Morphine-induced c-fos mRNA expression in striatofugal circuits: Modulation by dose, environmental context, and drug history

Neuropsychopharmacology

Volumn 29, Issue 9, 2004, Pages 1664-1674

  Ferguson, Susan M ^a   Thomas, Mark J ^b   Robinson, Terry E ^a,c  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF MINNESOTA   (United States)

^c UNIVERSITY OF MICHIGAN   (United States)

Author keywords

Caudate nucleus; Cingulate cortex; Dopamine; Immediate early genes; In situ hybridization; Rats

Indexed keywords

MORPHINE; PROTEIN C FOS;

ANIMAL EXPERIMENT; ARTICLE; CELL DENSITY; CINGULATE GYRUS; CONTROLLED STUDY; CORPUS STRIATUM; DRUG DEPENDENCE; GLOBUS PALLIDUS; MALE; NERVE CELL NETWORK; NIGRONEOSTRIATAL SYSTEM; NONHUMAN; PRIORITY JOURNAL; RAT; STRIATOFUGAL CIRCUIT;

ANALGESICS, OPIOID; ANIMALS; DOSE-RESPONSE RELATIONSHIP, DRUG; ENVIRONMENT; GENE EXPRESSION; GENES, FOS; GLOBUS PALLIDUS; HISTOCYTOCHEMISTRY; IN SITU HYBRIDIZATION; MALE; MORPHINE; MOTOR ACTIVITY; NEOSTRIATUM; NEURAL PATHWAYS; RATS; RATS, SPRAGUE-DAWLEY; RNA, MESSENGER;

EID: 3242685661     PISSN: 0893133X     EISSN: None     Source Type: Journal    
DOI: 10.1038/sj.npp.1300465     Document Type: Article

References (62)

