Chronic back pain is associated with alterations in dopamine neurotransmission in the ventral striatum

Journal of Neuroscience

Volumn 35, Issue 27, 2015, Pages 9957-9965

  Martikainen, Ilkka K ^a   Nuechterlein, Emily B ^a,d   Peciña, Marta ^a,b   Love, Tiffany M ^a,b   Cummiford, Chelsea M ^a   Green, Carmen R ^c,d   Stohler, Christian S ^e   Zubieta, Jon Kar ^a,b,c  

^a UNIVERSITY OF MICHIGAN   (United States)

^b UNIVERSITY OF MICHIGAN HEALTH SYSTEM   (United States)

^c UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^d UNIVERSITY OF MICHIGAN   (United States)

^e Och Spine at New York Presbyterian Hospitals   (United States)

Author keywords

Amygdala; Chronic pain; Dopamine; Endogenous opioid; Striatum

Indexed keywords

DOPAMINE; DOPAMINE 2 RECEPTOR; DOPAMINE 3 RECEPTOR; MU OPIATE RECEPTOR; RACLOPRIDE C 11; CARBON; CARFENTANIL; DOPAMINE RECEPTOR BLOCKING AGENT; FENTANYL; NARCOTIC ANALGESIC AGENT; PROTEIN BINDING; RACLOPRIDE;

ADULT; AMYGDALOID NUCLEUS; ARTICLE; BACKACHE; CLINICAL ARTICLE; CONTROLLED STUDY; DISEASE ASSOCIATION; FEMALE; HUMAN; MALE; MCGILL PAIN QUESTIONNAIRE; MOOD DISORDER; NEUROTRANSMISSION; NUCLEAR MAGNETIC RESONANCE IMAGING; PAIN THRESHOLD; POSITIVE AND NEGATIVE AFFECT SCHEDULE; POSITRON EMISSION TOMOGRAPHY; PRIORITY JOURNAL; PROFILE OF MOOD STATES; VENTRAL STRIATUM; VISUAL ANALOG SCALE; ANALOGS AND DERIVATIVES; BRAIN MAPPING; CHRONIC DISEASE; DRUG EFFECTS; METABOLISM; PAIN MEASUREMENT; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; SCINTISCANNING; SYNAPTIC TRANSMISSION; YOUNG ADULT;

ADULT; ANALGESICS, OPIOID; BACK PAIN; BRAIN MAPPING; CARBON RADIOISOTOPES; CHRONIC DISEASE; DOPAMINE; DOPAMINE ANTAGONISTS; FEMALE; FENTANYL; HUMANS; MALE; PAIN MEASUREMENT; PROTEIN BINDING; RACLOPRIDE; RECEPTORS, DOPAMINE D2; RECEPTORS, DOPAMINE D3; SYNAPTIC TRANSMISSION; VENTRAL STRIATUM; YOUNG ADULT;

EID: 84936881487     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4605-14.2015     Document Type: Article

References (62)

