Rapid dopamine dynamics in the accumbens core and shell: Learning and action

Frontiers in Bioscience - Elite

Volumn 5 E, Issue 1, 2013, Pages 273-288

  Saddoris, Michael P ^a   Sugam, Jonathan A ^a   Cacciapaglia, Fabio ^a,b   Carelli, Regina M ^a,c  

^a UNIVERSITY OF NORTH CAROLINA   (United States)

^b University of North Carolina at Chapel Hill   (United States)

^c UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

Associative learning; Catecholamine; Decision making; Error prediction; Microcircuit; Review; Reward; Ventral striatum

Indexed keywords

COCAINE; DOPAMINE; DOPAMINE RECEPTOR;

ADDICTION; ANIMAL BEHAVIOR; ARTICLE; ASSOCIATION; DECISION MAKING; DOPAMINE METABOLISM; DOPAMINE RELEASE; ELECTROPHYSIOLOGY; HIPPOCAMPUS; INSTRUMENTAL CONDITIONING; LEARNING; MOTIVATION; NONHUMAN; NUCLEUS ACCUMBENS; PARKINSONISM; POTENTIOMETRY; REINFORCEMENT; REWARD; SCHIZOPHRENIA; SUBSTANTIA NIGRA; SYNAPSE; ANIMAL; DOPAMINERGIC NERVE CELL; HUMAN; METABOLISM; PHYSIOLOGY; REVIEW;

ANIMALIA;

ANIMALS; DECISION MAKING; DOPAMINE; DOPAMINERGIC NEURONS; HUMANS; LEARNING; MOTIVATION; NUCLEUS ACCUMBENS; REWARD;

MLCS; MLOWN;

EID: 84878481642     PISSN: 19450494     EISSN: 19450508     Source Type: Journal    
DOI: 10.2741/e615     Document Type: Article

References (148)

