Separating analgesia from reward within the ventral tegmental area

Neuroscience

Volumn 263, Issue , 2014, Pages 72-87

  Schifirnet, E ^a   Bowen, S E ^a   Borszcz, G S ^a  

^a WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Addiction; Analgesia; Muscarinic; Nicotinic; Pain; Reward

Indexed keywords

ADDICTION; ANALGESIA; MUSCARINIC; NICOTINIC; PAIN; REWARD;

ANALGESIA; ANIMALS; ATROPINE; CARBACHOL; CHOLINERGIC AGONISTS; MALE; MECAMYLAMINE; MUSCARINIC ANTAGONISTS; NICOTINIC ANTAGONISTS; PAIN THRESHOLD; RATS; RATS, LONG-EVANS; REWARD; VENTRAL TEGMENTAL AREA;

EID: 84893777624     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2014.01.009     Document Type: Article

References (102)

1. Altier N., Stewart J. Dopamine receptor antagonists in the nucleus accumbens attenuate analgesia induced by ventral tegmental area substance P or morphine and by nucleus accumbens amphetamine. J Pharmacol Exp Ther 1998, 285:208-215.
2. Arencibia-Albite F., Paladini C., Williams J.T., Jimenez-Rivera C.A. Noradrenergic modulation of the hyperpolarization-activated cation current (Ih) in dopamine neurons of the ventral tegmental area. Neuroscience 2007, 149:303-314.
3. Bardo M.T., Bevins R.A. Conditioned place preference: what does it add to our preclinical understanding of drug reward?. Psychopharmacology (Berl) 2000, 153:31-43.
4. Basbaum A.I., Fields H.L. Endogenous pain control systems: brainstem spinal pathways and endorphin circuitry. Annu Rev Neurosci 1984, 7:309-338.
5. Baxter M.G., Murray E.A. The amygdala and reward. Nat Rev Neurosci 2002, 3:563-573.
6. Becker W.C., Sullivan L.E., Tetrault J.M., Desai R.A., Fiellin D.A. Non-medical use, abuse and dependence on prescription opioids among U.S. adults: psychiatric, medical and substance use correlates. Drug Alcohol Depend 2008, 94:38-47.
7. Blaha C.D., Allen L.F., Das S., Inglis W.L., Latimer M.P., Vincent S.R., Winn P. Modulation of dopamine efflux in the nucleus accumbens after cholinergic stimulation of the ventral tegmental area in intact, pedunculopontine tegmental nucleus-lesioned, and laterodorsal tegmental nucleus-lesioned rats. J Neurosci 1996, 16:714-722.
8. Bohnert A.S., Valenstein M., Bair M.J., Ganoczy D., McCarthy J.F., Ilgen M.A., Blow F.C. Association between opioid prescribing patterns and opioid overdose-related deaths. JAMA 2011, 305:1315-1321.
9. Borszcz G.S. The capacity of motor reflex and vocalization thresholds to support avoidance conditioning in the rat. Behav Neurosci 1993, 107:678-693.
10. Borszcz G.S. Pavlovian conditional vocalizations of the rat: a model system for analyzing the fear of pain. Behav Neurosci 1995, 109:648-662.
11. Borszcz G.S. Differential contributions of medullary, thalamic, and amygdaloid serotonin to the antinociceptive action of morphine administered into the periaqueductal gray: a model of morphine analgesia. Behav Neurosci 1999, 113:612-631.
12. Borszcz G.S. Contribution of the ventromedial hypothalamus to generation of the affective dimension of pain. Pain 2006, 123:155-168.
13. Borszcz G.S., Johnson C.P., Fahey K.A. Comparison of motor reflex and vocalization thresholds following systemically administered morphine, fentanyl, and diazepam in the rat: assessment of sensory and performance variables. Pharmaco Biochem Behav 1994, 49:827-834.
14. Borszcz G.S., Johnson C.P., Anderson M.E., Young B.J. Characterization of tailshock elicited withdrawal reflexes in intact and spinal rats. Physiol Behav 1992, 52:1055-1062.
15. Borszcz G.S., Leaton R.N. The effect of amygdala lesions on conditional and unconditional vocalizations in rats. Neurobiol Learn Mem 2003, 79:212-225.
16. Borszcz G.S., Spuz C.A. Hypothalamic control of pain vocalization and affective dimension of pain signaling. Handbook of mammalian vocalization 2009, 281-291. Academic Press, Oxford. S.M. Brudzynski (Ed.).
