Effects of Mindfulness-Oriented Recovery Enhancement on reward responsiveness and opioid cue-reactivity

Abstract

Rationale

Dysregulated reward processing is a hallmark feature of drug addiction; however, scant research has evaluated restructuring reward processing in the context of addiction treatment.

Objectives

We examined effects of Mindfulness-Oriented Recovery Enhancement (MORE) on reward responsiveness (RR) and opioid cue-reactivity in a sample of chronic pain patients with opioid use problems. We previously reported that MORE decreased pain, opioid misuse, and craving relative to a social support control group (SG). Here, we examined whether these outcomes were linked to changes in RR in a subset of participants.

Methods

Participants were chronic pain patients (71 % women, age 46.6 ± 13.9) who received MORE (n = 20) or SG (n = 29). RR was measured before and after 8 weeks of treatment via heart rate (HR) and heart rate variability (HRV) responses during a dot probe task that included opioid-related, pain-related, and natural reward stimuli, as well as craving ratings.

Results

The MORE group, who reported decreased opioid misuse and opioid craving during treatment, evidenced less subjective opioid cue-reactivity, greater HR decelerations, and greater increases in HRV to all cues after treatment compared to the SG; HR and HRV effects were most pronounced for natural reward cues. Within the MORE group, HR deceleration to natural reward cues was correlated with increased subjective arousal to the cues, whereas HR deceleration to opioid cues was correlated with decreased subjective arousal. Effects of MORE on craving were mediated by enhanced RR.

Conclusions

Results suggest that during treatment with MORE, cardiac-autonomic responsiveness to non-drug reward increases, while reactivity to opioid reward decreases. Studies are needed to discern whether changes in RR were a result or a determinant of reductions in opioid misuse and craving. RR may play a role in addiction treatment.

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References

  1. Alcaro A, Panksepp J (2011) The SEEKING mind: primal neuro-affective substrates for appetitive incentive states and their pathological dynamics in addictions and depression. Neurosci Biobehav Rev 35:1805–1820

    PubMed  Article  Google Scholar 

  2. Augustus Diggs H, Froeliger B, Carlson JM, Gilbert DG (2013) Smoker–nonsmoker differences in neural response to smoking-related and affective cues: an fMRI investigation. Psychiatry Res: Neuroimaging 211:85–87

    PubMed  Article  Google Scholar 

  3. Baron RM, Kenny DA (1986) The moderator-mediator variable distinction in social psychological research: conceptual, strategic, and statistical considerations. J Pers Soc Psychol 51:1173–1182

    CAS  PubMed  Article  Google Scholar 

  4. Berntson GG, Bigger JT Jr, Eckberg DL, Grossman P, Kaufman PG, Malik M, Nagaraja HN, Porges SW, Saul JP, Stone PH, van der Molen MW (1997) Heart rate variability: origins, methods, and interpretive caveats. Psychophysiol 34:623–648

    CAS  Article  Google Scholar 

  5. Bradley MM, Codispoti M, Cuthbert BN, Lang PJ (2001) Emotion and motivation I: defensive and appetitive reactions in picture processing. Emotion 1:276–298

    CAS  PubMed  Article  Google Scholar 

  6. Browne MW, Cudeck R (1993) Alternative ways of assessing model fit. Sage Focus Editions 154:136–136

    Google Scholar 

  7. Butler SF, Budman SH, Fernandez KC, Houle B, Benoit C, Katz N, Jamison RN (2007) Development and validation of the Current Opioid Misuse Measure. Pain 130:144–156

    PubMed Central  PubMed  Article  Google Scholar 

  8. Carmines EG, McIver JP (1981) Analyzing models with unobserved variables: analysis of covariance structures. Social measurement, Current issues:65–115

  9. Carter BL, Tiffany ST (1999) Meta-analysis of cue-reactivity in addiction research. Addiction 94:327–340

    CAS  PubMed  Article  Google Scholar 

  10. Chou R, Fanciullo GJ, Fine PG, Adler JA, Ballantyne JC, Davies P, Donovan MI, Fishbain DA, Foley KM, Fudin J et al (2009) Clinical guidelines for the use of chronic opioid therapy in chronic noncancer pain. J Pain 10:113–130