1. L. C. Parr-Brownlie and B. I. Hyland: Bradykinesia induced by dopamine D2 receptor blockade is associated with reduced motor cortex activity in the rat. J Neurosci, 25(24), 5700-9 (2005) (Pubitemid 40847882)
2. W. Schultz: Reward signaling by dopamine neurons. Neuroscientist, 7(4), 293-302 (2001) (Pubitemid 32666374)
3. A. Breier, T. P. Su, R. Saunders, R. E. Carson, B. S. Kolachana, A. de Bartolomeis, D. R. Weinberger, N. Weisenfeld, A. K. Malhotra, W. C. Eckelman and D. Pickar: Schizophrenia is associated with elevated amphetamine-induced synaptic dopamine concentrations: evidence from a novel positron emission tomography method. Proc Natl Acad Sci U S A, 94(6), 2569-74 (1997) (Pubitemid 27136916)
4. A. A. Grace: Phasic versus tonic dopamine release and the modulation of dopamine system responsivity: a hypothesis for the etiology of schizophrenia. Neuroscience, 41(1), 1-24 (1991)
5. D. L. Robinson, B. J. Venton, M. L. Heien and R. M. Wightman: Detecting subsecond dopamine release with fast-scan cyclic voltammetry in vivo. Clin Chem, 49(10), 1763-73 (2003) (Pubitemid 37194245)
6. L. A. Sombers, M. Beyene, R. M. Carelli and R. M. Wightman: Synaptic overflow of dopamine in the nucleus accumbens arises from neuronal activity in the ventral tegmental area. J Neurosci, 29(6), 1735-42 (2009)
7. W. Schultz, P. Dayan and P. R. Montague: A neural substrate of prediction and reward. Science, 275(5306), 1593-9 (1997) (Pubitemid 27120526)
8. M. F. Roitman, G. D. Stuber, P. E. Phillips, R. M. Wightman and R. M. Carelli: Dopamine operates as a subsecond modulator of food seeking. J Neurosci, 24(6), 1265-71 (2004) (Pubitemid 38222975)
9. D. L. Robinson, M. L. Heien and R. M. Wightman: Frequency of dopamine concentration transients increases in dorsal and ventral striatum of male rats during introduction of conspecifics. J Neurosci, 22(23), 10477-86 (2002) (Pubitemid 35416884)
10. D. L. Robinson, P. E. Phillips, E. A. Budygin, B. J. Trafton, P. A. Garris and R. M. Wightman: Sub-second changes in accumbal dopamine during sexual behavior in male rats. Neuroreport, 12(11), 2549-52 (2001) (Pubitemid 32682219)
11. M. Beyene, R. M. Carelli and R. M. Wightman: Cueevoked dopamine release in the nucleus accumbens shell tracks reinforcer magnitude during intracranial self-stimulation. Neuroscience, 169(4), 1682-1688 (2010)
12. J. F. Cheer, M. L. Heien, P. A. Garris, R. M. Carelli and R. M. Wightman: Simultaneous dopamine and single-unit recordings reveal accumbens GABAergic responses: implications for intracranial self-stimulation. Proc Natl Acad Sci U S A, 102(52), 19150-5 (2005) (Pubitemid 43049581)
13. C. A. Owesson-White, J. F. Cheer, M. Beyene, R. M. Carelli and R. M. Wightman: Dynamic changes in accumbens dopamine correlate with learning during intracranial self-stimulation. Proc Natl Acad Sci U S A, 105(33), 11957-62 (2008)
14. C. A. Owesson-White, J. Ariansen, G. D. Stuber, N. A. Cleaveland, J. F. Cheer, R. M. Wightman and R. M. Carelli: Neural encoding of cocaine-seeking behavior is coincident with phasic dopamine release in the accumbens core and shell. Eur J Neurosci, 30(6), 1117-27 (2009)
15. P. E. Phillips, G. D. Stuber, M. L. Heien, R. M. Wightman and R. M. Carelli: Subsecond dopamine release promotes cocaine seeking. Nature, 422(6932), 614-8 (2003) (Pubitemid 36460414)
16. F. Gonon: Prolonged and extrasynaptic excitatory action of dopamine mediated by D1 receptors in the rat striatum in vivo. J Neurosci, 17(15), 5972-8 (1997) (Pubitemid 27310510)
17. B. J. Venton, D. J. Michael and R. M. Wightman: Correlation of local changes in extracellular oxygen and pH that accompany dopaminergic terminal activity in the rat caudate-putamen. J Neurochem, 84(2), 373-81 (2003) (Pubitemid 36182278)
