Alteration of c-Fos mRNA in the accessory lobe of crayfish is associated with a conditioned-cocaine induced reward

Neuroscience Research

Volumn 72, Issue 3, 2012, Pages 243-256

  Nathaniel, Thomas I ^a   Panksepp, Jaak ^b   Huber, Robert ^c  

^a UNIVERSITY OF SOUTH CAROLINA SCHOOL OF MEDICINE GREENVILLE   (United States)

^b WASHINGTON STATE UNIVERSITY   (United States)

^c BOWLING GREEN STATE UNIVERSITY   (United States)

Author keywords

Accessory lobes; C Fos mRNA; Cocaine; Crayfish; Neuroanatomy; Reward

Indexed keywords

COCAINE; MESSENGER RNA; PROTEIN C FOS; SODIUM CHLORIDE;

ANIMAL EXPERIMENT; ARTICLE; BEHAVIOR; CONTROLLED STUDY; CRAYFISH; LOCOMOTION; MALE; NONHUMAN; PLACE PREFERENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REWARD; STIMULUS;

ANIMALS; ASTACOIDEA; BEHAVIOR, ANIMAL; BRAIN; COCAINE; CONDITIONING (PSYCHOLOGY); MALE; MOTOR ACTIVITY; PROTO-ONCOGENE PROTEINS C-FOS; REWARD;

EID: 84856529195     PISSN: 01680102     EISSN: 18728111     Source Type: Journal    
DOI: 10.1016/j.neures.2011.11.009     Document Type: Article

References (90)