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  11. Cleeland CS (1994) Brief Pain Inventory-Short Form (BPI-SF). Houston, TX

    Google Scholar 

  12. Cultbertson C, Nicholas S, Zaharovits I, London ED, De La Garza R, Brody AL, Newton TF (2010) Methamphetamine craving induced in an online virtual reality environment. Pharmacol, Biochem Behav 96:454–460

    Article  Google Scholar 

  13. Davidson L, White W (2007) The concept of recovery as an organizing principle for integrating mental health and addiction services. J Beh Health Services 34:1094–3412

    Google Scholar 

  14. De Wit H (2009) Impulsivity as a determinant and consequence of drug use: a review of underlying processes. Addict Biol 14:22–31

    PubMed Central  PubMed  Article  Google Scholar 

  15. Erblich J, Bovbjerg DH, Sloan RP (2011) Exposure to smoking cues: cardiovascular and autonomic effects. Addict Behav 36:737–742

    PubMed Central  PubMed  Article  Google Scholar 

  16. Garland EL (2013) Mindfulness-Oriented Recovery Enhancement for addiction, stress, and pain. NASW Press, Washington, D.C.

    Google Scholar 

  17. Garland EL, Fredrickson BL, Kring AM, Johnson DP, Meyer PS, Penn DL (2010a) Upward spirals of positive emotions counter downward spirals of negativity: insights from the broaden-and-build theory and affective neuroscience on the treatment of emotion dysfunctions and deficits in psychopathology. Clin Psychol Rev 30:849–864

    PubMed Central  PubMed  Article  Google Scholar 

  18. Garland EL, Gaylord SA, Boettiger CA, Howard MO (2010b) Mindfulness training modifies cognitive, affective, and physiological mechanisms implicated in alcohol dependence: results of a randomized controlled pilot trial. J Psychoactive Drugs 42:177–192

    PubMed Central  PubMed  Article  Google Scholar 

  19. Garland EL, Franken IH, Howard MO (2012a) Cue-elicited heart rate variability and attentional bias predict alcohol relapse following treatment. Psychopharmacology 222:17–26

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  20. Garland EL, Froeliger B, Passik S, Howard M (2012b) Attentional bias for prescription opioid cues among opioid dependent chronic pain patients. J Behav Med doi: 10.1007/s10865-012-9455-8

  21. Garland EL, Froeliger B, Zeidan F, Partin K, Howard MO (2013a) The downward spiral of chronic pain, prescription opioid misuse, and addiction: cognitive, affective, and neuropsychopharmacologic pathways. Neurosci Biobehav Rev 17:377–393. doi:10.1016/j.neubiorev.2013.08.006

    Google Scholar 

  22. Garland EL, Froeliger B, Howard MO (2014) Mindfulness training targets neurocognitive mechanisms of addiction at the attention-appraisal-emotion interface. Front Psychiatr 4:173. doi:10.3389/fpsyt.2013.00173

    Article  Google Scholar 

  23. Garland EL, Manusov EG, Froeliger B, Kelly A, Williams J, Howard MO (2014) Mindfulness-Oriented Recovery Enhancement for chronic pain and prescription opioid misuse: results from an early stage randomized controlled trial. J Consult Clin Psychol.

  24. Geschwind N, Peeters F, Drukker M, van Os J, Wichers M (2011) Mindfulness training increases momentary positive emotions and reward experience in adults vulnerable to depression: a randomized controlled trial. J Consult Clin Psychol 79:618–628

    PubMed  Article  Google Scholar 

  25. Gipson CD, Reissner KJ, Kupchik YM, Smith AC, Stankeviciute N, Hensley-Simon ME, Kalivas PW (2013) Reinstatement of nicotine seeking is mediated by glutamatergic plasticity. Proc Natl Acad Sci U S A 110:9124–9129

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  26. Heinz A, Siessmeier T, Wrase J, Hermann D, Klein S, Grusser SM, Flor H, Braus DF, Buchholz HG, Grunder G, Schreckenberger M, Smolka MN, Rosch F, Mann K, Bartenstein P (2004) Correlation between dopamine D(2) receptors in the ventral striatum and central processing of alcohol cues and craving. Am J Psychiatry 161:1783–1789