18. D. L. Robinson, A. Hermans, A. T. Seipel and R. M. Wightman: Monitoring rapid chemical communication in the brain. Chem Rev, 108(7), 2554-84 (2008)
19. K. T. Kawagoe, P. A. Garris, D. J. Wiedemann and R. M. Wightman: Regulation of transient dopamine concentration gradients in the microenvironment surrounding nerve terminals in the rat striatum. Neuroscience, 51(1), 55-64 (1992)
20. F. Cacciapaglia, R. M. Wightman and R. M. Carelli: Rapid dopamine signaling differentially modulates distinct microcircuits within the nucleus accumbens during sucrosedirected behavior. J Neurosci, 31(39), 13860-13869 (2011)
21. B. J. Aragona, N. A. Cleaveland, G. D. Stuber, J. J. Day, R. M. Carelli and R. M. Wightman: Preferential enhancement of dopamine transmission within the nucleus accumbens shell by cocaine is attributable to a direct increase in phasic dopamine release events. J Neurosci, 28(35), 8821-31 (2008)
22. E. B. Margolis, H. Lock, G. O. Hjelmstad and H. L. Fields: The ventral tegmental area revisited: is there an electrophysiological marker for dopaminergic neurons? J Physiol, 577(Pt 3), 907-24 (2006) (Pubitemid 44873655)
23. R. M. Carelli and R. M. Wightman: Functional microcircuitry in the accumbens underlying drug addiction: insights from real-time signaling during behavior. Current Opinion in Neurobiology, 14(6), 763-8 (2004) (Pubitemid 39576210)
24. C. I. Wright and H. J. Groenewegen: Patterns of overlap and segregation between insular cortical, intermediodorsal thalamic and basal amygdaloid afferents in the nucleus accumbens of the rat. Neuroscience, 73(2), 359-73 (1996) (Pubitemid 26168798)
25. J. S. Brog, A. Salyapongse, A. Y. Deutch and D. S. Zahm: The patterns of afferent innervation of the core and shell in the "accumbens" part of the rat ventral striatum: immunohistochemical detection of retrogradely transported fluoro-gold. J Comp Neurol, 338(2), 255-78 (1993) (Pubitemid 23339283)
26. D. S. Zahm and J. S. Brog: On the significance of subterritories in the "accumbens" part of the rat ventral striatum. Neuroscience, 50(4), 751-67 (1992)
27. H. W. Berendse, Y. Galis-de Graaf and H. J. Groenewegen: Topographical organization and relationship with ventral striatal compartments of prefrontal corticostriatal projections in the rat. J Comp Neurol, 316(3), 314-47 (1992)
28. L. W. Swanson: The projections of the ventral tegmental area and adjacent regions: a combined fluorescent retrograde tracer and immunofluorescence study in the rat. Brain Research Bulletin, 9(1-6), 321-53 (1982) (Pubitemid 13225278)
29. J. G. Ferreira, F. Del-Fava, R. H. Hasue and S. J. Shammah-Lagnado: Organization of ventral tegmental area projections to the ventral tegmental area-nigral complex in the rat. Neuroscience, 153(1), 196-213 (2008)
30. W. J. Nauta, G. P. Smith, R. L. Faull and V. B. Domesick: Efferent connections and nigral afferents of the nucleus accumbens septi in the rat. Neuroscience, 3(4-5), 385-401 (1978) (Pubitemid 8361179)
31. S. Totterdell and A. D. Smith: Convergence of hippocampal and dopaminergic input onto identified neurons in the nucleus accumbens of the rat. J Chem Neuroanat, 2(5), 285-98 (1989) (Pubitemid 19242125)
32. A. M. Brady and P. O'Donnell: Dopaminergic modulation of prefrontal cortical input to nucleus accumbens neurons in vivo. Journal of Neuroscience, 24(5), 1040-9 (2004) (Pubitemid 38177011)
33. S. Ikemoto: Dopamine reward circuitry: two projection systems from the ventral midbrain to the nucleus accumbens-olfactory tubercle complex. Brain Res Rev, 56(1), 27-78 (2007) (Pubitemid 350110353)