1. Albin RL, Young AB, Penney JB (1989). The functional anatomy of basal ganglia disorders. Trends Neurosci 12: 366-375.
2. Badiani A, Anagnostaras SG, Robinson TE (1995b). The development of sensitization to the psychomotor stimulant effects of amphetamine is enhanced in a novel environment. Psychopharmacology (Berl) 117: 443-452.
3. Badiani A, Browman KE, Robinson TE (1995a). Influence of novel versus home environments on sensitization to the psychomotor stimulant effects of cocaine and amphetamine. Brain Res 674: 291-298.
4. Badiani A, Oates MM, Day HE, Watson SJ, Akil H, Robinson TE (1998). Amphetamine-induced behavior, dopamine release, and c-fos mRNA expression: modulation by environmental novelty. J Neurosci 18: 10579-10593.
5. Badiani A, Oates MM, Day HE, Watson SJ, Akil H, Robinson TE (1999). Environmental modulation of amphetamine-induced c-fos expression in D1 versus D2 striatal neurons. Behav Brain Res 103: 203-209.
6. Badiani A, Oates MM, Robinson TE (2000). Modulation of morphine sensitization in the rat by contextual stimuli. Psychopharmacology (Berl) 151: 273-282.
7. Berretta S, Parthasarathy HB, Graybiel AM (1997). Local release of GABAergic inhibition in the motor cortex induces immediate-early gene expression in indirect pathway neurons of the striatum. J Neurosci 17: 4752-4763.
8. Berretta S, Robertson HA, Graybiel AM (1992). Dopamine and glutamate agonists stimulate neuron-specific expression of Fos-like protein in the striatum. J Neurophysiol 68: 767-777.
9. Bontempi B, Sharp FR (1997). Systemic morphine-induced Fos protein in the rat striatum and nucleus accumbens is regulated by mu opioid receptors in the substantia nigra and ventral tegmental area. J Neurosci 17: 8596-8612.
10. Cenci MA, Kalen P, Mandel RJ, Wictorin K, Bjorklund A (1992). Dopaminergic transplants normalize amphetamine- and apomorphine-induced Fos expression in the 6-hydroxydopamine-lesioned striatum. Neuroscience 46: 943-957.
11. Cole DG, Kobierski LA, Konradi C, Hyman SE (1994). 6-Hydroxydopamine lesions of rat substantia nigra up-regulate dopamine-induced phosphorylation of the cAMP-response element-binding protein in striatal neurons. Proc Natl Acad Sci USA 91: 9631-9635.
12. Curran EJ, Akil H, Watson SJ (1996). Psychomotor stimulant- and opiate-induced c-fos mRNA expression patterns in the rat forebrain: comparisons between acute drug treatment and a drug challenge in sensitized animals. Neurochem Res 21: 1425-1435.
13. Curran EJ, Watson Jr SJ (1995). Dopamine receptor mRNA expression patterns by opioid peptide cells in the nucleus accumbens of the rat: a double in situ hybridization study. J Comp Neurol 361: 57-76.
14. D'Souza DN, Harlan RE, Garcia MM (1999). Sexual dimorphism in the response to N-methyl-D-aspartate receptor antagonists and morphine on behavior and c-Fos induction in the rat brain. Neuroscience 93: 1539-1547.
15. Desole MS, Esposito G, Fresu L, Migheli R, Enrico P, Mura MA et al (1996). Effects of morphine treatment and withdrawal on striatal and limbic monoaminergic activity and ascorbic acid oxidation in the rat. Brain Res 723: 154-161.
16. Devine DP, Leone P, Pocock D, Wise RA (1993). Differential involvement of ventral tegmental mu, delta and kappa opioid receptors in modulation of basal mesolimbic dopamine release: in vivo microdialysis studies. J Pharmacol Exp Ther 266: 1236-1246.
17. Di Chiara G, North RA (1992). Neurobiology of opiate abuse. Trends Pharmacol Sci 13: 185-193.
18. Erdtmann-Vourliotis M, Mayer P, Linke R, Riechert U, Hollt V (1999b). Long-lasting sensitization towards morphine in motoric and limbic areas as determined by c-fos expression in rat brain. Brain Res Mol Brain Res 72: 1-16.
19. Erdtmann-Vourliotis M, Mayer P, Riechert U, Hollt V (1999a). Acute injection of drugs with low addictive potential (delta(9)-tetrahydrocannabinol, 3,4-methylenedioxymethamphetamine, lysergic acid diamide) causes a much higher c-fos expression in limbic brain areas than highly addicting drugs (cocaine and morphine). Brain Res Mol Brain Res 71: 313-324.
20. Ferguson SM, Norton CS, Watson SJ, Akil H, Robinson TE (2003). Amphetamine-evoked c-fos mRNA expression in the caudate-putamen: the effects of DA and NMDA receptor antagonists vary as a function of neuronal phenotype and environmental context. J Neurochem 86: 33-44.