17. Burkey A.R., Carstens E., Jasmin L. Dopamine reuptake inhibition in the rostral agranular insular cortex produces antinociception. J Neurosci 1999, 19:4169-4179.
18. Calabresi P., Lacey M.G., North R.A. Nicotinic excitation of rat ventral tegmental neurones in vitro studied by intracellular recording. Br J Pharmacol 1989, 98:135-140.
19. Carroll M.N., Lim K.S. Observations on the neuropharmacology of morphine and morphine like analgesia. Arch Int Pharmacodyn Ther 1960, 125:383-403.
20. Carr D.B., Sesack S.R. GABA-containing neurons in the rat ventral tegmental area project to the prefrontal cortex. Synapse 2000, 38:114-123.
21. de la Mora M.P., Gallegos-Cari A., Arizmendi-Garcia Y., Marcellino D., Fuxe K. Role of dopamine receptor mechanisms in the amygdaloid modulation of fear and anxiety: structural and functional analysis. Prog Neurobiol 2010, 90:198-216.
22. Deniau J.M., Thierry A.M., Feger J. Electrophysiological identification of mesencephalic ventromedial tegmental (VMT) neurons projecting to the frontal cortex, septum and nucleus accumbens. Brain Res 1980, 189:315-326.
23. Di Chiara G. Nucleus accumbens shell and core dopamine: differential role in behavior and addiction. Behav Brain Res 2002, 137:75-114.
24. Di Pietro N.C., Mashhoon Y., Heaney C., Yager L.M., Kantak K.M. Role of dopamine D1 receptors in the prefrontal dorsal agranular insular cortex in mediating cocaine self-administration in rats. Psychopharmacology (Berl) 2008, 200:81-91.
25. Fanselow M.S. Odors released by stressed rats produce opioid analgesia in unstressed rats. Behav Neurosci 1985, 99:589-592.
26. Fiorillo C.D., Williams J.T. Cholinergic inhibition of ventral midbrain dopamine neurons. J Neurosci 2000, 20:7855-7860.
27. Forster G.L., Blaha C.D. Laterodorsal tegmental stimulation elicits dopamine efflux in the rat nucleus accumbens by activation of acetylcholine and glutamate receptors in the ventral tegmental area. Eur J Neurosci 2000, 12:3596-3604.
28. Forster G.L., Yeomans J.S., Takeuchi J., Blaha C.D. M5 muscarinic receptors are required for prolonged accumbal dopamine release after electrical stimulation of the pons in mice. J Neurosci 2002, 22. RC190 (1-6).
29. Franklin K.B. Analgesia and the neural substrate of reward. Neurosci Biobehav Rev 1989, 13:149-154.
30. Franklin K.B. Analgesia and abuse potential: an accidental association or a common substrate?. Pharmacol Biochem Behav 1998, 59:993-1002.
31. Goeders N.E., Smith J.E. Cortical dopaminergic involvement in cocaine reinforcement. Science 1983, 221:773-775.
32. Goeders N.E., Smith J.E. Reinforcing properties of cocaine in the medical prefrontal cortex: primary action on presynaptic dopaminergic terminals. Pharmacol Biochem Behav 1986, 25:191-199.
33. Gracely R.H., McGrath P., Dubner R. Validity and sensitivity of ratio scales of sensory and affective verbal pain descriptors: manipulation of affect by diazepam. Pain 1978, 5:19-29.
34. Gronier B., Rasmussen K. Activation of midbrain presumed dopaminergic neurones by muscarinic cholinergic receptors: an in vivo electrophysiological study in the rat. Br J Pharmacol 1998, 124:455-464.
35. Gronier B., Perry K.W., Rasmussen K. Activation of the mesocorticolimbic dopaminergic system by stimulation of muscarinic cholinergic receptors in the ventral tegmental area. Psychopharmacology (Berl) 2000, 147:347-355.
36. Harte S.E., Spuz C.A., Borszcz G.S. Functional interaction between the medial thalamus and the rostral anterior cingulate cortex in the suppression of pain affect. Neuroscience 2011, 172:460-473.
37. Harte S.E., Lagman A.L., Borszcz G.S. Antinociceptive effects of morphine injected into the nucleus parafascicularis thalami of the rat. Brain Res 2000, 874:78-86.
38. Harte S.E., Hoot M.R., Borszcz G.S. Involvement of the intralaminar parafascicular nucleus in muscarinic-induced antinociception in rats. Brain Res 2004, 1019:152-161.