1. Alberstadt P.L., Steele C.W., Skinner C. Cover seeking behavior in juvenile and adult crayfish, Orconectes rusticus effects of darkness and thigmotactic cues. J. Crust. Biol. 1995, 15:537-541.
2. Andretic R., Chaney S., Hirsh J. Requirement of circadian genes for cocaine sensitization in Drosophila. Science 1999, 285:1066-1068.
3. Badiani A., Oates M.M., Day H.E.W., Watson S.J., Akil H., Robinson T.E. Amphetamine-induced behavior, dopamine release, and c-fos mRNA expression: modulation by environmental novelty. J. Neurosci. 1998, 18:10579-10593.
4. Badiani A., Oates M.M., Day H.E.W., Watson S.J., Akil H., Robinson T.E. Environmental modulation of amphetamine-induced c-fos expression in D1 versus D2 striatal neurons. Behav. Brain Res. 1999, 103:203-209.
5. Baird H.P., Patullo B.W., Macmillan D.L. Reducing aggression between freshwater crayfish (Cherax destructor Clark: Decapoda, Parastacidae) by increasing habitat complexity. Aquac. Res. 2006, 37:1419-1428.
6. Basil J., Sandeman D. Crayfish (Cherax destructor) use tactile cues to detect and learn topographical changes in their environment. Ethology 2000, 106:247-259.
7. Beckmann A.M., Wilce P.A. Egr transcription factors in the nervous system. Neurochem. Int. 1997, 31:477-510.
8. Beltz B.S. Distribution and functional anatomy of amine-containing neurons in decapod crustaceans. Microsc. Res. Technol. 1999, 44:105-120.
9. Benton J., Huber R., Ruchhoeft M., Helluy S., Beltz B. Serotonin depletion by 5,7-dihydroxytryptamine alters deutocerebral development in the lobster, Homarus americanus. J. Neurobiol. 1997, 33:357-373.
10. Berridge K.C., Robinson T.E. What is the role of dopamine in reward: hedonic impact, reward learning, or incentive salience. Brain Res. Rev. 1998, 28:309-369.
11. Brown E.E., Robertson G.S., Fibiger H.C. Evidence for conditional neuronal activation following exposure to a cocaine-paired environment: role of forebrain limbic structures. J. Neurosci. 1992, 12:4112-4121.
12. Brown E.E., Robertson G.S., Fibiger H.C. Evidence for conditional neuronal activation following exposure to a cocaine-paired environment-role of forebrain limbic structures. J. Neurosci. 1992, 12:4112-4121.
13. Carr K.D. The physiology of opiate hedonic effects and the role of opioids in motivated behavior. Adv Alcohol Subst Abuse 1984, 3:5-18.
14. Chocyk A., Czyrak A., Wedzony K. Acute and repeated cocaine induces alterations in FosB/DeltaFosB expression in the paraventricular nucleus of the hypothalamus. Brain Res. 2006, 1090:58-68.
15. Ciccocioppo R., Sanna P.P., Weiss F. Cocaine-predictive stimulus induces drug-seeking behavior and neural activation in limbic brain regions after multiple months of abstinence: reversal by D(1) antagonists. Proc. Natl. Acad. Sci. U.S.A. 2001, 98:1976-1981.
16. Crisp K.M., Mesce K.A. Beyond the central pattern generator: amine modulation of decision-making neural pathways descending from the brain of the medicinal leech. J. Exp. Biol. 2006, 209:1746-1756.
17. Curran E.J., Akil H., Watson S.J. 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. 1996, 21:1425-1435.
18. Curran T., Bravo R., Muller R. Transient induction of c-fos and c-myc in an immediate consequence of growth factor stimulation. Cancer Surv. 1985, 4:655-681.
19. Dziopa L., Imeh-Nathaniel A., Baeir D., Kiel M., Sameera S., Beatriz V., Nathaniel I.T. Morphine-conditioned cue alters c-Fos protein expression in the brain of crayfish. Brain Res. Bull. 2011, 85:385-395.
20. Franklin T.R., Druhan J.P. The retrograde tracer fluoro-gold interferes with the expression of fos-related antigens. J. Neurosci. Meth. 2000, 98:1-8.
21. Freet C.S., Steffen C., Nestler E.J., Grigson P.S. Overexpression of delta FosB is associated with attenuated cocaine-induced suppression of saccharin intake in mice. Behav. Neurosci. 2009, 123:397-407.
22. Furshpan E.J., Potter D.D. Transmission at the giant motor synapses of the crayfish. J. Physiol. 1959, 145:289-325.
23. Granados-Dominguez M., Escamilla-Chimal E.G., Fanjul-Moles M.L. Photic regulation of c-Fos expression in the protocerebrum of crayfish. Biol. Rhythm Res. 2005, 36:15-22.
