Slow phasic and tonic activity of ventral pallidal neurons during cocaine self-administration

Synapse

Volumn 66, Issue 2, 2012, Pages 106-127

  Root, David H ^a   Fabbricatore, Anthony T ^a   Pawlak, Anthony P ^a   Barker, David J ^a   Ma, Sisi ^a   West, Mark O ^a  

^a RUTGERS UNIVERSITY   (United States)

Author keywords

Accumbens; Dopamine; Striatopallidum; Striatum

Indexed keywords

COCAINE;

ANIMAL EXPERIMENT; ARTICLE; CELL FUNCTION; GABAERGIC SYSTEM; GLOBUS PALLIDUS; LIMBIC SYSTEM; MALE; NERVE CELL; NIGRONEOSTRIATAL SYSTEM; NONHUMAN; NUCLEUS ACCUMBENS; PHASE TRANSITION; PRIORITY JOURNAL; RAT; THALAMOCORTICAL TRACT; VENTRAL PALLIDAL NEURON;

ACTION POTENTIALS; ANIMALS; BASAL GANGLIA; COCAINE; COCAINE-RELATED DISORDERS; DISEASE MODELS, ANIMAL; DOPAMINE UPTAKE INHIBITORS; GLOBUS PALLIDUS; MALE; NEURONS; RATS; RATS, LONG-EVANS; REACTION TIME; SELF ADMINISTRATION;

EID: 83055186533     PISSN: 08874476     EISSN: 10982396     Source Type: Journal    
DOI: 10.1002/syn.20990     Document Type: Article

References (72)

