 86(9), 1119–1127. https://doi.org/10.1111/j.1360-0443.1991.tb01879.x
- Heilig, M., Epstein, D. H., Nader, M. A., & Shaham, Y. (2016). Time to connect: Bringing social context into addiction neuroscience. Nature Reviews Neuroscience, 17(9), 592–599. https://doi.org/10.1038/nrn.2016.67
- Hein, G., Lamm, C., Brodbeck, C., & Singer, T. (2011). Skin conductance response to the pain of others predicts later costly helping. PLoS One, 6(8), e22759. https://doi.org/10.1371/journal.pone.0022759
- Hygge, S., & Hugdahl, K. (1985). Skin conductance recordings and the NaCl concentration of the electrolyte. Psychophysiology, 22(3), 365–367. https://doi.org/10.1111/j.1469-8986.1985.tb01616.x
- Ingjaldsson, J. T., Thayer, J. F., & Laberg, J. C. (2003). Craving for alcohol and pre-attentive processing of alcohol stimuli. International Journal of Psychophysiology, 49(1), 29–39. https://doi.org/10.1016/s0167-8760(03)00075-8
- Karjalainen, T., Karlsson, H. K., Lahnakoski, J. M., Glerean, E., Nuutila, P., Jaaskelainen, I. P., Hari, R., Sams, M., & Nummenmaa, L. (2017). Dissociable roles of cerebral mu-opioid and type 2 dopamine receptors in vicarious pain: A combined PET-fMRI study. Cerebral Cortex, 27(8), 4257–4266. https://doi.org/10.1093/cercor/bhx129
- Kennedy, D., Goshko, C. B., Murch, W. S., Limbrick-Oldfield, E. H., Dunn, B. D., & Clark, L. (2019). Interoception and respiratory sinus arrhythmia in gambling disorder. Psychophysiology, 56(6), e13333. https://doi.org/10.1111/psyp.13333
- Kleiger, R. E., Stein, P. K., & Bigger, J. T. Jr (2005). Heart rate variability: Measurement and clinical utility. Annals of Noninvasive Electrocardiology, 10(1), 88–101. https://doi.org/10.1111/j.1542-474X.2005.10101.x
- Koenig, J., Jarczok, M. N., Warth, M., Ellis, R. J., Bach, C., Hillecke, T. K., & Thayer, J. F. (2014). Body mass index is related to autonomic nervous system activity as measured by heart rate variability–a replication using short term measurements. The Journal of Nutrition, Health & Aging, 18(3), 300–302. https://doi.org/10.1007/s12603-014-0022-6
- Kogan, A., Oveis, C., Carr, E. W., Gruber, J., Mauss, I. B., Shallcross, A., Impett, E. A., van der Lowe, I., Hui, B., Cheng, C., & Keltner, D. (2014). Vagal activity is quadratically related to prosocial traits, prosocial emotions, and observer perceptions of prosociality. Journal of Personality and Social Psychology, 107(6), 1051–1063. https://doi.org/10.1037/a0037509
- Kroll, S. L., Nikolic, E., Bieri, F., Soyka, M., Baumgartner, M. R., & Quednow, B. B. (2018). Cognitive and socio-cognitive functioning of chronic non-medical prescription opioid users. Psychopharmacology, 235(12), 3451–3464. https://doi.org/10.1007/s00213-018-5060-z
- Kroll, S. L., Williams, D. W. P., Thoma, M., Staib, M., Binz, T. M., Baumgartner, M. R., Kirschbaum, C., Thayer, J. F., & Quednow, B. B. (2019). Non-medical prescription opioid users exhibit dysfunctional physiological stress responses to social rejection. Psychoneuroendocrinology, 100, 264–275. https://doi.org/10.1016/j.psyneuen.2018.09.023
- Kroll, S. L., Wunderli, M. D., Vonmoos, M., Hulka, L. M., Preller, K. H., Bosch, O. G., Baumgartner, M. R., & Quednow, B. B. (2018). Socio-cognitive functioning in stimulant polysubstance users. Drug and Alcohol Dependence, 190, 94–103. https://doi.org/10.1016/j.drugalcdep.2018.06.001
- Laborde, S., Mosley, E., & Thayer, J. F. (2017). Heart rate variability and cardiac vagal tone in psychophysiological research—Recommendations for experiment planning, data analysis, and data reporting. Frontiers in Psychology, 8, 213. https://doi.org/10.3389/fpsyg.2017.00213
- Lamm, C., Batson, C. D., & Decety, J. (2007). The neural substrate of human empathy: Effects of perspective-taking and cognitive appraisal. Journal of Cognitive Neuroscience, 19(1), 42–58. https://doi.org/10.1162/jocn.2007.19.1.42
- Lamm, C., Decety, J., & Singer, T. (2011). Meta-analytic evidence for common and distinct neural networks associated with directly experienced pain and empathy for pain. NeuroImage, 54(3), 2492–2502. https://doi.org/10.1016/j.neuroimage.2010.10.014
- Lamm, C., & Majdandzic, J. (2015). The role of shared neural activations, mirror neurons, and morality in empathy—A critical comment. Neuroscience Research, 90, 15–24. https://doi.org/10.1016/j.neures.2014.10.008
- Lamm, C., Porges, E. C., Cacioppo, J. T., & Decety, J. (2008). Perspective taking is associated with specific facial responses during empathy for pain. Brain Research, 1227, 153–161. https://doi.org/10.1016/j.brainres.2008.06.066
- Lamm, C., Rütgen, M., & Wagner, I. C. (2019). Imaging empathy and prosocial emotions. Neuroscience Letters, 693, 49–53. https://doi.org/10.1016/j.neulet.2017.06.054
- Lehrl, S. (1999). Mehrfachwahl-Wortschatz-Intelligenztest (MWT-B) ( 4th ed.) Hogrefe.
