Repeated amphetamine administration induces Fos in prefrontal cortical neurons that project to the lateral hypothalamus but not the nucleus accumbens or basolateral amygdala

Psychopharmacology

Volumn 197, Issue 2, 2008, Pages 179-189

  Morshedi, Maud M ^a   Meredith, Gloria E ^a  

^a ROSALIND FRANKLIN UNIVERSITY OF MEDICINE AND SCIENCE   (United States)

Author keywords

Addiction; Behavioral sensitization; Dopamine; Fluoro gold; Infralimbic cortex; Orexin; Prelimbic cortex; Psychostimulant; Reward

Indexed keywords

DEXAMPHETAMINE; FLUOROGOLD; OREXIN; PROTEIN FOS;

AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DRUG DOSE INCREASE; DRUG DOSE REDUCTION; DRUG EFFECT; IMMUNOHISTOCHEMISTRY; LATERAL HYPOTHALAMUS; MALE; NEUROCHEMISTRY; NONHUMAN; NUCLEUS ACCUMBENS; PREFRONTAL CORTEX; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN INDUCTION; PSYCHOPHARMACOLOGY; PYRAMIDAL NERVE CELL; RAT; REWARD;

AMPHETAMINE; AMYGDALA; ANIMALS; CENTRAL NERVOUS SYSTEM STIMULANTS; HYPOTHALAMIC AREA, LATERAL; IMAGE PROCESSING, COMPUTER-ASSISTED; IMMUNOHISTOCHEMISTRY; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MALE; MICROINJECTIONS; MOTOR ACTIVITY; NEURAL PATHWAYS; NEURONS; NEUROPEPTIDES; NUCLEUS ACCUMBENS; PERFUSION; PREFRONTAL CORTEX; PROTO-ONCOGENE PROTEINS C-FOS; PYRAMIDAL CELLS; RATS; RATS, SPRAGUE-DAWLEY; STILBAMIDINES;

EID: 40949119459     PISSN: 00333158     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00213-007-1021-7     Document Type: Article

References (78)