24. Guan X.W., Hu J., Li S.N. Involvement of extracellular signal-regulated protein kinase in acute cocaine-induced c-fos in nucleus accumbens. Neurosci. Lett. 2008, 438:155-158.
25. Herberholz J., Marjorie M., Edwards D.H. Escape behavior and escape circuit activation in juvenile crayfish during prey-predator interactions. J. Exp. Biol. 2004, 207:1855-1863.
26. Hoffman G.E., Lyo D. Anatomical markers of activity in neuroendocrine systems: are we all 'Fos-ed out'?. J. Neuroendocrinol. 2002, 14:259-268.
27. Hope B.T., Simmons D.E., Mitchell T.B., Kreuter J.D., Mattson B.J. Cocaine-induced locomotor activity and Fos expression in nucleus accumbens are sensitized for 6 months after repeated cocaine administration outside the home cage. Eur. J. Neurosci. 2006, 24:867-875.
28. Hotsenpiller G., Horak B.T., Wolf M.E. Dissociation of conditioned locomotion and Fos induction in response to stimuli formerly paired with cocaine. Behav. Neurosci. 2002, 116:634-645.
29. Huber R., Delago A. Serotonin alters decisions to withdraw in fighting crayfish, Astacus astacus: the motivational concept revisited. 1998. J. Comp. Physiol. A 1998, 182:573-583.
30. Hughes P., Dragunow D. Induction of immediate-early genes and the control of neurotransmitter-regulated gene expression within the nervous system. Pharmacol. Rev. 1995, 47:133-178.
31. Hyman S.E., Kosofsky B.E., Nguyen T.V., Cohen B.M., Comb M.J. Everything activates c-fos--how can it matter?. NIDA Res. Monogr. 1993, 125:25-37.
32. Ikemoto S., Panksepp J. The role of nucleus accumbens dopamine in motivated behavior: a unifying interpretation with special reference to reward-seeking. Brain Res. Rev. 1999, 31:6-41.
33. Ilona C.K., Paul R.E., Barbara S.K., Alison R.M. Distribution of dopamine receptors and dopamine receptor homologs in the brain of the honey bee Apis mellifera L. Microsc. Res. Technol. 1999, 44:2-3.
34. Iverson L.L., Mitchel J.F., Srinivason V. The release of y-aminobutyric acid during inhibition in the cat visual cortex. J. Physiol. 1971, 212:519-534.
35. Kalivas P.W., McFarland K. Brain circuitry and the reinstatement of cocaine-seeking behavior. Psychopharmacology 2003, 168:44-56.
36. Kalivas P.W., Volkow N.D. The neural basis of addiction: a pathology of motivation and choice. Am. J. Psychiat. 2005, 162:1403-2141.
37. Kaun K.R., Azanchi R., Maung Z., Hirsh J., Heberlein U. Drosophila model for alcohol reward. Nat. Neurosci. 2011, 14:612-619.
38. Kravitz E.A., Kuffler S.W., Potter D.D. Synaptic chemistry in single neurons: GABA is identified as an inhibitory neurotransmitter. J. Neurophysiol. 1963, 26:739-751.
39. Kravitz E.A. Hormonal control of behavior: amines and the biasing of behavioral output in lobsters. Science 1988, 241:1775-1781.
40. Kufahl P.R., Zavala A.R., Singh A., Thiel K.J., Dickey E.D., Joyce J.N., Neisewander J.L. c-Fos expression associated with reinstatement of cocaine-seeking behavior by response-contingent conditioned cues. Synapse 2009, 63:823-835.
41. Marchant N.J., Furlong T.M., McNally G.P. Medial dorsal hypothalamus mediates the inhibition of reward seeking after extinction. J. Neurosci. 2010, 30:14102-14115.
42. Marinelli M., Barrot M., Simon H., Oberlander C., Dekeyne A., Le Moal M., Alvarez R.A. Pharmacological stimuli decreasing nucleus accumbens dopamine can act as positive reinforcers but have a low addictive potential. Eur. J. Neurosci. 1998, 10:3269-3275.
43. Martin-Iverson M.T., Reimer A.R. Classically conditioned motor effects do not occur with cocaine in an unbiased conditioned place preferences procedure. Behav. Pharmacol. 1996, 7:303-314.
44. McClung C., Hirsh J. Stereotypical behavioral responses to free-base cocaine and the development of behavioral sensitization in Drosophila. Curr. Biol. 1998, 8:109-112.
45. McGillis J.P., Miller C.N., Schneider D.B., Fernandez S., Knopf M. Calcitonin gene-related peptide induces AP-1 activity by a PKA and c-fos-dependent mechanism in pre-B cells. J. Neuroimmunol. 2002, 123:83-90.
46. Miller C.A., Marshall J.F. Altered prelimbic cortex output during cue-elicited drug seeking. J. Neurosci. Meth. 2004, 24:6889-6897.