- Lischke, A., Pahnke, R., Mau-Moeller, A., Behrens, M., Grabe, H. J., Freyberger, H. J., Hamm, A. O., & Weippert, M. (2018). Inter-individual differences in heart rate variability are associated with inter-individual differences in empathy and alexithymia. Frontiers in Psychology, 9, 229. https://doi.org/10.3389/fpsyg.2018.00229
- Lutz, P. E., & Kieffer, B. L. (2013). The multiple facets of opioid receptor function: Implications for addiction. Current Opinion in Neurobiology, 23(4), 473–479. https://doi.org/10.1016/j.conb.2013.02.005
- Mintzer, M. Z., & Johnson, M. W. (2007). Opioids. In A. Kalechstein, & W. G. Gorp (Eds.), Neuropsychology and substance use. Taylor & Francis.
- NCHS. (2017). Wide-ranging online data for epidemiologic research (WONDER). https://wonder.cdc.gov/
- Park, G., & Thayer, J. F. (2014). From the heart to the mind: Cardiac vagal tone modulates top-down and bottom-up visual perception and attention to emotional stimuli. Frontiers in Psychology, 5, 278. https://doi.org/10.3389/fpsyg.2014.00278
- Petrovic, P., Kalso, E., Petersson, K. M., & Ingvar, M. (2002). Placebo and opioid analgesia—Imaging a shared neuronal network. Science, 295(5560), 1737–1740. https://doi.org/10.1126/science.1067176
- Pfabigan, D. M., Seidel, E. M., Wucherer, A. M., Keckeis, K., Derntl, B., & Lamm, C. (2015). Affective empathy differs in male violent offenders with high- and low-trait psychopathy. Journal of Personality Disorders, 29(1), 42–61. https://doi.org/10.1521/pedi_2014_28_145
- Preller, K. H., Hulka, L. M., Vonmoos, M., Jenni, D., Baumgartner, M. R., Seifritz, E., Dziobek, I., & Quednow, B. B. (2014). Impaired emotional empathy and related social network deficits in cocaine users. Addiction Biology, 19(3), 452–466. https://doi.org/10.1111/adb.12070
- 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
- Quednow, B. B. (2020). Social cognition in addiction. In A. Verdejo-Garcia (Ed.), Cognition and addiction: A researcher's guide from mechanisms towards interventions (pp. 63–78). Academic Press.