21. Frankel PS, Garcia MM, Harlan RE (1999a). Infusion of beta-FNA into the thalamus attenuates morphine-induced c-Fos induction in the rat caudate putamen. Brain Res 838: 222-226.
22. Frankel PS, Harlan RE, Garcia MM (1999b). Chronic administration of morphine alters immediate-early gene expression in the forebrain of post-dependent rats. Brain Res 835: 204-212.
23. Garcia MM, Anderson AT, Edwards R, Harlan RE (2003). Morphine induction of c-fos expression in the rat forebrain through glutamatergic mechanisms: role of non-n-methyl-D-aspartate receptors. Neuroscience 119: 787-794.
24. Garcia MM, Brown HE, Harlan RE (1995). Alterations in immediate-early gene proteins in the rat forebrain induced by acute morphine injection. Brain Res 692: 23-40.
25. Garcia MM, Harlan RE (1997). Neurochemical characterization of cortical and striatal neurons expressing c-Fos protein after acute morphine administration. Soc Neurosci Abstr 23: 1107.
26. Gerfen CR (1992). The neostriatal mosaic: multiple levels of compartmental organization. Trends Neurosci 15: 133-139.
27. Gerfen CR, Engber TM, Mahan LC, Susel Z, Chase TN, Monsma Jr FJ et al (1990). D1 and D2 dopamine receptor-regulated gene expression of striatonigral and striatopallidal neurons. Science 250: 1429-1432.
28. Giacchino JL, Henriksen SJ (1996). Systemic morphine and local opioid effects on neuronal activity in the medial prefrontal cortex. Neuroscience 70: 941-949.
29. Giacchino JL, Henriksen SJ (1998). Opioid effects on activation of neurons in the medial prefrontal cortex. Prog Neuropsychopharmacol Biol Psychiatry 22: 1157-1178.
30. Girault JA, Barbeito L, Spampinato U, Gozlan H, Glowinski J, Besson MJ (1986). In vivo release of endogenous amino acids from the rat striatum: further evidence for a role of glutamate and aspartate in corticostriatal neurotransmission. J Neurochem 47: 98-106.
31. Gray AM, Rawls SM, Shippenberg TS, McGinty JF (1999). The kappa-opioid agonist, U-69593, decreases acute amphetamine-evoked behaviors and calcium-dependent dialysate levels of dopamine and glutamate in the ventral striatum. J Neurochem 73: 1066-1074.
32. Harlan RE, Garcia MM (1998). Drugs of abuse and immediate-early genes in the forebrain. Mol Neurobiol 16: 221-267.
33. Hyman SE, Malenka RC (2001). Addiction and the brain: the neurobiology of compulsion and its persistence. Nat Rev Neurosci 2: 695-703.
34. Jaber M, Cador M, Dumartin B, Normand E, Stinus L, Bloch B (1995). Acute and chronic amphetamine treatments differently regulate neuropeptide messenger RNA levels and Fos immunoreactivity in rat striatal neurons. Neuroscience 65: 1041-1050.
35. Johansson B, Lindstrom K, Fredholm BB (1994). Differences in the regional and cellular localization of c-fos messenger RNA induced by amphetamine, cocaine and caffeine in the rat. Neuroscience 59: 837-849.
36. Johnson SW, North RA (1992). Opioids excite dopamine neurons by hyperpolarization of local interneurons. J Neurosci 12: 483-488.
37. Konradi C, Cole RL, Heckers S, Hyman SE (1994). Amphetamine regulates gene expression in rat striatum via transcription factor CREB. J Neurosci 14: 5623-5634.
38. Konradi C, Leveque JC, Hyman SE (1996). Amphetamine and dopamine-induced immediate early gene expression in striatal neurons depends on postsynaptic NMDA receptors and calcium. J Neurosci 16: 4231-4239.
39. Liu J, Nickolenko J, Sharp FR (1994). Morphine induces c-fos and junB in striatum and nucleus accumbens via D1 and N-methyl-D-aspartate receptors. Proc Natl Acad Sci USA 91: 8537-8541.
40. Lovenberg TW, Nichols DE, Nestler EJ, Roth RH, Mailman RB (1991). Guanine nucleotide binding proteins and the regulation of cyclic AMP synthesis in NS20Y neuroblastoma cells: role of D1 dopamine and muscarinic receptors. Brain Res 556: 101-107.
41. Matthews RT, German DC (1984). Electrophysiological evidence for excitation of rat ventral tegmental area dopamine neurons by morphine. Neuroscience 11: 617-625.
42. Mayer P, Erdtmann-Vourliotis M, Riechert U, Ammon S, Hollt V (2002). Mild stress sensitizes the brain's response to morphine. Brain Res Mol Brain Res 104: 143-147.
