Ventral pallidal neurons code incentive motivation: Amplification by mesolimbic sensitization and amphetamine

European Journal of Neuroscience

Volumn 22, Issue 10, 2005, Pages 2617-2634

  Tindell, Amy J ^a   Berridge, Kent C ^a   Zhang, Jun ^a   Peciña, Susana ^a   Aldridge, J Wayne ^a,b  

^a UNIVERSITY OF MICHIGAN   (United States)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

Addiction; Amphetamine sensitization; Incentive salience; Neural coding; Single unit activity; Sprague Dawley rat

Indexed keywords

AMPHETAMINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN NERVE CELL; CELL POPULATION; CONDITIONED REFLEX; CONTROLLED STUDY; ELECTROPHYSIOLOGY; GLOBUS PALLIDUS; LEARNING; LIMBIC SYSTEM; MALE; MOTIVATION; NEUROTRANSMISSION; NONHUMAN; PREDICTION; PRIORITY JOURNAL; RAT; SENSITIZATION; SIGNAL TRANSDUCTION; STIMULUS RESPONSE; TRAINING;

ALGORITHMS; AMPHETAMINE; ANIMALS; CENTRAL NERVOUS SYSTEM STIMULANTS; CONDITIONING, CLASSICAL; CUES; ELECTRODES, IMPLANTED; GLOBUS PALLIDUS; LIMBIC SYSTEM; MALE; MOTIVATION; MOTOR ACTIVITY; NEURONS; RATS; RATS, SPRAGUE-DAWLEY; REWARD; STEREOTYPED BEHAVIOR;

EID: 28744455575     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2005.04411.x     Document Type: Article

References (56)