    PubMed  Article  Google Scholar 

  27. Inagaki H, Kuwahara M, Tsubone H (2005) Changes in autonomic control of heart associated with classical appetitive conditioning in rats. Exp Animals 54:61–69

    CAS  Article  Google Scholar 

  28. Kabat-Zinn J (1982) An outpatient program in behavioral medicine for chronic pain patients based on the practice of mindfulness meditation: theoretical considerations and preliminary results. Gen Hosp Psychiatry 4:33–47

    CAS  PubMed  Article  Google Scholar 

  29. Kalivas PW, Volkow ND (2005) The neural basis of addiction: a pathology of motivation and choice. Amer J Psychiatry 162:1403–1413

    Article  Google Scholar 

  30. Kline RB (1998) Principles and practice of structural equation modeling. Guilford, New York

    Google Scholar 

  31. Kober H, Mende-Siedlecki P, Kross EF, Weber J, Mischel W, Hart CL, Ochsner KN (2011) Prefrontal-striatal pathway underlies cognitive regulation of craving. Proc Natl Acad Sci U S A 107:14811–14816

    Article  Google Scholar 

  32. Koob GD, Le Moal M (2001) Drug addiction, dysregulation of reward, and allostasis. Neuropsychopharmacology 24:97–129

    CAS  PubMed  Article  Google Scholar 

  33. Koob GF, Le Moal M (2008) Neurobiological mechanisms for opponent motivational processes in addiction. Phil Trans Royal Soc B: Bio Sci 363:3113–3123

    Article  Google Scholar 

  34. Kreibig SD (2011) Autonomic nervous system activation in emotion: a review. Biol Psychol. doi:10.1016/j.biopsycho.2010.03.010

    PubMed  Google Scholar 

  35. Lane RD, McRae K, Reiman EM, Chen K, Ahern GL, Thayer JF (2009) Neural correlates of heart rate variability during emotion. Neuroimage 44:213–222

    PubMed  Article  Google Scholar 

  36. Lang PJ, Bradley MM, Cuthbert BN (1997a) International affective picture system (IAPS): technical manual and affective ratings. NIMH Center for the Study of Emotion and Attention. Gainesville, FL

    Google Scholar 

  37. Lang PJ, Bradley MM, Cuthbert BN (1997b) Motivated attention: affect, activation, and action. In: Lang PJ, Simons RF, Balaban MT (eds) Attention and orienting: sensory and motivational processes. Hillsdale, NJ, Erlbaum, pp 97–135

    Google Scholar 

  38. Lee B, London ED, Poldrack RA, Farahi J, Nacca A, Monterosso JR, Mumford JA, Bokarius AV, Dahlbom M, Mukherjee J (2009) Striatal dopamine d2/d3 receptor availability is reduced in methamphetamine dependence and is linked to impulsivity. J Neurosci 29:14734–14740

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  39. Lintas A, Chi N, Lauzon NM, Bishop SF, Sun N, Tan H, Laviolette SR (2012) Inputs from the basolateral amygdala to the nucleus accumbens shell control opiate reward magnitude via differential dopamine D1 or D2 receptor transmission. Eur J Neurosci 35:279–290

    PubMed  Article  Google Scholar 

  40. Lubman DI, Allen NB, Peters LA, Deakin JF (2007) Electrophysiological evidence of the motivational salience of drug cues in opiate addiction. Psychol Med 37:1203–1209

    PubMed  Article  Google Scholar 

  41. Lubman DI, Allen NB, Peters LA, Deakin JF (2008) Electrophysiological evidence that drug cues have greater salience than other affective stimuli in opiate addiction. J Psychopharm 22:836–842

    CAS  Article  Google Scholar 

  42. Lubman DI, Yucel M, Kettle JW, Scaffidi A, Mackenzie T, Simmons JG, Allen NB (2009) Responsiveness to drug cues and natural rewards in opiate addiction: associations with later heroin use. Arch Gen Psychiatry 66:205–212

    PubMed  Article  Google Scholar 

  43. Nederkoorn C, Smulders FTY, Jansen A (2000) Cephalic phase responses, craving, and food intake in normal subjects. Appetite 35:45–55