43. McGeorge AJ, Faull RL (1989). The organization of the projection from the cerebral cortex to the striatum in the rat. Neuroscience 29: 503-537.
44. Nestler EJ, Hope BT, Widnell KL (1993). Drug addiction: a model for the molecular basis of neural plasticity. Neuron 11: 995-1006.
45. Nicol B, Rowbotham DJ, Lambert DG (1996). mu- and kappa-opioids inhibit K+ evoked glutamate release from rat cerebrocortical slices. Neurosci Lett 218: 79-82.
46. Ostrander MM, Badiani A, Day HE, Norton CS, Watson SJ, Akil H et al (2003). Environmental context and drug history modulate amphetamine-induced c-fos mRNA expression in the basal ganglia, central extended amygdala, and associated limbic forebrain. Neuroscience 120: 551-571.
47. Paolone G, Burdino R, Badiani A (2003). Dissociation in the modulatory effects of environmental novelty on the locomotor, analgesic, and eating response to acute and repeated morphine in the rat. Psychopharmacology (Berl) 166: 146-155.
48. Parthasarathy HB, Graybiel AM (1997). Cortically driven immediate-early gene expression reflects modular influence of sensorimotor cortex on identified striatal neurons in the squirrel monkey. J Neurosci 17: 2477-2491.
49. Paxinos G, Watson C (1998). The Rat Brain in Stereotaxic Coordinates, 4th edn. Academic: San Diego.
50. Reid MS, Hsu Jr K, Berger SP (1997). Cocaine and amphetamine preferentially stimulate glutamate release in the limbic system: studies on the involvement of dopamine. Synapse 27: 95-105.
51. Ruskin DN, Bergstrom DA, Mastropietro CW, Twery MJ, Walters JR (1999). Dopamine agonist-mediated rotation in rats with unilateral nigrostriatal lesions is not dependent on net inhibitions of rate in basal ganglia output nuclei. Neuroscience 91: 935-946.
52. Ruskin DN, Marshall JF (1994). Amphetamine- and cocaine-induced fos in the rat striatum depends on D2 dopamine receptor activation. Synapse 18: 233-240.
53. Sgambato V, Abo V, Rogard M, Besson MJ, Deniau JM (1997). Effect of electrical stimulation of the cerebral cortex on the expression of the Fos protein in the basal ganglia. Neuroscience 81: 93-112.
54. Sharp FR, Liu J, Nickolenko J, Bontempi B (1995). NMDA and D1 receptors mediate induction of c-fos and junB genes in striatum following morphine administration: implications for studies of memory. Behav Brain Res 66: 225-230.
55. Smith JA, Mo Q, Guo H, Kunko PM, Robinson SE (1995). Cocaine increases extraneuronal levels of aspartate and glutamate in the nucleus accumbens. Brain Res 683: 264-269.
56. Spanagel R, Herz A, Shippenberg TS (1992). Opposing tonically active endogenous opioid systems modulate the mesolimbic dopaminergic pathway. Proc Natl Acad Sci USA 89: 2046-2050.
57. Spencer HJ (1976). Antagonism of cortical excitation of striatal neurons by glutamic acid diethyl ester: evidence for glutamic acid as an excitatory transmitter in the rat striatum. Brain Res 102: 91-101.
58. Uslaner J, Badiani A, Norton CS, Day HE, Watson SJ, Akil H et al (2001). Amphetamine and cocaine induce different patterns of c-fos mRNA expression in the striatum and subthalamic nucleus depending on environmental context. Eur J Neurosci 13: 1977-1983.
59. Uslaner JM, Crombag HS, Ferguson SM, Robinson TE (2003a). Cocaine-induced psychomotor activity is associated with its ability to induce c-fos mRNA expression in the subthalamic nucleus: effects of dose and repeated treatment. Eur J Neurosci 17: 2180-2186.
60. Uslaner JM, Norton CS, Watson SJ, Akil H, Robinson TE (2003b). Amphetamine-induced c-fos mRNA expression in the caudate-putamen and subthalamic nucleus: interactions between dose, environment, and neuronal phenotype. J Neurochem 85: 105-114.
61. Waszczak BL, Martin L, Boucher N, Zahr N, Sikes RW, Stellar JR (2001). Electrophysiological and behavioral output of the rat basal ganglia after intrastriatal infusion of d-amphetamine: lack of support for the basal ganglia model. Brain Res 920: 170-182.
62. Waszczak BL, Martin LP, Finlay HE, Zahr N, Stellar JR (2002). Effects of individual and concurrent stimulation of striatal D1 and D2 dopamine receptors on electrophysiological and behavioral output from rat basal ganglia. J Pharmacol Exp Ther 300: 850-861.