1. Ahmed SH, Lutjens R, van der Stap LD, Lekic D, Romano-Spica V, Morales M, Koob GF, Repunte-Canonigo V, Sanna PP (2005) Gene expression evidence for remodeling of lateral hypothalamic circuitry in cocaine addiction. Proc Natl Acad Sci USA 102:11533-8
2. Berod AM, Colussi-Mas J (2005) Afferent projections to the rat ventral tegmental area activated by a single exposure to amphetamine. Society for Neuroscience, Abstract Viewer/Itinerary Planner, Washington, DC
3. Borgland SL, Taha SA, Sarti F, Fields HL, Bonci A (2006) Orexin A in the VTA is critical for the induction of synaptic plasticity and behavioral sensitization to cocaine. Neuron 49:589-601
4. Brady AM, O'Donnell P (2004) Dopaminergic modulation of prefrontal cortical input to nucleus accumbens neurons in vivo. J Neurosci 24:1040-1049
5. Brown EE, Fibiger HC (1993) Differential effects of excitotoxic lesions of the amygdala on cocaine-induced conditioned locomotion and conditioned place preference. Psychopharmacology (Berl) 113:123-130
6. Cadoni C, Solinas M, Di Chiara G (2000) Psychostimulant sensitization: differential changes in accumbal shell and core dopamine. Eur J Pharmacol 388:69-76
7. Ciccocioppo R, Sanna PP, Weiss F (2001) 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 USA 98:1976-1981
8. Dado RJ, Burstein R, Cliffer KD, Giesler GJ Jr (1990) Evidence that Fluoro-Gold can be transported avidly through fibers of passage. Brain Res 533:329-333
9. de Lecea L, Jones BE, Boutrel B, Borgland SL, Nishino S, Bubser M, DiLeone R (2006) Addiction and arousal: alternative roles of hypothalamic peptides. J Neurosci 26:10372-10375
10. de Souza IE, Meredith GE (1999) NMDA receptor blockade attenuates the haloperidol induction of Fos protein in the dorsal but not the ventral striatum. Synapse 32:243-253
11. De Vries TJ, Schoffelmeer AN, Binnekade R, Mulder AH, Vanderschuren LJ (1998) Drug-induced reinstatement of heroin- and cocaine-seeking behaviour following long-term extinction is associated with expression of behavioural sensitization. Eur J Neurosci 10:3565-3571
12. Di Chiara G (2002) Nucleus accumbens shell and core dopamine: differential role in behavior and addiction. Behav Brain Res 137:75-114
13. Dragunow M, Robertson HA (1987) Kindling stimulation induces c-fos protein(s) in granule cells of the rat dentate gyrus. Nature 329:441-442
14. Everitt BJ, Wolf ME (2002) Psychomotor stimulant addiction: a neural systems perspective. J Neurosci 22:3312-3320
15. Fadel J, Deutch AY (2002) Anatomical substrates of orexin-dopamine interactions: lateral hypothalamic projections to the ventral tegmental area. Neuroscience 111:379-387
16. Fadel J, Bubser M, Deutch AY (2002) Differential activation of orexin neurons by antipsychotic drugs associated with weight gain. J Neurosci 22:6742-6746
17. Feldpausch DL, Needham LM, Stone MP, Althaus JS, Yamamoto BK, Svensson KA, Merchant KM (1998) The role of dopamine D4 receptor in the induction of behavioral sensitization to amphetamine and accompanying biochemical and molecular adaptations. J Pharmacol Exp Ther 286:497-508
18. Franklin TR, Druhan JP (2000) The retrograde tracer fluoro-gold interferes with the expression of fos-related antigens. J Neurosci Methods 98:1-8
19. Fuchs RA, See RE (2002) Basolateral amygdala inactivation abolishes conditioned stimulus- and heroin-induced reinstatement of extinguished heroin-seeking behavior in rats. Psychopharmacology (Berl) 160:425-433
20. Fuchs RA, Evans KA, Ledford CC, Parker MP, Case JM, Mehta RH, See RE (2005) The role of the dorsomedial prefrontal cortex, basolateral amygdala, and dorsal hippocampus in contextual reinstatement of cocaine seeking in rats. Neuropsychopharmacology 30:296-309
21. Gabbott PL, Warner TA, Jays PR, Salway P, Busby SJ (2005) Prefrontal cortex in the rat: projections to subcortical autonomic, motor, and limbic centers. J Comp Neurol 492:145-177
22. Giorgi O, Piras G, Lecca D, Corda MG (2005) Differential activation of dopamine release in the nucleus accumbens core and shell after acute or repeated amphetamine injections: a comparative study in the Roman high- and low-avoidance rat lines. Neuroscience 135:987-998
23. Hagan JJ, Leslie RA, Patel S, Evans ML, Wattam TA, Holmes S, Benham CD, Taylor SG, Routledge C, Hemmati P, Munton RP, Ashmeade TE, Shah AS, Hatcher JP, Hatcher PD, Jones DN, Smith MI, Piper DC, Hunter AJ, Porter RA, Upton N (1999) Orexin A activates locus coeruleus cell firing and increases arousal in the rat. Proc Natl Acad Sci USA 96:10911-10916
24. Harris GC, Wimmer M, Aston-Jones G (2005) A role for lateral hypothalamic orexin neurons in reward seeking. Nature 437:556-559
25. Hedou G, Feldon J, Heidbreder CA (1999) Effects of cocaine on dopamine in subregions of the rat prefrontal cortex and their efferents to subterritories of the nucleus accumbens. Eur J Pharmacol 372:143-155