10.1016/B978-0-12-815298-0.00005-8 Google Scholar
- Quednow, B. B., Kuhn, K. U., Hoenig, K., Maier, W., & Wagner, M. (2004). Prepulse inhibition and habituation of acoustic startle response in male MDMA (‘ecstasy’) users, cannabis users, and healthy controls. Neuropsychopharmacology, 29(5), 982–990. https://doi.org/10.1038/sj.npp.1300396
- Quintana, D. S., Guastella, A. J., McGregor, I. S., Hickie, I. B., & Kemp, A. H. (2013). Heart rate variability predicts alcohol craving in alcohol dependent outpatients: Further evidence for HRV as a psychophysiological marker of self-regulation. Drug and Alcohol Dependence, 132(1–2), 395–398. https://doi.org/10.1016/j.drugalcdep.2013.02.025
- Rütgen, M., Pletti, C., Tik, M., Kraus, C., Pfabigan, D. M., Sladky, R., Klöbl, M., Woletz, M., Vanicek, T., Windischberger, C., Lanzenberger, R., & Lamm, C. (2019). Antidepressant treatment, not depression, leads to reductions in behavioral and neural responses to pain empathy. Translational Psychiatry, 9(1), 164. https://doi.org/10.1038/s41398-019-0496-4
- Rütgen, M., Seidel, E. M., Pletti, C., Riecansky, I., Gartus, A., Eisenegger, C., & Lamm, C. (2018). Psychopharmacological modulation of event-related potentials suggests that first-hand pain and empathy for pain rely on similar opioidergic processes. Neuropsychologia, 116(Pt A), 5–14. https://doi.org/10.1016/j.neuropsychologia.2017.04.023
- Rütgen, M., Seidel, E. M., Riecansky, I., & Lamm, C. (2015). Reduction of empathy for pain by placebo analgesia suggests functional equivalence of empathy and first-hand emotion experience. Journal of Neuroscience, 35(23), 8938–8947. https://doi.org/10.1523/JNEUROSCI.3936-14.2015
- Rütgen, M., Seidel, E.-M., Silani, G., Riečanský, I., Hummer, A., Windischberger, C., Petrovic, P., & Lamm, C. (2015). Placebo analgesia and its opioidergic regulation suggest that empathy for pain is grounded in self pain. Proceedings of the National Academy of Sciences of the United States of America, 112(41), E5638–E5646. https://doi.org/10.1073/pnas.1511269112
- SAMHSA (2017). Key substance use and mental health indicators in the United States: Results from the 2016 National Survey on Drug Use and Health. https://www.samhsa.gov/data/
- Singer, T., & Lamm, C. (2009). The social neuroscience of empathy. Annals of the New York Academy of Sciences, 1156(1), 81–96. https://doi.org/10.1111/j.1749-6632.2009.04418.x
- Stellar, J. E., Cohen, A., Oveis, C., & Keltner, D. (2015). Affective and physiological responses to the suffering of others: Compassion and vagal activity. Journal of Personality and Social Psychology, 108(4), 572–585. https://doi.org/10.1037/pspi0000010
- Tarvainen, M. P., Niskanen, J. P., Lipponen, J. A., Ranta-Aho, P. O., & Karjalainen, P. A. (2014). Kubios HRV—Heart rate variability analysis software. Computer Methods and Programs in Biomedicine, 113(1), 210–220. https://doi.org/10.1016/j.cmpb.2013.07.024
- Task Force of the European Society of Cardiology. (1996). Heart rate variability: standards of measurement, physiological interpretation, and clinical use. task force of the European society of cardiology and the north American society of pacing and electrophysiology. Circulation, 93(5), 1043–1065. https://doi.org/10.1161/01.cir.93.5.1043
- Thayer, J. F., Ahs, F., Fredrikson, M., Sollers, J. J. 3rd, & Wager, T. D. (2012). A meta-analysis of heart rate variability and neuroimaging studies: Implications for heart rate variability as a marker of stress and health. Neuroscience & Biobehavioral Reviews, 36(2), 747–756. https://doi.org/10.1016/j.neubiorev.2011.11.009
- Thayer, J. F., & Lane, R. D. (2000). A model of neurovisceral integration in emotion regulation and dysregulation. Journal of Affective Disorders, 61(3), 201–216. https://doi.org/10.1016/S0165-0327(00)00338-4
- Thayer, J. F., & Lane, R. D. (2009). Claude Bernard and the heart-brain connection: Further elaboration of a model of neurovisceral integration. Neuroscience & Biobehavioral Reviews, 33(2), 81–88. https://doi.org/10.1016/j.neubiorev.2008.08.004
- Thayer, J. F., Sollers, J. J. 3rd, Ruiz-Padial, E., & Vila, J. (2002). Estimating respiratory frequency from autoregressive spectral analysis of heart period. IEEE Engineering in Medicine and Biology Magazine, 21(4), 41–45. https://doi.org/10.1109/memb.2002.1032638