34. H. N. David, M. Ansseau and J. H. Abraini: Dopamineglutamate reciprocal modulation of release and motor responses in the rat caudate-putamen and nucleus accumbens of "intact" animals. Brain Res Brain Res Rev, 50(2), 336-60 (2005) (Pubitemid 41654400)
35. X. Y. Lu, M. B. Ghasemzadeh and P. W. Kalivas: Expression of D1 receptor, D2 receptor, substance P and enkephalin messenger RNAs in the neurons projecting from the nucleus accumbens. Neuroscience, 82(3), 767-80 (1998) (Pubitemid 27479616)
36. D. S. Zahm: An integrative neuroanatomical perspective on some subcortical substrates of adaptive responding with emphasis on the nucleus accumbens. Neurosci Biobehav Rev, 24(1), 85-105 (2000) (Pubitemid 30026150)
37. D. S. Zahm and L. Heimer: Specificity in the efferent projections of the nucleus accumbens in the rat: comparison of the rostral pole projection patterns with those of the core and shell. J Comp Neurol, 327(2), 220-32 (1993) (Pubitemid 23019812)
38. I. Usuda, K. Tanaka and T. Chiba: Efferent projections of the nucleus accumbens in the rat with special reference to subdivision of the nucleus: biotinylated dextran amine study. Brain Res, 797(1), 73-93 (1998) (Pubitemid 28331492)
39. L. Heimer, D. S. Zahm, L. Churchill, P. W. Kalivas and C. Wohltmann: Specificity in the projection patterns of accumbal core and shell in the rat. Neuroscience, 41(1), 89-125 (1991)
40. Y. C. van Dongen, J. M. Deniau, C. M. Pennartz, Y. Galis-de Graaf, P. Voorn, A. M. Thierry and H. J. Groenewegen: Anatomical evidence for direct connections between the shell and core subregions of the rat nucleus accumbens. Neuroscience, 136(4), 1049-71 (2005) (Pubitemid 41790520)
41. Y. C. van Dongen, P. Mailly, A. M. Thierry, H. J. Groenewegen and J. M. Deniau: Three-dimensional organization of dendrites and local axon collaterals of shell and core medium-sized spiny projection neurons of the rat nucleus accumbens. Brain Struct Funct, 213(1-2), 129-47 (2008)
42. A. C. Wong, M. E. Shetreat, J. O. Clarke and S. Rayport: D1-and D2-like dopamine receptors are colocalized on the presynaptic varicosities of striatal and nucleus accumbens neurons in vitro. Neuroscience, 89(1), 221-33 (1999) (Pubitemid 29049041)
43. P. M. Groves: A theory of the functional organization of the neostriatum and the neostriatal control of voluntary movement. Brain Res, 286(2), 109-32 (1983) (Pubitemid 13127381)
44. W. Shen, M. Flajolet, P. Greengard and D. J. Surmeier: Dichotomous dopaminergic control of striatal synaptic plasticity. Science, 321(5890), 848-51 (2008)
45. J. Bertran-Gonzalez, C. Bosch, M. Maroteaux, M. Matamales, D. Herve, E. Valjent and J. A. Girault: Opposing patterns of signaling activation in dopamine D1 and D2 receptor-expressing striatal neurons in response to cocaine and haloperidol. J Neurosci, 28(22), 5671-85 (2008)
46. M. P. Arts and H. J. Groenewegen: Relationships of the Dendritic Arborizations of Ventral Striatomesencephalic Projection Neurons With Boundaries of Striatal Compartments. An In vitro Intracellular Labelling Study in the Rat. Eur J Neurosci, 4(6), 574-588 (1992)
47. S. N. Haber and R. Calzavara: The cortico-basal ganglia integrative network: the role of the thalamus. Brain Res Bull, 78(2-3), 69-74 (2009)
48. D. Belin and B. J. Everitt: Cocaine seeking habits depend upon dopamine-dependent serial connectivity linking the ventral with the dorsal striatum. Neuron, 57(3), 432-41 (2008) (Pubitemid 351179162)
49. D. Belin, S. Jonkman, A. Dickinson, T. W. Robbins and B. J. Everitt: Parallel and interactive learning processes within the basal ganglia: relevance for the understanding of addiction. Behav Brain Res, 199(1), 89-102 (2009)
50. T. W. Robbins, K. D. Ersche and B. J. Everitt: Drug addiction and the memory systems of the brain. Ann N Y Acad Sci, 1141, 1-21 (2008)