1. Abercrombie ED, Keefe KA, DiFrischia DS, Zigmond MJ (1989) Differential effect of stress on in vivo dopamine release in striatum, nucleus accumbens, and medial frontal cortex. J Neurochem 52: 1655-1658. CrossRef Medline.
2. Altier N, Stewart J (1999) The role of dopamine in the nucleus accumbens in analgesia. Life Sci 65: 2269-2287. CrossRef Medline.
3. Austin PJ, Beyer K, Bembrick AL, Keay KA (2010) Peripheral nerve injury differentially regulates dopaminergic pathways in the nucleus accumbens of rats with either 'pain alone' or 'pain and disability'. Neuroscience 171: 329-343. CrossRef Medline.
4. Baliki MN, Geha PY, Fields HL, Apkarian AV (2010) Predicting value of pain and analgesia: nucleus accumbens response to noxious stimuli changes in the presence of chronic pain. Neuron 66: 149-160. CrossRef Medline.
5. Baliki MN, Petre B, Torbey S, Herrmann KM, Huang L, Schnitzer TJ, Fields HL, Apkarian AV (2012) Corticostriatal functional connectivity predicts transition to chronic back pain. Nat Neurosci 15: 1117-1119. CrossRef Medline.
6. Becker S, Ceko M, Louis-Foster M, Elfassy NM, Leyton M, Shir Y, Schweinhardt P (2013) Dopamine and pain sensitivity: neither sulpiride nor acute phenylalanine and tyrosine depletion have effects on thermal pain sensations in healthy volunteers. PLoS One 8: e80766. CrossRef Medline.
7. Brischoux F, Chakraborty S, Brierley DI, Ungless MA (2009) Phasic excitation of dopamine neurons in ventral VTA by noxious stimuli. Proc Natl Acad Sci U S A 106: 4894-4899. CrossRef Medline.
8. Burgdorf J, Panksepp J (2006) The neurobiology of positive emotions. Neurosci Biobehav Rev 30: 173-187. CrossRef Medline.
9. Carson RE, Breier A, de Bartolomeis A, Saunders RC, Su TP, Schmall B, Der MG, Pickar D, Eckelman WC (1997) Quantification of amphetamineinduced changes in [11C]raclopride binding with continuous infusion. J Cereb Blood Flow Metab 17: 437-447. Medline.
10. Chang PC, Pollema-Mays SL, Centeno MV, Procissi D, Contini M, Baria AT, Martina M, Apkarian AV (2014) Role of nucleus accumbens in neuropathic pain: linked multi-scale evidence in the rat transitioning to neuropathic pain. Pain 155: 1128-1139. CrossRef Medline.
11. Chen JF, Aloyo VJ, Weiss B (1993) Continuous treatment with the D2 dopamine receptor agonist quinpirole decreases D2 dopamine receptors, D2 dopamine receptor messenger RNA and proenkephalin messenger RNA, and increases mu opioid receptors in mouse striatum. Neuroscience 54: 669-680. CrossRef Medline.
12. Clauw DJ, Williams D, Lauerman W, Dahlman M, Aslami A, Nachemson AL, Kobrine AI, Wiesel SW (1999) Pain sensitivity as a correlate of clinical status in individuals with chronic low back pain. Spine 24: 2035-2041. CrossRef Medline.
13. Coghill RC, Sang CN, Maisog JM, Iadarola MJ (1999) Pain intensity processing within the human brain: a bilateral, distributed mechanism. J Neurophysiol 82: 1934-1943. Medline.
14. Edwards RR, Doleys DM, Lowery D, Fillingim RB (2003) Pain tolerance as a predictor of outcome following multidisciplinary treatment for chronic pain: differential effects as a function of sex. Pain 106: 419-426. CrossRef Medline.
15. Fudge JL, Haber SN (2000) The central nucleus of the amygdala projection to dopamine subpopulations in primates. Neuroscience 97: 479-494. CrossRef Medline.
16. Gear RW, Aley KO, Levine JD (1999) Pain-induced analgesia mediated by mesolimbic reward circuits. J Neurosci 19: 7175-7181. Medline.
17. Giesecke T, Gracely RH, Grant MA, Nachemson A, Petzke F, Williams DA, Clauw DJ (2004) Evidence of augmented central pain processing in idiopathic chronic low back pain. Arthritis Rheum 50: 613-623. CrossRef Medline.
18. Haber SN (2003) The primate basal ganglia: parallel and integrative networks. J Chem Neuroanat 26: 317-330. CrossRef Medline.
19. Haber SN (2011) Neuroanatomy of reward: a view from the ventral striatum. In: Neurobiology of sensation and reward (Gottfried JA, ed). Boca Raton, FL: CRC.
20. Hagelberg N, Martikainen IK, Mansikka H, Hinkka S, Någren K, Hietala J, Scheinin H, Pertovaara A (2002) Dopamine D2 receptor binding in the human brain is associated with the response to painful stimulation and pain modulatory capacity. Pain 99: 273-279. CrossRef Medline.