26. Hedou G, Jongen-Relo AL, Murphy CA, Heidbreder CA, Feldon J (2002) Sensitized Fos expression in subterritories of the rat medial prefrontal cortex and nucleus accumbens following amphetamine sensitization as revealed by stereology. Brain Res 950:165-179
27. Heimer L, Zahm DS, Churchill L, Kalivas PW, Wohltmann C (1991) Specificity in the projection patterns of accumbal core and shell in the rat. Neuroscience 41:89-125
28. Henry DJ, White FJ (1995) The persistence of behavioral sensitization to cocaine parallels enhanced inhibition of nucleus accumbens neurons. J Neurosci 15:6287-6299
29. Ito R, Robbins TW, Everitt BJ (2004) Differential control over cocaine-seeking behavior by nucleus accumbens core and shell. Nat Neurosci 7:389-397
30. Korotkova TM, Sergeeva OA, Eriksson KS, Haas HL, Brown RE (2003) Excitation of ventral tegmental area dopaminergic and nondopaminergic neurons by orexins/hypocretins. J Neurosci 23:7-11
31. Labiner DM, Butler LS, Cao Z, Hosford DA, Shin C, McNamara JO (1993) Induction of c-fos mRNA by kindled seizures: complex relationship with neuronal burst firing. J Neurosci 13:744-751
32. Marcus JN, Aschkenasi CJ, Lee CE, Chemelli RM, Saper CB, Yanagisawa M, Elmquist JK (2001) Differential expression of orexin receptors 1 and 2 in the rat brain. J Comp Neurol 435:6-25
33. McFarland K, Kalivas PW (2001) The circuitry mediating cocaine-induced reinstatement of drug-seeking behavior. J Neurosci 21:8655-8663
34. McLaughlin J, See RE (2003) Selective inactivation of the dorsomedial prefrontal cortex and the basolateral amygdala attenuates conditioned-cued reinstatement of extinguished cocaine-seeking behavior in rats. Psychopharmacology (Berl) 168:57-65
35. Miller CA, Marshall JF (2004) Altered prelimbic cortex output during cue-elicited drug seeking. J Neurosci 24:6889-6897
36. Miller CA, Marshall JF (2005) Altered Fos expression in neural pathways underlying cue-elicited drug seeking in the rat. Eur J Neurosci 21:1385-1393
37. Morshedi MM, Meredith GE (2007) Differential laminar effects of amphetamine on prefrontal parvalbumin interneurons. Neuroscience 149:617-624
38. Nakamura T, Uramura K, Nambu T, Yada T, Goto K, Yanagisawa M, Sakurai T (2000) Orexin-induced hyperlocomotion and stereotypy are mediated by the dopaminergic system. Brain Res 873:181-187
39. Nasif FJ, Hu XT, White FJ (2005) Repeated cocaine administration increases voltage-sensitive calcium currents in response to membrane depolarization in medial prefrontal cortex pyramidal neurons. J Neurosci 25:3674-3679
40. Nikulina EM, Covington HE 3rd, Ganschow L, Hammer RP Jr., Miczek KA (2004) Long-term behavioral and neuronal cross-sensitization to amphetamine induced by repeated brief social defeat stress: Fos in the ventral tegmental area and amygdala. Neuroscience 123:857-865
41. Nogueira L, Kalivas PW, Lavin A (2006) Long-term neuroadaptations produced by withdrawal from repeated cocaine treatment: role of dopaminergic receptors in modulating cortical excitability. J Neurosci 26:12308-12313
42. Onn SP, Grace AA (2000) Amphetamine withdrawal alters bistable states and cellular coupling in rat prefrontal cortex and nucleus accumbens neurons recorded in vivo. J Neurosci 20:2332-2345
43. Ostrander MM, Richtand NM, Herman JP (2003) Stress and amphetamine induce Fos expression in medial prefrontal cortex neurons containing glucocorticoid receptors. Brain Res 990:209-214
44. Paulson PE, Camp DM, Robinson TE (1991) Time course of transient behavioral depression and persistent behavioral sensitization in relation to regional brain monoamine concentrations during amphetamine withdrawal in rats. Psychopharmacology (Berl) 103:480-492
45. Paxinos G, Watson C (2005) The rat brain in stereotaxic coordinates, 5th edn. Academic, New York
46. Peterson JD, Wolf ME, White FJ (2000) Altered responsiveness of medial prefrontal cortex neurons to glutamate and dopamine after withdrawal from repeated amphetamine treatment. Synapse 36:342-344
47. Peyron C, Tighe DK, van den Pol AN, de Lecea L, Heller HC, Sutcliffe JG, Kilduff TS (1998) Neurons containing hypocretin (orexin) project to multiple neuronal systems. J Neurosci 18:9996-10015
48. Pierce RC, Kalivas PW (1995) Amphetamine produces sensitized increases in locomotion and extracellular dopamine preferentially in the nucleus accumbens shell of rats administered repeated cocaine. J Pharmacol Exp Ther 275:1019-1029
49. Pierce RC, Kalivas PW (1997) A circuitry model of the expression of behavioral sensitization to amphetamine-like psychostimulants. Brain Res Brain Res Rev 25:192-216
50. Pierce RC, Bell K, Duffy P, Kalivas PW (1996) Repeated cocaine augments excitatory amino acid transmission in the nucleus accumbens only in rats having developed behavioral sensitization. J Neurosci 16:1550-1560
51. Pierce RC, Reeder DC, Hicks J, Morgan ZR, Kalivas PW (1998) Ibotenic acid lesions of the dorsal prefrontal cortex disrupt the expression of behavioral sensitization to cocaine. Neuroscience 82:1103-1114