39. Himmelsbach C.K. Studies of the addiction liability of "demerol" (D-140). J Pharmacol Exp Ther 1942, 75:64-68.
40. Hitchcott P.K., Phillips G.D. Effects of intra-amygdala R(+) 7-OH-DPAT on intra-accumbens d-amphetamine-associated learning. I. Pavlovian conditioning. Psychopharmacology (Berl) 1998, 140:300-309.
41. Hnasko T.S., Hjelmstad G.O., Fields H.L., Edwards R.H. Ventral tegmental area glutamate neurons: electrophysiological properties and projections. J Neurosci 2012, 32:15076-15085.
42. Hoffmeister F. Effects of psychotropic drugs on pain. Pain 1968, 309-319. Academic Press, New York. A. Soulariarc, J. Cahn, J. Charpentier (Eds.).
43. Ikemoto S., Wise R.A. Rewarding effects of the cholinergic agents carbachol and neostigmine in the posterior ventral tegmental area. J Neurosci 2002, 22:9895-9904.
44. Kender R.G., Harte S.E., Munn E.M., Borszcz G.S. Affective analgesia following muscarinic activation of the ventral tegmental area in rats. J Pain 2008, 9:597-605.
45. Kirouac G.J., Li S., Mabrouk G. GABAergic projection from the ventral tegmental area and substantia nigra to the periaqueductal gray region and the dorsal raphe nucleus. J Comp Neurol 2004, 469:170-184.
46. Kiyatkin E.A. Dopamine in the nucleus accumbens: cellular actions, drug- and behavior-associated fluctuations, and a possible role in an organism's adaptive activity. Behav Brain Res 2002, 137:27-46.
47. Koob G.F., Volkow N.D. Neurocircuitry of addiction. Neuropsychopharmacology 2010, 35:217-238.
48. Kulkarni B., Bentley D.E., Elliott R., Youell P., Watson A., Derbyshire S.W., Frackowiak R.S., Friston K.J., Jones A.K. Attention to pain localization and unpleasantness discriminates the functions of the medial and lateral pain systems. Eur J Neurosci 2005, 21:3133-3142.
49. LaBuda C.J., Fuchs P.N. Attenuation of negative pain affect produced by unilateral spinal nerve injury in the rat following anterior cingulate cortex activation. Neuroscience 2005, 136:311-322.
50. Lacey M.G., Calabresi P., North R.A. Muscarine depolarizes rat substantia nigra zona compacta and ventral tegmental neurons in vitro through M1-like receptors. J Pharmacol Exp Ther 1990, 253:395-400.
51. Lester D.B., Miller A.D., Blaha C.D. Muscarinic receptor blockade in the ventral tegmental area attenuates cocaine enhancement of laterodorsal tegmentum stimulation-evoked accumbens dopamine efflux in the mouse. Synapse 2010, 64:216-223.
52. Loeser J.D. Pain and suffering. Clin J Pain 2000, 16:S2-S6.
53. Lopez-Avila A., Coffeen U., Ortega-Legaspi J.M., del Angel R., Pellicer F. Dopamine and NMDA systems modulate long-term nociception in the rat anterior cingulate cortex. Pain 2004, 111:136-143.
54. Marcangione C., Rompre P.P. Topographical Fos induction within the ventral midbrain and projection sites following self-stimulation of the posterior mesencephalon. Neuroscience 2008, 154:1227-1241.
55. Mark V.H., Ervin F.R., Yakovlev P.I. Correlation of pain relief, sensory loss, and anatomical lesion sites in pain patients treated with stereotactic thalamotomy. Trans Am Neurol Assoc 1961, 86:86-90.
56. May E.L. The chemistry of drugs of addiction. Am J Med 1953, 14:540-545.
57. Miller A.D., Forster G.L., Yeomans J.S., Blaha C.D. Midbrain muscarinic receptors modulate morphine-induced accumbal and striatal dopamine efflux in the rat. Neuroscience 2005, 136:531-538.
58. Moore R.Y., Bloom F.E. Central catecholamine neuron systems: anatomy and physiology of the dopamine systems. Annu Rev Neurosci 1978, 1:129-169.
59. Munn E.M., Harte S.E., Lagman A., Borszcz G.S. Contribution of the periaqueductal gray to the suppression of pain affect produced by administration of morphine into the intralaminar thalamus of rat. J Pain 2009, 10:426-435.