1. Alexander GE, DeLong MR, Strick PL. 1986. Parallel organization of functionally segregated circuits linking basal ganglia and cortex. Annu Rev Neurosci 9: 357-381.
2. Belin D, Everitt BJ. 2008. Cocaine seeking habits depend upon dopamine-dependent serial connectivity linking the ventral with the dorsal striatum. Neuron 57: 432-441.
3. Bell K, Churchill L, Kalivas PW. 1995. GABAergic projection from the ventral pallidum and globus pallidus to the subthalamic nucleus. Synapse 20: 10-18.
4. Bengston CP, Lee DJ, Osborne PB. 2004. Opposing electrophysiological actions of 5-HT on noncholinergic and cholinergic neurons in the rat ventral pallidum in vitro. J Neurophysiol 92: 433-443.
5. Bevan MD, Smith AD, Bolam JP. 1996. The substantia nigra as a site of synaptic integration of functionally diverse information arising from the ventral pallidum and the globus pallidus in the rat. Neuroscience 75: 5-12.
6. Bevan MD, Clarke NP, Bolam JP. 1997. Synaptic integration of functionally diverse pallidal information in the entopeduncular nucleus and subthalamic nucleus in the rat. J Neurosci 17: 308-324
7. Brog JS, Salyapongse A, Deutch AY, Zahm DS. 1992. The patterns of afferent innervation of the core and shell in the "accumbens" partof the rat ventral striatum: Immunohistochemical detection ofretrogradely transported fluoro-gold. J Comp Neurol 338: 255-278.
8. Chrobak JJ, Napier TC. 1993. Opioid and GABA modulation of accumbens-evoked ventral pallidal activity. J Neural Transm [GenSect] 93: 123-143.
9. Churchill L, Dilts RP, Kalivas PW. 1990. Changes in gamma-aminobutyric acid, mu-opioid and neurotensin receptors in the accumbens-pallidal projection after discrete quinolinic acid lesions in the nucleus accumbens. Brain Res 511: 41-54.
10. Churchill L, Zahm DS, Kalivas PW. 1996. The mediodorsal nucleus of the thalamus in rats-I. Forebrain gabaergic innervation. Neuroscience 70: 83-102.
11. Comrey AL. 1962. A first course on factor analysis. New York, NY: Academic Press.
12. Fabbricatore AT, Ghitza UE, Prokopenko VF, West MO. 2009. Electrophysiological evidence of mediolateral functional dichotomy in the rat accumbens during cocaine self-administration: Tonic firing patterns. Eur J Neurosci 30: 2387-2400.
13. Fabbricatore AT, Ghitza UE, Prokopenko VF, West MO. 2010. Electrophysiological evidence of mediolateral functional dichotomy in the rat accumbens during cocaine self-administration II: Phasic firing patterns. Eur J Neurosci 31: 1671-1682.
14. Fuller TA, Russchen FT, Price JL. 1987. Sources of presumptive glutamergic/aspartergic afferents to the rat ventral striatopallidal region. J Comp Neurol 258: 317-338.
15. Geisler S, Derst C, Veh RW, Zahm DS. 2007. Glutamatergic afferents of the ventral tegmental area in the rat. J Neurosci 27: 5730-5743.
16. Ghitza UE, Fabbricatore AT, Prokopenko V, Pawlak AP, West MO. 2003. Persistent cue-evoked activity of accumbens neurons after prolonged abstinence from self-administered cocaine. J Neurosci 23: 7239-7245.
17. Ghitza UE, Fabbricatore AT, Prokopenko VF, West MO. 2004. Differences between accumbens core and shell neurons exhibiting phasic firing patterns related to drug-seeking behavior during a discriminative stimulus task. J Neurophysiol 92: 1608-1614.
18. Ghitza UE, Prokopenko VF, West MO, Fabbricatore AT. 2006. Higher magnitude accumbal phasic firing changes among core neurons exhibiting tonic firing increases during cocaine self-administration. Neuroscience 137: 1075-1085.
19. Goeders NE, Smith JE. 1983. Cortical dopamine involvement in cocaine reinforcement. Science 221: 773-775.
20. Gorsuch RK. 1983. Factor analysis, 2nd ed. Hillsdale, NJ: Lawrence Erlbaum Associates.
21. Groenewegen HJ, Berendse HW, Haber SN. 1993. Organization of the output of the ventral striatopallidal system in the rat: Ventral pallidal efferents. Neuroscience 57: 113-142.
22. Heidenreich BA, Napier TC. 2000. Effects of serotonergic 5-HT1A and 5-HT1B ligands on ventral pallidal neuronal activity. Neuroreport 11: 2849-2853.
23. Heimer L, Wilson RD. 1975. The subcortical projections of the allocortex: Similarities in the neural associations of the hippocampus, the piriform cortex, and the neocortex. In: Golgi Centennial Symposium. New York: Raven Press. p 177-193.
24. Heimer L, Zahm DS, Churchill L, Kalivas PW, Wohltmann 1991. Specificity in the projection patterns of accumbal core and shell in the rat. Neuroscience 41: 89-125.