51. M. F. Roitman, R. A. Wheeler and R. M. Carelli: Nucleus accumbens neurons are innately tuned for rewarding and aversive taste stimuli, encode their predictors, and are linked to motor output. Neuron, 45(4), 587-97 (2005) (Pubitemid 40249870)
52. S. A. Taha and H. L. Fields: Inhibitions of nucleus accumbens neurons encode a gating signal for reward-directed behavior. J Neurosci, 26(1), 217-22 (2006) (Pubitemid 43089534)
53. S. A. Taha and H. L. Fields: Encoding of palatability and appetitive behaviors by distinct neuronal populations in the nucleus accumbens. J Neurosci, 25(5), 1193-202 (2005) (Pubitemid 40268961)
54. M. P. Saddoris, A. Stamatakis and R. M. Carelli: Neural correlates of Pavlovian-to-instrumental transfer in the nucleus accumbens shell are selectively potentiated following cocaine self-administration. Eur J Neurosci, 33(12), 2274-87 (2011)
55. B. Setlow, G. Schoenbaum and M. Gallagher: Neural encoding in ventral striatum during olfactory discrimination learning. Neuron, 38(4), 625-36 (2003) (Pubitemid 36645036)
56. R. A. Wheeler and R. M. Carelli: Dissecting motivational circuitry to understand substance abuse. Neuropharmacology, 56 Suppl 1, 149-59 (2009)
57. R. A. Wheeler, R. C. Twining, J. L. Jones, J. M. Slater, P. S. Grigson and R. M. Carelli: Behavioral and electrophysiological indices of negative affect predict cocaine self-administration. Neuron, 57(5), 774-85 (2008) (Pubitemid 351335347)
58. M. F. Roitman, R. A. Wheeler, P. H. Tiesinga, J. D. Roitman and R. M. Carelli: Hedonic and nucleus accumbens neural responses to a natural reward are regulated by aversive conditioning. Learn Mem, 17(11), 539-46 (2010)
59. V. Bassareo and G. Di Chiara: Differential influence of associative and nonassociative learning mechanisms on the responsiveness of prefrontal and accumbal dopamine transmission to food stimuli in rats fed ad libitum. J Neurosci, 17(2), 851-61 (1997) (Pubitemid 27024596)
60. V. Bassareo and G. Di Chiara: Differential responsiveness of dopamine transmission to food-stimuli in nucleus accumbens shell/core compartments. Neuroscience, 89(3), 637-41 (1999) (Pubitemid 29070991)
61. M. F. Roitman, R. A. Wheeler, R. M. Wightman and R. M. Carelli: Real-time chemical responses in the nucleus accumbens differentiate rewarding and aversive stimuli. Nat Neurosci, 11(12), 1376-7 (2008)
62. R. A. Wheeler, B. J. Aragona, K. A. Fuhrmann, J. L. Jones, J. J. Day, F. Cacciapaglia, R. M. Wightman and R. M. Carelli: Cocaine cues drive opposing context-dependent shifts in reward processing and emotional state. Biol Psychiatry, 69(11), 1067-74 (2011)
63. G. D. Stuber, M. F. Roitman, P. E. Phillips, R. M. Carelli and R. M. Wightman: Rapid dopamine signaling in the nucleus accumbens during contingent and noncontingent cocaine administration. Neuropsychopharmacology, 30(5), 853-63 (2005) (Pubitemid 40570901)
64. P. W. Kalivas and P. Duffy: Selective activation of dopamine transmission in the shell of the nucleus accumbens by stress. Brain Res, 675(1-2), 325-8 (1995)
65. L. Levita, J. W. Dalley and T. W. Robbins: Nucleus accumbens dopamine and learned fear revisited: a review and some new findings. Behav Brain Res, 137(1-2), 115-27 (2002) (Pubitemid 35346431)
66. S. M. Nicola, S. A. Taha, S. W. Kim and H. L. Fields: Nucleus accumbens dopamine release is necessary and sufficient to promote the behavioral response to rewardpredictive cues. Neuroscience, 135(4), 1025-33 (2005) (Pubitemid 41416666)
67. R. A. Rescorla: Pavlovian conditioning. It's not what you think it is. American Psychologist, 43(3), 151-60 (1988)
68. A. Dickinson: Contemporary Animal Learning Theory. Cambridge University Press, Cambridge (1980)