52. Pieribone VA, Aston-Jones G (1988) The iontophoretic application of Fluoro-Gold for the study of afferents to deep brain nuclei. Brain Res 475:259-271
53. Pinto A, Sesack SR (2000) Limited collateralization of neurons in the rat prefrontal cortex that project to the nucleus accumbens. Neuroscience 97:635-642
54. Rademacher DJ, Kovacs B, Shen F, Napier TC, Meredith GE (2006) The neural substrates of amphetamine conditioned place preference: implications for the formation of conditioned stimulus-reward associations. Eur J Neurosci 24:2089-2097
55. Robinson TE, Camp DM (1987) Long-lasting effects of escalating doses of d-amphetamine on brain monoamines, amphetamine-induced stereotyped behavior and spontaneous nocturnal locomotion. Pharmacol Biochem Behav 26:821-827
56. Robinson TE, Kolb B (1997) Persistent structural modifications in nucleus accumbens and prefrontal cortex neurons produced by previous experience with amphetamine. J Neurosci 17:8491-8497
57. Robinson TE, Kolb B (1999) Alterations in the morphology of dendrites and dendritic spines in the nucleus accumbens and prefrontal cortex following repeated treatment with amphetamine or cocaine. Eur J Neurosci 11:1598-1604
58. Robinson TE, Berridge KC (2000) The psychology and neurobiology of addiction: an incentive-sensitization view. Addiction 95(Suppl 2):S91-S117
59. Rosenkranz JA, Grace AA (2001) Dopamine attenuates prefrontal cortical suppression of sensory inputs to the basolateral amygdala of rats. J Neurosci 21:4090-4103
60. Saito Y, Cheng M, Leslie FM, Civelli O (2001) Expression of the melanin-concentrating hormone (MCH) receptor mRNA in the rat brain. J Comp Neurol 435:26-40
61. Schmued LC, Fallon JH (1986) Fluoro-Gold: a new fluorescent retrograde axonal tracer with numerous unique properties. Brain Res 377:147-154
62. Schultz W, Tremblay L, Hollerman JR (2000) Reward processing in primate orbitofrontal cortex and basal ganglia. Cereb Cortex 10:272-284
63. Self DW, Nestler EJ (1998) Relapse to drug-seeking: neural and molecular mechanisms. Drug Alcohol Depend 51:49-60
64. Sesack SR, Deutch AY, Roth RH, Bunney BS (1989) Topographical organization of the efferent projections of the medial prefrontal cortex in the rat: an anterograde tract-tracing study with Phaseolus vulgaris leucoagglutinin. J Comp Neurol 290:213-242
65. Simpson JN, Wang JQ, McGinty JF (1995) Repeated amphetamine administration induces a prolonged augmentation of phosphorylated cyclase response element-binding protein and Fos-related antigen immunoreactivity in rat striatum. Neuroscience 69:441-457
66. Smith DG, Tzavara ET, Shaw J, Luecke S, Wade M, Davis R, Salhoff C, Nomikos GG, Gehlert DR (2005) Mesolimbic dopamine super-sensitivity in melanin-concentrating hormone-1 receptor-deficient mice. J Neurosci 25:914-922
67. Sutcliffe JG, de Lecea L (2002) The hypocretins: setting the arousal threshold. Nat Rev Neurosci 3:339-349
68. Thomas KL, Everitt BJ (2001) Limbic-cortical-ventral striatal activation during retrieval of a discrete cocaine-associated stimulus: a cellular imaging study with gamma protein kinase C expression. J Neurosci 21:2526-2535
69. Trantham H, Szumlinski KK, McFarland K, Kalivas PW, Lavin A (2002) Repeated cocaine administration alters the electrophysiological properties of prefrontal cortical neurons. Neuroscience 113:749-753
70. Uslaner J, Badiani A, Day HE, Watson SJ, Akil H, Robinson TE (2001) Environmental context modulates the ability of cocaine and amphetamine to induce c-fos mRNA expression in the neocortex, caudate nucleus, and nucleus accumbens. Brain Res 920:106-116
71. Vertes RP (2004) Differential projections of the infralimbic and prelimbic cortex in the rat. Synapse 51:32-58
72. White FJ, Hu XT, Henry DJ (1993) Electrophysiological effects of cocaine in the rat nucleus accumbens: microiontophoretic studies. J Pharmacol Exp Ther 266:1075-1084
73. White FJ, Hu XT, Zhang XF, Wolf ME (1995) Repeated administration of cocaine or amphetamine alters neuronal responses to glutamate in the mesoaccumbens dopamine system. J Pharmacol Exp Ther 273:445-454
74. Wolf ME (1998) The role of excitatory amino acids in behavioral sensitization to psychomotor stimulants. Prog Neurobiol 54:679-720
75. Wolf ME (2002) Addiction: making the connection between behavioral changes and neuronal plasticity in specific pathways. Mol Interv 2:146-157
76. Yoshida K, McCormack S, Espana RA, Crocker A, Scammell TE (2006) Afferents to the orexin neurons of the rat brain. J Comp Neurol 494:845-861
77. Zhang XF, Hu XT, White FJ (1998) Whole-cell plasticity in cocaine withdrawal: reduced sodium currents in nucleus accumbens neurons. J Neurosci 18:488-498
78. Zhang XF, Cooper DC, White FJ (2002) Repeated cocaine treatment decreases whole-cell calcium current in rat nucleus accumbens neurons. J Pharmacol Exp Ther 301:1119-1125