25. Hubner CB, Koob GF. 1990. The ventral pallidum plays a role in mediating cocaine and heroin self-administration in the rat. Brain Res 508: 20-29.
26. Johnson PI, Napier TC. 1996. Contribution of the nucleus accumbens to cocaine-induced responses of ventral pallidal neurons. Synapse 22: 253-260.
27. Johnson PI, Napier TC. 1997. GABA- and glutamate-evoked responses in the rat ventral pallidum are modulated by dopamine. Eur J Neurosci 9: 1397-1406.
28. Kalivas PW, Churchill L, Klitenick MA. 1993. GABA and enkephalin projection from the nucleus accumbens and ventral pallidum to the ventral tegmental area. Neuroscience 57: 1047-1060.
29. Klitenick MA, Deutch AY, Churchill L, Kalivas PW. 1992. Topography and functional role of dopaminergic projections from the ventral mesencephalic tegmentum to the ventral pallidum. Neuroscience 50: 371-386.
30. Li X, Li J, Peng XQ, Spiller K, Gardner EL, Xi ZX. 2009. Metabotropic glutamate receptor 7 modulates the rewarding effects of cocaine in rats: Involvement of a ventral pallidal GABAergic mechanism. Neuropharmacology 34: 1783-1796.
31. Maickel RP, Cox RH Jr, Miller FP, Segal DS, Russell RW. 1969. Correlation of brain levels of drugs with behavioral effects. J Pharm Exp Ther 165: 216-224.
32. Maslowski-Cobuzzi RJ, Napier TC. 1994. Activation of dopaminergic neurons modulates ventral pallidal response evoked by amygdala stimulation. Neuroscience 62: 1103-1120.
33. McFarland K, Davidge SB, Lapish CC, Kalivas PW. 2004. Limbic and motor circuitry underlying footshock-induced reinstatement of cocaine-seeking behavior. J Neurosci 24: 1551-1560.
34. McGregor A, Baker G, Roberts DC. 1996. Effect of 6-hydroxydopamine lesions of the medial prefrontal cortex on intravenous cocaine self-administration under a progressive ratio schedule of reinforcement. Pharmacol Biochem Behav 53: 5-9.
35. Mengual E, Pickel VM. 2004. Regional and subcellular compartmentation of the dopamine transporter and tyrosine hydroxylase in the rat ventral pallidum. J Comp Neurol 468: 395-409.
36. Mitrovic I, Napier TC. 2002. Mu and kappa opioid agonists modulate ventral tegmental area input to the ventral pallidum. Eur J Neurosci 15: 257-268.
37. Mogenson GJ, Jones DL, Yim CY. 1980. From motivation to action: Functional interface between the limbic system and the motor system. Prog Neurobiol 14: 69-97.
38. Napier TC, Muench MB, Maslowski RJ, Battaglia G. 1991. Is dopamine a neurotransmitter within the ventral pallidum/substantia innominata? In: Napier TC, Kalivas PW, Hanin I, editors. The basal forebrain: Anatomy to function. Advances in experimental medicine and biology. New York: Plenum Press. p 183-195
39. Napier TC. 1992. Functional pharmacology of basal forebrain dopamine. In: Levin ED, editor. Neurotransmitter interactions and cognitive function. p 66-77.
40. Napier TC. 1992. Contribution of the amygdala and nucleus accumbens to ventral pallidal responses to dopamine agonists. Synapse 10: 110-119.
41. Napier TC. 1993. Transmitter actions and interactions on pallidal neuronal function. In: Kalivas PW, Barnes CS, editors. Limbic motor circuits and neuropsychiatry. Boca Raton, FL: CRC Press, Inc. p 125-152.
42. Napier TC, Mitrovic I, Churchill L, Klitenick MA, Lu XY, Kalivas PW. 1995. Substance P in the ventral pallidum: Projection from the ventral striatum, and electrophysiological and behavioral consequences of pallidal substance P. Neuroscience 69: 59-70.
43. Nauta WJ, Smith GP, Faull RL, Domesick VB. 1978. Efferent connections and nigral afferents of the nucleus accumbens septi in the rat. Neuroscience 3: 385-401.
44. Nayak PK, Misra AL, Mulé SJ. 1976. Physiological disposition and biotransformation of (3H) cocaine in acutely and chronically treated rats. J Pharmacol Exp Ther 196: 556-569.
45. Nicola SM, Deadwyler SA. 2000. Firing rate of nucleus accumbens neurons is dopamine-dependent and reflects the timing of cocaine-seeking behavior in rats on a progressive ratio schedule of reinforcement. J Neurosci 20: 5526-5537.
46. Norman AB, Tsibulsky VL. 2006. The compulsion zone: A pharmacological theory of acquired cocaine self-administration. Brain Res 1116: 143-152.
47. O'Donnell P, Lavi'n A, Enquist LW, Grace AA, Card JP. 1997. Interconnected parallel circuits between rat nucleus accumbens and thalamus revealed by retrograde transynaptic transport of pseudorabies virus. J Neurosci 17: 2143-2167.