69. P. C. Holland: Event representation in Pavlovian conditioning: image and action. Cognition, 37(1-2), 105-31 (1990)
70. H. J. Cassaday, R. R. Horsley and C. Norman: Electrolytic lesions to nucleus accumbens core and shell have dissociable effects on conditioning to discrete and contextual cues in aversive and appetitive procedures respectively. Behav Brain Res, 160(2), 222-35 (2005) (Pubitemid 40603519)
71. L. H. Corbit, J. L. Muir and B. W. Balleine: The role of the nucleus accumbens in instrumental conditioning: Evidence of a functional dissociation between accumbens core and shell. J Neurosci, 21(9), 3251-60 (2001) (Pubitemid 32323507)
72. J. A. Parkinson, R. N. Cardinal and B. J. Everitt: Limbic cortical-ventral striatal systems underlying appetitive conditioning. Progress in Brain Research, 126, 263-85 (2000) (Pubitemid 35461294)
73. C. A. Blaiss and P. H. Janak: The nucleus accumbens core and shell are critical for the expression, but not the consolidation, of Pavlovian conditioned approach. Behav Brain Res (2008)
74. T. Singh, M. A. McDannald, R. Z. Haney, D. H. Cerri and G. Schoenbaum: Nucleus Accumbens Core and Shell are Necessary for Reinforcer Devaluation Effects on Pavlovian Conditioned Responding. Front Integr Neurosci, 4, 126 (2010)
75. M. A. McDannald, F. Lucantonio, K. A. Burke, Y. Niv and G. Schoenbaum: Ventral striatum and orbitofrontal cortex are both required for model-based, but not modelfree, reinforcement learning. J Neurosci, 31(7), 2700-5 (2011)
76. J. J. Day, R. A. Wheeler, M. F. Roitman and R. M. Carelli: Nucleus accumbens neurons encode Pavlovian approach behaviors: evidence from an autoshaping paradigm. Eur J Neurosci, 23(5), 1341-51 (2006)
77. R. A. Rescorla and A. D. Wagner: A theory of Pavlovian conditioning: Variations in the effectiveness of reinforcement and nonreinforcement. In: Classical Conditioning II: Theory and Research. Ed A. H. Black & W. F. Prokasy. Appleton-Century-Crofts, New York (1972)
78. J. M. Pearce and G. Hall: A model for Pavlovian learning: variations in the effectiveness of conditioned but not of unconditioned stimuli. Psychological Reviews, 87(6), 532-52 (1980)
79. N. J. Mackintosh: The Psychology of Animal Learning. Academic Press, London (1974)
80. G. R. Esber and M. Haselgrove: Reconciling the influence of predictiveness and uncertainty on stimulus salience: a model of attention in associative learning. Proc Biol Sci, 278(1718), 2553-61 (2011)
81. P. Waelti, A. Dickinson and W. Schultz: Dopamine responses comply with basic assumptions of formal learning theory. Nature, 412(6842), 43-8 (2001) (Pubitemid 32851502)
82. E. B. Margolis, J. M. Mitchell, J. Ishikawa, G. O. Hjelmstad and H. L. Fields: Midbrain dopamine neurons: projection target determines action potential duration and dopamine D (2) receptor inhibition. J Neurosci, 28(36), 8908-13 (2008)
83. E. B. Margolis, A. R. Coker, J. R. Driscoll, A. I. Lemaitre and H. L. Fields: Reliability in the identification of midbrain dopamine neurons. PLoS One, 5(12), e15222 (2010)
84. J. J. Day, M. F. Roitman, R. M. Wightman and R. M. Carelli: Associative learning mediates dynamic shifts in dopamine signaling in the nucleus accumbens. Nat Neurosci, 10(8), 1020-8 (2007) (Pubitemid 47185195)
85. G. Schoenbaum and B. Setlow: Lesions of nucleus accumbens disrupt learning about aversive outcomes. Journal of Neuroscience, 23(30), 9833-41 (2003) (Pubitemid 37371597)
86. R. de Borchgrave, J. N. Rawlins, A. Dickinson and B. W. Balleine: Effects of cytotoxic nucleus accumbens lesions on instrumental conditioning in rats. Exp Brain Res, 144(1), 50-68 (2002) (Pubitemid 34439304)