21. Hagelberg N, Forssell H, Rinne JO, Scheinin H, Taiminen T, Aalto S, Luutonen S, Någren K, Jääskeläinen S (2003a) Striatal dopamine D1 and D2 receptors in burning mouth syndrome. Pain 101: 149-154. CrossRef Medline.
22. Hagelberg N, Forssell H, Aalto S, Rinne JO, Scheinin H, Taiminen T, Någren K, Eskola O, Jääskeläinen SK (2003b) Altered dopamine D2 receptor binding in atypical facial pain. Pain 106: 43-48. CrossRef Medline.
23. Horvitz JC (2000) Mesolimbocortical and nigrostriatal dopamine responses to salient non-reward events. Neuroscience 96: 651-656. CrossRef Medline.
24. Jääskeläinen SK, Lindholm P, Valmunen T, Pesonen U, Taiminen T, Virtanen A, Lamusuo S, Forssell H, Hagelberg N, Hietala J, Pertovaara A (2014) Variation in the dopamine D2 receptor gene plays a key role in human pain and its modulation by transcranial magnetic stimulation. Pain 155: 2180-2187. CrossRef Medline.
25. Jewett DM (2001) A simple synthesis of [11C]carfentanil using an extraction disk instead of HPLC. Nucl Med Biol 28: 733-734. CrossRef Medline.
26. Kelley AE, Domesick VB, Nauta WJ (1982) The amygdalostriatal projection in the rat-an anatomical study by anterograde and retrograde tracing methods. Neuroscience 7: 615-630. CrossRef Medline.
27. Ladouceur A, Tessier J, Provencher B, Rainville P, Piché M (2012) Topdown attentional modulation of analgesia induced by heterotopic noxious counterstimulation. Pain 153: 1755-1762. CrossRef Medline.
28. Logan J, Fowler JS, Volkow ND, Wang GJ, Ding YS, Alexoff DL (1996) Distribution volume ratios without blood sampling from graphical analysis of PET data. J Cereb Blood Flow Metab 16: 834-840. Medline.
29. Magnusson JE, Fisher K (2000) The involvement of dopamine in nociception: the role of D(1) and D(2) receptors in the dorsolateral striatum. Brain Res 855: 260-266. CrossRef Medline.
30. Martikainen IK, Peciña M, Love TM, Nuechterlein EB, Cummiford CM, Green CR, Harris RE, Stohler CS, Zubieta JK (2013) Alterations in endogenous opioid functional measures in chronic back pain. J Neurosci 33: 14729-14737. CrossRef Medline.
31. McNair D, Lorr M, Droppleman L (1992) EdITS manual for the profile of mood states. San Diego: Educational and Industrial Testing Service.
32. Melzack R, Torgerson WS (1971) On the language of pain. Anesthesiology 34: 50-59. CrossRef Medline.
33. Minoshima S, Koeppe RA, Mintun MA, Berger KL, Taylor SF, Frey KA, Kuhl DE (1993) Automated detection of the intercommissural line for stereotactic localization of functional brain images. J Nucl Med 34: 322-329. Medline.
34. Morgan MJ, Franklin KB (1990) 6-Hydroxydopamine lesions of the ventral tegmentum abolish D-amphetamine and morphine analgesia in the formalin test but not in the tail flick test. Brain Res 519: 144-149. CrossRef Medline.
35. Morgan MJ, Franklin KB (1991) Dopamine receptor subtypes and formalin test analgesia. Pharmacol Biochem Behav 40: 317-322. CrossRef Medline.
36. O'Neill S, Manniche C, Graven-Nielsen T, Arendt-Nielsen L (2007) Generalized deep-tissue hyperalgesia in patients with chronic low-back pain. Eur J Pain 11: 415-420. CrossRef Medline.
37. Phillips AG, Ahn S, Howland JG (2003) Amygdalar control of the mesocorticolimbic dopamine system: parallel pathways to motivated behavior. Neurosci Biobehav Rev 27: 543-554. CrossRef Medline.
38. Rougé-Pont F, Piazza PV, Kharouby M, Le Moal M, SimonH (1993) Higher and longer stress-induced increase in dopamine concentrations in the nucleus accumbens of animals predisposed to amphetamine selfadministration. A microdialysis study. Brain Res 602: 169-174. CrossRef Medline.
39. Salamone JD, Correa M (2012) The mysterious motivational functions of mesolimbic dopamine. Neuron 76: 470-485. CrossRef Medline.
40. Schmidt BL, Tambeli CH, Barletta J, Luo L, Green P, Levine JD, Gear RW (2002) Altered nucleus accumbens circuitry mediates pain-induced antinociception in morphine-tolerant rats. J Neurosci 22: 6773-6780. Medline.
41. Schwartz N, Temkin P, Jurado S, Lim BK, Heifets BD, Polepalli JS, Malenka RC (2014) Chronic pain. Decreased motivation during chronic pain requires long-term depression in the nucleus accumbens. Science 345: 535-542. CrossRef Medline.