47. Morgan J.I., Urran T. Stimulus-transcription coupling in the nervous system. Annu. Rev. Neurosci. 1991, 14:421-452.
48. Nathaniel T.I., Panksepp J., Huber R. Drug-seeking behavior in an invertebrate system: Evidence of morphine-induced reward, extinction and reinstatement in crayfish. Behav. Brain Res. 2009, 197:331-338.
49. Nathaniel T.I., Panksepp J., Huber R. Effects of a single and repeated morphine treatment on conditioned and unconditioned behavioral sensitization in Crayfish. Behav. Brain Res. 2010, 207:310-320.
50. Neisewander J.L., Baker D.A., Fuchs R.A., Tran-Nguyen L.T.L., Palmer A.J., Marshall J.F. Fos protein expression and cocaine-seeking behavior in rats after exposure to a cocaine self-administration environment. J. Neurosci. 2000, 20:798-805.
51. Norris B.J., Coleman M.J., Nusbaum M.P. Recruitment of a projection neuron determines gastric mill motor pattern selection in the stomatogastric nervous system of the crab, Cancer borealis. J. Neurophysiol. 1994, 72:1451-1463.
52. Ons S., Rotllant D., Marín-Blasco I.J., Armario A. Immediate-early gene response to repeated immobilization: Fos protein and arc mRNA levels appear to be less sensitive than c-fos mRNA to adaptation. Eur. J. Neurosci. 2010, 31:2043-2052.
53. Otsuka M., Kravitz E.A., Potter D.D. Physiological and chemical architecture of a lobster ganglion with particular reference to gamma-aminobutyrate and glutamate. J. Neurophysiol. 1967, 30:725-752.
54. Panksepp, J., 1998. Affective neuroscience. The foundations of human and animal emotions, Oxford University Press, New York.
55. Panksepp J., Huber R. Long-term changes in serotonin function: dynamic neurochemical properties in agonistic behavior of the Crayfish Orconectes rusticus. J. Neurobiol. 2004, 50:276-290.
56. Panksepp J.B., Yue Z., Drerup C., Huber R. Amine neurochemistry and aggression in crayfish. Microsc. Res. Techn. 2003, 60:360-368.
57. Panksepp J.B., Huber R. Ethological analyses of crayfish behavior: a new invertebrate system for measuring the rewarding properties of psychostimulants. Behav. Brain Res. 2004, 153:171-180.
58. Partridge B., Schenk S. Context-independent sensitization to the locomotor-activating effects of cocaine. Pharmacol. Biochem. Behav. 1999, 63:543-548.
59. Perrotti L.I., Hadeishi Y., Ulery P.G., Barrot M., Monteggia L., Duman R.S., Nestler E.J. Induction of deltaFosB in reward-related brain structures after chronic stress. J. Neurosci. 2004, 24:10594-10602.
60. Polanska M.A., Yasuda A., Harzsch S. Immunolocalisation of crustacean-SIFamide in the median brain and eyestalk neuropils of the marbled crayfish. Cell Tissue Res. 2007, 330:331-344.
61. Porzgen P., Park S.K., Hirsh J., Sonders M.S., Amara S.G. The antidepressant-sensitive dopamine transporter in Drosophila melanogaster: a primordial carrier for catecholamines. Molec Pharmacol. 2001, 59:83-95.
62. Robinson T.E., Berridge K.C. The neural basis of drug craving-an incentive-sensitization theory of addiction. Brain Res. Rev. 1993, 18:247-291.
63. Robinson T.E., Berridge K.C. The incentive sensitization theory of addiction: some current issues. Phil. Trans. Roy. Soc. B-Biol. Sci. 2008, 363:3137-3146.
64. Sandeman D., Sandeman R., Derby C., Schmidt M. Morphology of the brain of crayfish, crabs, and spiny lobsters: a common nomenclature for homologous structures. Biol. Bull. 1992, 183:304-326.
65. Sandeman D., Beltz B., Sandeman R. Crayfish brain interneurons that converge with serotonin giant cells in accessory lobe glomeruli. J. Comp. Neurol. 1995, 352:263-279.
66. Schiller M., Bohm M., Dennler S., Ehrchen J.M., Mauviel A. Mitogen- and stress-activated protein kinase 1 is critical for interleukin-1-induced, CREB-mediated, c-fos gene expression in keratinocytes. Oncogene 2006, 25:4449-4457.
67. Schultz W. Dopamine neurons and their role in reward mechanisms. Curr. Opin. Neurobiol. 1997, 7:191-197.
68. Seymour C.M., Wagner J.J. Simultaneous expression of cocaine-induced behavioral sensitization and conditioned place preference in individual rats. Brain Res. 2005, 5:57-68.