60. Nair-Roberts R.G., Chatelain-Badie S.D., Benson E., White-Cooper H., Bolam J.P., Ungless M.A. Stereological estimates of dopaminergic, GABAergic and glutamatergic neurons in the ventral tegmental area, substantia nigra and retrorubral field in the rat. Neuroscience 2008, 152:1024-1031.
61. Nandigama P., Borszcz G.S. Affective analgesia following the administration of morphine into the amygdala of rats. Brain Res 2003, 959:343-354.
62. National Institute on Drug Abuse (2011) Topics in brief: prescription drug abuse. A research update from the National Institute on Drug Abuse. http://www.drugabuse.gov/publications/topics-in-brief/prescription-drug-abuse.
63. Navratilova E., Xie J.Y., Okun A., Qu C., Eyde N., Ci S., Ossipov M.H., King T., Fields H.L., Porreca F. Pain relief produces negative reinforcement through activation of mesolimbic reward-valuation circuitry. Proc Natl Acad Sci U S A 2012, 109:20709-20713.
64. Nisell M., Nomikos G.G., Svensson T.H. Systemic nicotine-induced dopamine release in the rat nucleus accumbens is regulated by nicotinic receptors in the ventral tegmental area. Synapse 1994, 16:36-44.
65. Oades R.D., Halliday G.M. Ventral tegmental (A10) system: neurobiology. 1. Anatomy and connectivity. Brain Res 1987, 434:117-165.
66. Oberst F.W., Reichard J.D., Lee L.E., Clark B.B., Himmelsbach C.K. Symposium: can the euphoric, analgetic and physical dependence of drugs be separated?. FASEB 1943, 187-203.
67. Omelchenko N., Sesack S.R. Laterodorsal tegmental projections to identified cell populations in the rat ventral tegmental area. J Comp Neurol 2005, 483:217-235.
68. Omelchenko N., Sesack S.R. Cholinergic axons in the rat ventral tegmental area synapse preferentially onto mesoaccumbens dopamine neurons. J Comp Neurol 2006, 494:863-875.
69. Paladini C.A., Williams J.T. Noradrenergic inhibition of midbrain dopamine neurons. J Neurosci 2004, 24:4568-4575.
70. Pavlovic Z.W., Bodnar R.J. Opioid supraspinal analgesic synergy between the amygdala and periaqueductal gray in rats. Brain Res 1998, 779:158-169.
71. Paxinos G., Watson C. The rat brain in stereotaxic coordinates 1998, Academic Press, New York. 4th ed.
72. Paxinos G., Watson C. The rat brain in stereotaxic coordinates 2007, Academic Press, New York. 6th ed.
73. Pons S., Fattore L., Cossu G., Tolu S., Porcu E., McIntosh J.M., Changeux J.P., Maskos U., Fratta W. Crucial role of alpha4 and alpha6 nicotinic acetylcholine receptor subunits from ventral tegmental area in systemic nicotine self-administration. J Neurosci 2008, 28:12318-12327.
74. Price D.D., Von der Gruen A., Miller J., Rafii A., Price C. A psychophysical analysis of morphine analgesia. Pain 1985, 22:261-269.
75. Rada P.V., Mark G.P., Yeomans J.J., Hoebel B.G. Acetylcholine release in ventral tegmental area by hypothalamic self-stimulation, eating, and drinking. Pharmacol Biochem Behav 2000, 65:375-379.
76. Rezayof A., Nazari-Serenjeh F., Zarrindast M.R., Sepehri H., Delphi L. Morphine-induced place preference: involvement of cholinergic receptors of the ventral tegmental area. Eur J Pharmacol 2007, 562:92-102.
77. Schultz W. Multiple reward signals in the brain. Nat Rev Neurosci 2000, 1:199-207.
78. Scott D.J., Stohler C.S., Egnatuk C.M., Wang H., Koeppe R.A., Zubieta J.K. Placebo and nocebo effects are defined by opposite opioid and dopaminergic responses. Arch Gen Psychiatry 2008, 65:220-231.
79. Shyu B.C., Kiritsy-Roy J.A., Morrow T.J., Casey K.L. Neurophysiological, pharmacological and behavioral evidence for medial thalamic mediation of cocaine-induced dopaminergic analgesia. Brain Res 1992, 572:216-223.
80. Smith K.S., Berridge K.C. The ventral pallidum and hedonic reward: neurochemical maps of sucrose "liking" and food intake. J Neurosci 2005, 25:8637-8649.
81. Spender J.K. Remarks on "Analgesics". Br Med J 1887, 1:819-822.
82. Spuz C.A., Borszcz G.S. NMDA or non-NMDA receptor antagonism within the amygdaloid central nucleus suppresses the affective dimension of pain in rats: evidence for hemispheric synergy. J Pain 2012, 13:328-337.