42. Scott DJ, Heitzeg MM, Koeppe RA, Stohler CS, Zubieta JK (2006) Variations in the human pain stress experience mediated by ventral and dorsal basal ganglia dopamine activity. J Neurosci 26: 10789-10795. CrossRef Medline.
43. Scott DJ, Stohler CS, Koeppe RA, Zubieta JK (2007) Time-course of change in [11C]carfentanil and [11C]raclopride binding potential after a nonpharmacological challenge. Synapse 61: 707-714. CrossRef Medline.
44. Scott DJ, Stohler CS, Egnatuk CM, Wang H, Koeppe RA, Zubieta JK (2008) Placebo and nocebo effects are defined by opposite opioid and dopaminergic responses. Arch Gen Psychiatry 65: 220-231. CrossRef Medline.
45. Seeman P, Wilson A, Gmeiner P, Kapur S (2006) Dopamine D2 and D3 receptors in human putamen, caudate nucleus, and globus pallidus. Synapse 60: 205-211. CrossRef Medline.
46. Soderman AR, Unterwald EM (2009) Cocaine-induced mu opioid receptor occupancy within the striatum is mediated by dopamine D2 receptors. Brain Res 1296: 63-71. CrossRef Medline.
47. Sowman PF, Wang K, Svensson P, Arendt-Nielsen L (2011) Diffuse noxious inhibitory control evoked by tonic craniofacial pain in humans. Eur J Pain 15: 139-145. CrossRef Medline.
48. Steiner H, Gerfen CR (1998) Role of dynorphin and enkephalin in the regulation of striatal output pathways and behavior. Exp Brain Res 123: 60-76. CrossRef Medline.
49. Stohler CS, Kowalski CJ (1999) Spatial and temporal summation of sensory and affective dimensions of deep somatic pain. Pain 79: 165-173. CrossRef Medline.
50. Strand EB, Zautra AJ, Thoresen M, Ødegård S, Uhlig T, Finset A (2006) Positive affect as a factor of resilience in the pain-negative affect relationship in patients with rheumatoid arthritis. J Psychosom Res 60: 477-484. CrossRef Medline.
51. Tang NK, Salkovskis PM, Hodges A, Wright KJ, Hanna M, Hester J (2008) Effects of mood on pain responses and pain tolerance: an experimental study in chronic back pain patients. Pain 138: 392-401. CrossRef Medline.
52. Taylor BK, Joshi C, Uppal H (2003) Stimulation of dopamine D2 receptors in the nucleus accumbens inhibits inflammatory pain. Brain Res 987: 135-143. CrossRef Medline.
53. Tiemann L, Heitmann H, Schulz E, Baumkötter J, Ploner M (2014) Dopamine precursor depletion influences pain affect rather than pain sensation. PLoS One 9: e96167. CrossRef Medline.
54. Treister R, Pud D, Ebstein RP, Laiba E, Gershon E, Haddad M, Eisenberg E (2009) Associations between polymorphisms in dopamine neurotransmitter pathway genes and pain response in healthy humans. Pain 147: 187-193. CrossRef Medline.
55. Volkow ND, Fowler JS, Wang GJ, Swanson JM, Telang F (2007) Dopamine in drug abuse and addiction: results of imaging studies and treatment implications. Arch Neurol 64: 1575-1579. CrossRef Medline.
56. Von Korff M, Miglioretti DL (2005) A prognostic approach to defining chronic pain. Pain 117: 304-313. CrossRef Medline.
57. Watabe H, Endres CJ, Breier A, Schmall B, Eckelman WC, Carson RE (2000) Measurement of dopamine release with continuous infusion of [11C]raclopride: optimization and signal-to-noise considerations. J Nucl Med 41: 522-530. Medline.
58. Watson D, Clark LA (1999) Manual for the positive and negative affect schedule-expanded form. Iowa City, IA: The University of Iowa.
59. Wood PB, Schweinhardt P, Jaeger E, Dagher A, Hakyemez H, Rabiner EA, Bushnell MC, Chizh BA (2007) Fibromyalgia patients show an abnormal dopamine response to pain. Eur J Neurosci 25: 3576-3582. CrossRef Medline.
60. Zautra AJ, Johnson LM, Davis MC (2005) Positive affect as a source of resilience for women in chronic pain. J Consult Clin Psychol 73: 212-220. CrossRef Medline.
61. Zhang X, Ashton-Miller JA, Stohler CS (1993) A closed-loop system for maintaining constant experimental muscle pain in man. IEEE Trans Biomed Eng 40: 344-352. CrossRef Medline.
62. Zubieta JK, Smith YR, Bueller JA, Xu Y, Kilbourn MR, Jewett DM, Meyer CR, Koeppe RA, Stohler CS (2001) Regional mu opioid receptor regulation of sensory and affective dimensions of pain. Science 293: 311-315. CrossRef Medline.