1. Aldridge, J.W. & Berridge, K.C. (1998) Coding of serial order by neostriatal neurons: a 'natural action' approach to movement sequence. J. Neurosci., 18, 2777-2787.
2. Balleine, B.W., Garner, C., Gonzalez, F. & Dickinson, A. (1995) Motivational control of heterogeneous instrumental chains. J. Exp. Psych.: Anim. Behav. Proc., 21, 203-217.
3. Berke, J.D. & Hyman, S.E. (2000) Addiction, dopamine, and the molecular mechanisms of memory. Neuron, 25, 515-532.
4. Berridge, K.C. (2000) Measuring hedonic impact in animals and infants: microstructure of affective taste reactivity patterns. Neurosci. Biobehav. Rev., 24, 173-198.
5. Berridge, K.C. & Robinson, T.E. (1998) What is the role of dopamine in reward: hedonic impact, reward learning, or incentive salience? Brain Res. Rev., 28, 309-369.
6. Berridge, K.C. & Valenstein, E.S. (1991) What psychological process mediates feeding evoked by electrical stimulation of the lateral hypothalamus? Behav. Neurosci., 105, 3-14.
7. Corbit, L.H. & Balleine, B.W. (2003) Instrumental and Pavlovian incentive processes have dissociable effects on components of a heterogeneous instrumental chain. J. Exp. Psych.: Anim. Behav. Proc., 29, 99-106.
8. Critchfield, T.S. & Kollins, S.H. (2001) Temporal discounting: basic research and the analysis of socially important behavior. J. Appl. Behav. Anal., 34, 101-122.
9. Dayan, P. & Balleine, B.W. (2002) Reward, motivation and, reinforcement learning. Neuron, 36, 285-298.
10. Di Chiara, G. (2002) Nucleus accumbens shell and core dopamine: differential role in behavior and addiction. Behav. Brain Res., 137, 75-114.
11. Dickinson, A. & Balleine, B. (2002) The role of learning in the operation of motivational systems. In Gallistel, C.R. (Ed.), Stevens' Handbook of Experimental Psychology: Learning, Motivation, and Emotion. Wiley and Sons, New York, pp. 497-534.
12. Everitt, B.J. & Wolf, M.E. (2002) Psychomotor stimulant addiction: a neural systems perspective. J. Neurosci., 22, 3312-3320.
13. Galaverna, O.G., Seeley, R.J., Berridge, K.C., Grill, H.J., Epstein, A.N. & Schulkin, J. (1993) Lesions of the central nucleus of the amygdala. I: Effects on taste reactivity, taste aversion learning and sodium appetite. Behav. Brain Res., 59, 11-17.
14. Ghitza, U.E., Fabbricatore, A.T., Prokopenko, V., Pawlak, A.P. & West, M.O. (2003) Persistent cue-evoked activity of accumbens neurons after prolonged abstinence from self-administered cocaine. J. Neurosci., 23, 7239-7245.
15. Giordano, L.A., Bickel, W.K., Loewenstein, G., Jacobs, E.A., Marsch, L. & Badger, G.J. (2002) Mild opioid deprivation increases the degree that opioid-dependent outpatients discount delayed heroin and money. Psychopharmacology, 163, 174-182.
16. Harmer, C.J. & Phillips, G.D. (1998) Enhanced appetitive conditioning following repeated pretreatment with d-amphetamine. Behav. Pharmacol., 9, 299-308.
17. Hyman, S.E. & Malenka, R.C. (2001) Addiction and the brain: the neurobiology of compulsion and its persistence. Nat. Rev. Neurosci., 2, 695-703.
18. Kalivas, P.W., Churchill, L. & Romanides, A. (1999) Involvement of the pallidal-thalamocortical circuit in adaptive behavior. Ann. N.Y. Acad. Sci., 877, 64-70.
19. Kalivas, P.W. & Nakamura, M. (1999) Neural systems for behavioral activation and reward. Curr. Opin. Neurobiol., 9, 223-227.
20. Kelley, A.E., Andrzejewski, M.E., Baldwin, A.E., Hernandez, P.J. & Pratt, W.E. (2003) Glutamate-mediated plasticity in corticostriatal networks: role in adaptive motor learning. Ann. N.Y. Acad. Sci., 1003, 159-168.
21. Klitenick, M.A., Deutch, A.Y., Churchill, L. & Kalivas, P.W. (1992) Topography and functional role of dopaminergic projections from the ventral mesencephalic tegmentum to the ventral pallidum. Neuroscience, 50, 371-386.
22. Kuczenski, R., Melega, W.P., Cho, A.K. & Segal, D.S. (1997) Extracellular dopamine and amphetamine after systemic amphetamine administration: comparison to the behavioral response. J. Pharmacol. Exp. Ther., 282, 591-596.
23. MacLennan, A.J. & Maier, S.F. (1983) Coping and the stress-induced potentiation of stimulant stereotypy in the rat. Science, 219, 1091-1093.
24. Marinelli, M., Cooper, D.C., Baker, L.K. & White, F.J. (2003) Impulse activity of midbrain dopamine neurons modulates drug-seeking behavior. Psychopharmacology, 168, 84-98.
25. Matthews, T.J. & Lerer, B.E. (1987) Behavior patterns in pigeons during autoshaping with an incremental conditioned-stimulus. Learn. Behav., 15, 69-75.
26. McClure, S.M., Daw, N.D. & Montague, P.R. (2003) A computational substrate for incentive salience. Trends Neurosci., 26, 423-428.
27. Montague, P.R. & Berns, G.S. (2002) Neural economics and the biological substrates of valuation. Neuron, 36, 265-284.
28. Nicola, S.M., Yun, I.A., Wakabayashi, K.T. & Fields, H.L. (2004) Cue-evoked firing of nucleus accumbens neurons encodes motivational significance during a discriminative stimulus task. J. Neurophysiol., 91, 1840-1865.