83. Substance Abuse and Mental Health Services Administration (2011) Results from the 2010 National Survey on Drug Use and Health: Summary of National Findings. NSDUH:Series H-41.
84. Sulzer D., Rayport S. Dale's principle and glutamate corelease from ventral midbrain dopamine neurons. Amino Acids 2000, 19:45-52.
85. Swanson L.W. The projections of the ventral tegmental area and adjacent regions: a combined fluorescent retrograde tracer and immunofluorescence study in the rat. Brain Res Bull 1982, 9:321-353.
86. Sweet W.H. Central mechanisms of chronic pain (neuralgias and certain other neurogenic pain). Pain 1980, 287-303. Raven Press, New York. J.J. Bonica (Ed.).
87. Trudeau L.E. Glutamate co-transmission as an emerging concept in monoamine neuron function. J Psychiatry Neurosci 2004, 29:296-310.
88. UK Ministry of Health Morphine and heroin addiction: Departmental Committee's Report. Br Med J 1926, 1:391-393.
89. Van Bockstaele E.J., Pickel V.M. GABA-containing neurons in the ventral tegmental area project to the nucleus accumbens in rat brain. Brain Res 1995, 682:215-221.
90. Volkow N.D., Wang G.J., Ma Y., Fowler J.S., Wong C., Ding Y.S., Hitzemann R., Swanson J.M., Kalivas P. Activation of orbital and medial prefrontal cortex by methylphenidate in cocaine-addicted subjects but not in controls: relevance to addiction. J Neurosci 2005, 25:3932-3939.
91. Weigel R., Krauss J.K. Center median-parafascicular complex and pain control. Review from a neurosurgical perspective. Stereotact Funct Neurosurg 2004, 82:115-126.
92. Westerink B.H., Kwint H.F., deVries J.B. The pharmacology of mesolimbic dopamine neurons: a dual-probe microdialysis study in the ventral tegmental area and nucleus accumbens of the rat brain. J Neurosci 1996, 16:2605-2611.
93. Wise R.A. Dopamine, learning and motivation. Nat Rev Neurosci 2004, 5:483-494.
94. Xavier L.L., Viola G.G., Ferraz A.C., Da Cunha C., Deonizio J.M., Netto C.A., Achaval M. A simple and fast densitometric method for the analysis of tyrosine hydroxylase immunoreactivity in the substantia nigra pars compacta and in the ventral tegmental area. Brain Res Brain Res Protoc 2005, 16:58-64.
95. Xia Y., Driscoll J.R., Wilbrecht L., Margolis E.B., Fields H.L., Hjelmstad G.O. Nucleus accumbens medium spiny neurons target non-dopaminergic neurons in the ventral tegmental area. J Neurosci 2011, 31:7811-7816.
96. Yeomans J., Baptista M. Both nicotinic and muscarinic receptors in ventral tegmental area contribute to brain-stimulation reward. Pharmacol Biochem Behav 1997, 57:915-921.
97. Yeomans J., Forster G., Blaha C. M5 muscarinic receptors are needed for slow activation of dopamine neurons and for rewarding brain stimulation. Life Sci 2001, 68:2449-2456.
98. Yeomans J.S., Kofman O., McFarlane V. Cholinergic involvement in lateral hypothalamic rewarding brain stimulation. Brain Res 1985, 329:19-26.
99. Yeomans J.S., Takeuchi J., Baptista M., Flynn D.D., Lepik K., Nobrega J., Fulton J., Ralph M.R. Brain-stimulation reward thresholds raised by an antisense oligonucleotide for the M5 muscarinic receptor infused near dopamine cells. J Neurosci 2000, 20:8861-8867.
100. You Z.B., Wang B., Zitzman D., Wise R.A. Acetylcholine release in the mesocorticolimbic dopamine system during cocaine seeking: conditioned and unconditioned contributions to reward and motivation. J Neurosci 2008, 28:9021-9029.
101. Zhang L., Liu Y., Chen X. Carbachol induces burst firing of dopamine cells in the ventral tegmental area by promoting calcium entry through L-type channels in the rat. J Physiol 2005, 568:469-481.
102. Zubieta J.K., Smith Y.R., Bueller J.A., Xu Y., Kilbourn M.R., Jewett D.M., Meyer C.R., Koeppe R.A., Stohler C.S. Regional mu opioid receptor regulation of sensory and affective dimensions of pain. Science 2001, 293:311-315.