69. Shohamy D., Myers C.E., Kalanithi J., Gluck M.A. Basal ganglia and dopamine contributions to probabilistic category learning. Neurosci. Biobehav. Rev. 2007, 12:3-134.
70. Slattery D., Morrow J.A., Hudson A.L., Hill D.R., Nutt D.J., Henry B. Comparison of alterations in c-fos and Egr-1 (zif268) expression throughout the rat brain following acute administration of different classes of antidepressant compounds. Neuropsychopharmacology 2005, 30:1278-1287.
71. Sullivan J.M., Beltz B.S. Development and connectivity of olfactory pathways in the brain of the lobster Homarus americanus. J. Comp. Neurol. 2001, 441:23-43.
72. Sullivan J.M., Beltz B.S. Newborn cells in the adult crayfish brain differentiate into distinct neuronal types. J. Neurobiol. 2005, 65:157-170.
73. Sullivan J.M., Beltz B.S. Integration and segregation of inputs to higher-order neuropils of the crayfish brain. J. Comp. Neurol. 2005, 48:118-126.
74. Tassin J.P. Role of dopamine in drug dependence processes. Bull. Acad. Natl. Med. 2002, 186:295-304.
75. Teegarden S.L., Nestler E.J., Bale T.L. Delta FosB-mediated alterations in dopamine signaling are normalized by a palatable high-fat diet. Biol. Psychiatry 2008, 64:941-950.
76. Thiel K.J., Okun A.C., Neisewander J.L. Social reward-conditioned place preference: a model revealing an interaction between cocaine and social context rewards in rats. Drug Alcohol Depend. 2008, 96:202-212.
77. Thiel K.J., Sanabria F., Neisewander J.L. Synergistic interaction between nicotine and social rewards in adolescent male rats. Psychopharmacology (Berl) 2009, 204:391-402.
78. Tierney A.N., Kim T., Abrams R. Dopamine in crayfish and other crustaceans: distribution in the central nervous system and physiological functions. Microsc. Res. Techn. 2003, 60:325-335.
79. Tricarico E., Gherardia F. Biogenic amines influence aggressiveness in crayfish but not their force or hierarchical rank. Anim. Behav. 2007, 74:1715-1724.
80. Velázquez-Sánchez C., Ferragud A., Hernández-Rabaza V., Nácher A., Merino V., Cardá M., Murga J., Canales J. NMDA antagonist and antipsychotic actions in cortico-subcortical circuits. Neurotox. Res. 2008, 14:129-140.
81. Velázquez-Sánchez C., Ferragud A., Hernández-Rabaza V., Nácher A., Merino V., Cardá M., Murga J., Canales J.J. The dopamine uptake inhibitor 3 alpha-[bis(4'-fluorophenyl)metoxy]-tropane reduces cocaine-induced early-gene expression, locomotor activity, and conditioned reward. Neuropsychopharmacology 2009, 34:2497-2507.
82. Wachowiak M., Diebel C.E., Ache B.W. Functional organization of olfactory processing in the accessory lobe of the spiny lobster. J. Comp. Physiol. A 1996, 178:211-226.
83. Watanabe H., Henriksson R., Ohnishi Y.N., Ohnishi Y.H., Harper C., Sheedy D., Garrick T., Nyberg F., Nestler E.J., Bakalkin G., Yakovleva T. FOSB proteins in the orbitofrontal and dorsolateral prefrontal cortices of human alcoholics. Addict. Biol. 2009, 14:294-297.
84. Wolf F.W., Heberlein U. Invertebrate models of drug abuse. J. Neurobiol. 2003, 54:161-178.
85. Xu M. c-Fos is an intracellular regulator of cocaine-induced long-term changes. Ann. N Y Acad. Sci. 2008, 1139:1-9.
86. Yamada H., Kuroki T., Nakahara T., Hashimoto K., Tsutsumi T., Hirano M., Maeda H. The dopamine D1 receptor agonist, but not the D2 receptor agonist, induces gene expression of Homer 1a in rat striatum and nucleus accumbens. Brain Res. 2007, 1131:88-96.
87. Zangenehpour S., Chaudhuri A. Differential induction and decay curves of c-fos and zif268 revealed through dual activity maps. Mol. Brain Res. 2002, 109:221-225.
88. Zavala A.R., Biswas S., Harlan R.E., Neisewander J.L. Fos and glutamate AMPA receptor subunit coexpression associated with cue-elicited cocaine-seeking behavior in abstinent rats. Neuroscience 2007, 145:438-452.
89. Zavala A.R., Osredkar T., Joyce J.N., Neisewander J.L. Upregulation of Arc mRNA expression in the prefrontal cortex following cue-induced reinstatement of extinguished cocaine-seeking behavior. Synapse 2008, 62:421-431.
90. Zawilska J.B. Dopamine receptors-structure, characterization and function. Postepy Hig Med. Dosw. 2003, 57:293-322.