29. O'Doherty, J.P., Dayan, P., Friston, K., Critchley, H. & Dolan, R.J. (2003) Temporal difference models and reward-related learning in the human brain. Neuron, 38, 329-337.
30. O'Donnell, P. (2003) Dopamine gating of forebrain neural ensembles. Eur. J. Neurosci., 17, 429-435.
31. Olausson, P., Jentsch, J.D. & Taylor, J.R. (2003) Repeated nicotine exposure enhances reward-related learning in the rat. Neuropsychopharmacology, 28, 1264-1271.
32. Paulson, P.E., Camp, D.M. & Robinson, T.E. (1991) Time course of transient behavioral depression and persistent behavioral sensitization in relation to regional brain monoamine concentrations during amphetamine withdrawal in rats. Psychopharmacologia, 103, 480-492.
33. Peoples, L.L., Uzwiak, A.J., Gee, F. & West, M.O. (1999) Tonic firing of rat nucleus accumbens neurons: changes during the first 2 weeks of daily cocaine self-administration sessions. Brain Res., 822, 231-236.
34. Phillips, G.D., Harmer, C.J. & Hitchcott, P.K. (2002) Blockade of sensitisation-induced facilitation of appetitive conditioning by post-session intra-amygdala nafadotride. Behav. Brain Res., 134, 249-257.
35. Pierce, R.C. & Kalivas, P.W. (1997) A circuitry model of the expression of behavioral sensitization to amphetamine-like psychostimulants. Brain Res. Brain Res. Rev., 25, 192-216.
36. Redish, A.D. (2004) Addiction as a computational process gone awry. Science, 306, 1944-1947.
37. Robinson, T.E. & Berridge, K.C. (1993) The neural basis of drug craving - an incentive-sensitization theory of addiction. Brain Res. Rev., 18, 247-291.
38. Robinson, T.E. & Berridge, K.C. (2003) Addiction. Annu. Rev. Psychol., 54, 25-53.
39. Robinson, T.E. & 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.
40. Robinson, S., Sandstrom, S.M., Denenberg, V.H. & Palmiter, R.D. (2005) Distinguishing whether dopamine regulates liking, wanting, and/or learning about rewards. Behav. Neurosci., 119, 5-15.
41. Roitman, M.F., Na, E., Anderson, G., Jones, T.A. & Bernstein, I.L. (2002) Induction of a salt appetite alters dendritic morphology in nucleus accumbens and sensitizes rats to amphetamine. J. Neurosci., 22, RC225-RC229.
42. Schultz, W. (2002) Getting formal with dopamine and reward. Neuron, 36, 241-263.
43. Schultz, W., Dayan, P. & Montague, P.R. (1997) A neural substrate of prediction and reward. Science, 275, 1593-1599.
44. Smith, K.S. & Berridge, K.C. (2005) The ventral pallidum and hedonic reward: neurochemical maps of sucrose 'liking' and eating. J. Neurosci., 25, 8637-8649.
45. Steiner, J.E., Glaser, D., Hawilo, M.E. & Berridge, K.C. (2001) Comparative expression of hedonic impact: affective reactions to taste by human infants and other primates. Neurosci. Biobehav. Rev., 25, 53-74.
46. Tang, X.C., McFarland, K., Cagle, S. & Kalivas, P.W. (2005) Cocaine-induced reinstatement requires endogenous stimulation of mu-opioid receptors in the ventral pallidum. J. Neurosci., 25, 4512-4520.
47. Taylor, J.R. & Jentsch, J.D. (2001) Repeated intermittent administration of psychomotor stimulant drugs alters the acquisition of Pavlovian approach behavior in rats: differential effects of cocaine, d-amphetamine and 3,4-methylenedioxymethamphetamine ('Ecstasy'). Biol. Psychiat., 50, 137-143.
48. Timberlake, W., Wahl, G. & King, D. (1982) Stimulus and response contingencies in the misbehavior of rats. J. Exp. Psych.: Anim. Behav. Proc., 8, 65-85.
49. Tindell, A.J., Berridge, K.C. & Aldridge, J.W. (2004) Ventral pallidal representation of pavlovian cues and reward: population and rate codes. J. Neurosci., 24, 1058-1069.
50. Toates, F. (1986) Motivational Systems. Cambridge University Press, Cambridge.
51. Turner, M.S., Lavin, A., Grace, A.A. & Napier, T.C. (2001) Regulation of limbic information outflow by the subthalamic nucleus: excitatory amino acid projections to the ventral pallidum. J. Neurosci., 21, 2820-2832.
52. Turner, M.S., Mignon, L. & Napier, T.C. (2002) Alterations in responses of ventral pallidal neurons to excitatory amino acids after long-term dopamine depletion. J. Pharmacol. Exp. Ther., 301, 371-381.
53. Usuda, I., Tanaka, K. & Chiba, T. (1998) Efferent projections of the nucleus accumbens in the rat with special reference to subdivision of the nucleus: biotinylated dextran amine study. Brain Res., 797, 73-93.
54. Vuchinich, R.E. & Simpson, C.A. (1998) Hyperbolic temporal discounting in social drinkers and problem drinkers. Exp. Clin. Psychopharmacol., 6, 292-305.
55. Wyvell, C.L. & Berridge, K.C. (2001) Incentive sensitization by previous amphetamine exposure: increased cue-triggered 'wanting' for sucrose reward. J. Neurosci., 21, 7831-7840.
56. Zhang, J., Riehle, A., Requin, J. & Kornblum, S. (1997) Dynamics of single neuron activity in monkey primary motor cortex related to sensorimotor transformation. J. Neurosci., 17, 2227-2246.