    CAS  PubMed  Article  Google Scholar 

  44. Ochsner KN, Gross JJ (2005) The cognitive control of emotion. Trends Cog Sci 9:242–249

    Article  Google Scholar 

  45. Rawson R, McCann MJ (2006) Counselor’s treatment manual: matrix intensive outpatient treatment for people with stimulant use disorders. DHHS Publication No. (SMA)

  46. Rosenzweig S, Greeson JM, Reibel DK, Green JS, Jasser SA, Beasley D (2010) Mindfulness-based stress reduction for chronic pain conditions: variation in treatment outcomes and role of home meditation practice. J Psychosom Res 68:29–36

    PubMed  Article  Google Scholar 

  47. Sayette MA, Tiffany ST (2013) Peak-provoked craving: an alternative to smoking cue-reactivity. Addiction 108:1030–1031

    PubMed  Article  Google Scholar 

  48. Segerstrom SC, Nes LS (2007) Heart rate variability reflects self-regulatory strength, effort, and fatigue. Psychol Sci 18:275–281

    PubMed  Article  Google Scholar 

  49. Sheehan DV, Lecrubier Y, Sheehan KH, Amorim P, Janavs J, Weiller E, Hergueta T, Baker R, Dunbar GC (1998) The Mini-International Neuropsychiatric Interview (M.I.N.I.): the development and validation of a structured diagnostic psychiatric interview for DSM-IV and ICD-10. J Clin Psychiatry 59(Suppl 20):22–33

    PubMed  Google Scholar 

  50. Shizgal P, Hyman SP (2013) Motivational and addictive states. In: Kandel ER, Schwartz JH, Jessell TM, Siegelbaum S, Hudspeth J (eds) Principles of neural science, 5th edn. McGraw-Hill, New York

    Google Scholar 

  51. Thayer JF, Lane RD (2009) Claude Bernard and the heart-brain connection: further elaboration of a model of neurovisceral integration. Neurosci Biobehav Rev 33:81–88

    PubMed  Article  Google Scholar 

  52. Thayer JF, Hansen AL, Saus-Rose ES, Johnsen BH (2009) Heart rate variability, prefrontal neural function, and cognitive performance: the neurovisceral integration perspective on self-regulation, adaptation, and health. Ann Behav Med 37:141–153

    PubMed  Article  Google Scholar 

  53. Tiffany ST, Wray JW (2012) The clinical significance of drug craving. Ann NY Acad Sci 1248:1–17

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  54. Udo T, Weinberger AH, Grilo CM, Brownell KD, DiLeone RJ, Lampert R, Matlin SL, Yanagisawa K, McKee SA (2013) Heightened vagal activity during high-calorie food presentation in obese compared with non-obese individuals—results of a pilot study. Obes Res Clin Practice. doi:10.1016/j.orcp.2013.05.006

  55. Volkow ND, Fowler JS, Wang G-J (2004) The addicted human brain viewed in the light of imaging studies: brain circuits and treatment strategies. Neuropharmacology 47:3–13

    CAS  PubMed  Article  Google Scholar 

  56. Volkow ND, Wang G-J, Fowler JS, Tomasi D, Telang F, Baler R (2010) Addiction: decreased reward sensitivity and increased expectation sensitivity conspire to overwhelm the brain’s control circuit. BioEssays 32:748–755

    PubMed Central  PubMed  Article  Google Scholar 

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Acknowledgments

This work was supported by grant numbers DA032517 and DA037005 from the National Institutes of Health awarded to E.L.G. and a grant from the Fahs Beck Fund for Research and Experimentation, also awarded to E.L.G.

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Correspondence to Eric L. Garland.

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Garland, E.L., Froeliger, B. & Howard, M.O. Effects of Mindfulness-Oriented Recovery Enhancement on reward responsiveness and opioid cue-reactivity. Psychopharmacology 231, 3229–3238 (2014). https://doi.org/10.1007/s00213-014-3504-7

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Keywords

  • Mindfulness
  • Chronic pain
  • Opioid misuse
  • Addiction
  • Reward
  • Heart rate variability
  • Attentional bias
  • Positive affect
  • Allostasis
  • Cue-reactivity