48. Paxinos G, Watson C. 2005. The rat brain in stereotaxic coordinates. New York: Academic Press. 5th Edition.
49. Peoples LL, West MO. 1996. Phasic firing of single neurons in the rat nucleus accumbens correlated with the timing of intravenous cocaine self-administration. J Neurosci 16: 3459-3473.
50. Peoples LL, Gee F, Bibi R, West MO. 1998. Phasic firing time locked to cocaine self-infusion and locomotion: Dissociable firing patterns of single nucleus accumbens neurons in the rat. J Neurosci 18: 7588-7598.
51. Pickens R, Thompson T. 1968. Cocaine-reinforced behavior in rats: Effects of reinforcement magnitude and fixed-ratio size. J Pharmacol Exp Ther 161: 122-129.
52. Roberts DC, Corcoran ME, Fibiger HC. 1977. On the role of ascending catecholaminergic systems in intravenous self-administration of cocaine. Pharmacol Biochem Behav 6: 615-620.
53. Roberts DC, Koob GF. 1982. Disruption of cocaine self-administration following 6-hydroxydopamine lesions of the ventral tegmental area in rats. Pharmacol Biochem Behav 17: 901-904.
54. Roberts DC, Koob GF, Klonoff P, Fibiger HC. 1980. Extinction and recovery of cocaine self-administration following 6-hydroxydopamine lesions of the nucleus accumbens. Pharmacol Biochem Behav 12: 781-787.
55. Robledo P, Koob GF. 1993. Two discrete nucleus accumbens projection areas differentially mediate cocaine self-administration in the rat. Behav Brain Res 55: 159-166.
56. Rodgers JL, Ghee S, See RE. 2008. The neural circuitry underlying reinstatement of heroin-seeking behavior in an animal model of relapse. Neuroscience 151: 579-588.
57. Root DH, Fabbricatore AT, Ma S, Barker DJ, West MO. 2010. Rapid phasic activity of ventral pallidal neurons during cocaine self-administration. Synapse 64: 704-713.
58. Root DH, Barker DJ, Ma S, Coffey KR, Fabbricatore AT, West MO. 2011. Evidence for learned skill during cocaine self-administration in rats. Psychopharmacol 217: 91-100.
59. Smith KS, Berridge KC. 2005. The ventral pallidum and hedonic reward: Neurochemical maps of sucrose "liking" and food intake. J Neurosci 25: 8637-8649.
60. Smith JE, Koves TR, Co C. 2003. Brain neurotransmitter turnover rates during rat intravenous cocaine self-administration. Neuroscience 117: 461-475.
61. Sizemore GM, Co C, Smith JE. 2000. Ventral pallidal extracellular fluid levels of dopamine, serotonin, gamma amino butyric acid, and glutamate during cocaine self-administration in rats. Psychopharmacology 150: 391-398.
62. Stokes ME, Davis CS, Koch GG. 2009. Categorical data analysis using the SAS system, 2nd ed. Cary, NC: SAS Publishing.
63. Tang XC, McFarland K, Cagle S, Kalivas PW. 2005. Cocaine-induced reinstatement requires endogenous stimulation of mu-opioid receptors in the ventral pallidum. J Neurosci 25: 4512-4520.
64. Tabachnick BG, Fidell LS. 1989. Using multivariale statistics, 2nd ed. New York, NY: HarperCollins Publishers.
65. Torregrossa MM, Tang XC, Kalivas PW. 2008. The glutamatergic projection from the prefrontal cortex to the nucleus accumbens core is required for cocaine-induced decreases in ventral pallidal GABA. Neurosci Lett 438: 142-145.
66. Totterdell S, Smith AD. 1989. Convergence of hippocampal and dopaminergic input onto identified neurons in the nucleus accumbens of the rat. J Chem Neuroanat 2: 285-298.
67. Tripathi A, Prensa L, Cebrian C, Mengual E. 2010. Axonal branching patterns of nucleus accumbens neurons in the rat. J Comp Neurol 518: 4649-4673.
68. Walaas I, Fonnum F. 1979. The distribution and origin of glutamate decarboxylase and choline acetyltransferase in ventral pallidum and other basal forebrain regions. Brain Res 177: 325-336.
69. Wise RA, Newton P, Leeb K, Burnette B, Pocock D, Justice JBJr. 1995. Fluctuations in nucleus accumbens dopamine concentration during intravenous cocaine self-administration in rats. Psychopharmacology 120: 10-20.
70. Yokel AR, Pickens R. 1974. Drug level of d- and l-amphetamine during intravenous self-administration. Psychopharmacologia 34: 255-264.
71. Zahm DS, Záborszky L, Alones VE, Heimer L. 1985. Evidence for the coexistence of glutamate decarboxylase and Met-enkephalin immunoreactivities in axon terminals of rat ventral pallidum. Brain Res 325: 317-321.
72. Zahm DS, Williams E, Wohltmann C. 1996. Ventral striatopallidothalamic projection: IV. Relative involvements of neurochemically distinct subterritories in the ventral pallidum and adjacent parts of the rostroventral forebrain. J Comp Neurol 364: 340-362.