- Thayer, J. F., & Sternberg, E. (2006). Beyond heart rate variability: Vagal regulation of allostatic systems. Annals of the New York Academy of Sciences, 1088, 361–372. https://doi.org/10.1196/annals.1366.014
- Umetani, K., Singer, D. H., McCraty, R., & Atkinson, M. (1998). Twenty-four hour time domain heart rate variability and heart rate: Relations to age and gender over nine decades. Journal of the American College of Cardiology, 31(3), 593–601. https://doi.org/10.1016/s0735-1097(97)00554-8
- Upadhyay, J., Maleki, N., Potter, J., Elman, I., Rudrauf, D., Knudsen, J., Wallin, D., Pendse, G., McDonald, L., Griffin, M., Anderson, J., Nutile, L., Renshaw, P., Weiss, R., Becerra, L., & Borsook, D. (2010). Alterations in brain structure and functional connectivity in prescription opioid-dependent patients. Brain, 133(Pt 7), 2098–2114. https://doi.org/10.1093/brain/awq138
- Vowles, K. E., McEntee, M. L., Julnes, P. S., Frohe, T., Ney, J. P., & van der Goes, D. N. (2015). Rates of opioid misuse, abuse, and addiction in chronic pain: A systematic review and data synthesis. Pain, 156(4), 569–576. https://doi.org/10.1097/01.j.pain.0000460357.01998.f1
- Wager, T. D., Scott, D. J., & Zubieta, J. K. (2007). Placebo effects on human mu-opioid activity during pain. Proceedings of the National Academy of Sciences of the United States of America, 104(26), 11056–11061. https://doi.org/10.1073/pnas.0702413104
- Watson, D., Clark, L. A., & Tellegen, A. (1988). Development and validation of brief measures of positive and negative affect: The PANAS scales. Journal of Personality and Social Psychology, 54(6), 1063–1070. https://doi.org/10.1037/0022-3514.54.6.1063
- Weiss, R. D., Potter, J. S., Griffin, M. L., McHugh, R. K., Haller, D., Jacobs, P., Gardin, J., Fischer, D., & Rosen, K. D. (2014). Reasons for opioid use among patients with dependence on prescription opioids: The role of chronic pain. Journal of Substance Abuse Treatment, 47(2), 140–145. https://doi.org/10.1016/j.jsat.2014.03.004
- Williams, D. P., Cash, C., Rankin, C., Bernardi, A., Koenig, J., & Thayer, J. F. (2015). Resting heart rate variability predicts self-reported difficulties in emotion regulation: A focus on different facets of emotion regulation. Frontiers in Psychology, 6, 261. https://doi.org/10.3389/fpsyg.2015.00261
- Williams, D. P., Feeling, N. R., Hill, L. K., Spangler, D. P., Koenig, J., & Thayer, J. F. (2017). Resting heart rate variability, facets of rumination and trait anxiety: Implications for the perseverative cognition hypothesis. Frontiers in Human Neuroscience, 11, 520. https://doi.org/10.3389/fnhum.2017.00520
- Wittchen, H. U., Wunderliche, U., Gruschwitz, S., & Zaudig, M. (1997). SKID-I. Strukturiertes Klinisches Interview für DSM-IV Achse I: Psychische Störungen (SCID-I. Structured Clinical Interview for DSM-IV Axes I: Mental Disorders). Hogrefe.
- Wunderli, M. D., Vonmoos, M., Treichler, L., Zeller, C., Dziobek, I., Kraemer, T., Baumgartner, M. R., Seifritz, E., & Quednow, B. B. (2018). Social cognition and interaction in chronic users of 3,4-methylenedioxymethamphetamine (MDMA, “Ecstasy”). International Journal of Neuropsychopharmacology, 21(4), 333–344. https://doi.org/10.1093/ijnp/pyx098
- Yarlott, L., Heald, E., & Forton, D. (2017). Hepatitis C virus infection, and neurological and psychiatric disorders—A review. Journal of Advanced Research, 8(2), 139–148. https://doi.org/10.1016/j.jare.2016.09.005
- Younger, J. W., Chu, L. F., D'Arcy, N. T., Trott, K. E., Jastrzab, L. E., & Mackey, S. C. (2011). Prescription opioid analgesics rapidly change the human brain. Pain, 152(8), 1803–1810. https://doi.org/10.1016/j.pain.2011.03.028
- Zhao, Y., Rutgen, M., Zhang, L., & Lamm, C. (2020). Pharmacological fMRI provides evidence for opioidergic modulation of discrimination of facial pain expressions. Psychophysiology, 58(2), e13717. https://doi.org/10.1111/psyp.13717
- Zubieta, J. K., Bueller, J. A., Jackson, L. R., Scott, D. J., Xu, Y., Koeppe, R. A., Nichols, T. E., & Stohler, C. S. (2005). Placebo effects mediated by endogenous opioid activity on mu-opioid receptors. Journal of Neuroscience, 25(34), 7754–7762. https://doi.org/10.1523/JNEUROSCI.0439-05.2005
Citing Literature