87. G. J. Mogenson, D. L. Jones and C. Y. Yim: From motivation to action: functional interface between the limbic system and the motor system. Prog Neurobiol, 14(2-3), 69-97 (1980) (Pubitemid 10053405)
88. P. A. Garris, M. Kilpatrick, M. A. Bunin, D. Michael, Q. D. Walker and R. M. Wightman: Dissociation of dopamine release in the nucleus accumbens from intracranial self-stimulation. Nature, 398(6722), 67-9 (1999)
89. M. Beyene, R. M. Carelli and R. M. Wightman: Cueevoked dopamine release in the nucleus accumbens shell tracks reinforcer magnitude during intracranial self-stimulation. Neuroscience, 169(4), 1682-8 (2010)
90. F. Cacciapaglia, M. P. Saddoris, R. M. Wightman and R. M. Carelli: Differential dopamine release dynamics in the nucleus accumbens core and shell track distinct aspects of goal-directed behavior for sucrose Neuropharmacology (in press)
91. M. P. Saddoris, P. C. Holland and M. Gallagher: Associatively learned representations of taste outcomes activate taste-encoding neural ensembles in gustatory cortex. J Neurosci, 29(49), 15386-96 (2009)
92. R. C. Rizley and R. A. Rescorla: Associations in secondorder conditioning and sensory preconditioning. J Comp Physiol Psychol, 81(1), 1-11 (1972)
93. P. C. Holland and R. A. Rescorla: The effect of two ways of devaluing the unconditioned stimulus after first-and second-order appetitive conditioning. Journal of Experimental Psychology: Animal Behavior Processes, 1(4), 355-363 (1975)
94. P. C. Holland and R. A. Rescorla: Second-order conditioning with food unconditioned stimulus. J Comp Physiol Psychol, 88(1), 459-67 (1975)
95. R. A. Rescorla: Aspects of the reinforcer learned in second-order Pavlovian conditioning. J Exp Psychol Anim Behav Process, 5(1), 79-95 (1979)
96. B. Setlow, P. C. Holland and M. Gallagher: Disconnection of the basolateral amygdala complex and nucleus accumbens impairs appetitive pavlovian secondorder conditioned responses. Behav Neurosci, 116(2), 267-75 (2002) (Pubitemid 34274234)
97. M. P. Saddoris, C. M. Cameron, J. D. Briley and R. M. Carelli: Long-term exposure to cocaine self-administration disrupts the behavioral and neural correlates of Pavlovian second-order conditioning in the nucleus accumbens of rats. In: Society for Neuroscience Annual Meeting. San Diego, CA (2010)
98. W. K. Estes: Discriminative conditioning; effects of a Pavlovian conditioned stimulus upon a subsequently established operant response. J Exp Psychol, 38(2), 173-7 (1948)
99. R. A. Rescorla and R. L. Solomon: Two-process learning theory: Relationships between Pavlovian conditioning and instrumental learning. Psychol Rev, 74(3), 151-82 (1967)
100. P. C. Holland: Relations between Pavlovianinstrumental transfer and reinforcer devaluation. Journal of Experimental Psychology: Animal Behavior Processes, 30(2), 104-17 (2004) (Pubitemid 38491959)
101. A. R. Delamater and P. C. Holland: The influence of CS-US interval on several different indices of learning in appetitive conditioning. J Exp Psychol Anim Behav Process, 34(2), 202-22 (2008) (Pubitemid 351671859)
102. M. A. McDannald and E. M. Galarce: Measuring Pavlovian fear with conditioned freezing and conditioned suppression reveals different roles for the basolateral amygdala. Brain Res, 1374, 82-9 (2011)
103. J. Hall, J. A. Parkinson, T. M. Connor, A. Dickinson and B. J. Everitt: Involvement of the central nucleus of the amygdala and nucleus accumbens core in mediating Pavlovian influences on instrumental behaviour. Eur J Neurosci, 13(10), 1984-92 (2001) (Pubitemid 32537225)
104. C. L. Wyvell and K. C. Berridge: Intra-accumbens amphetamine increases the conditioned incentive salience of sucrose reward: enhancement of reward "wanting" without enhanced "liking" or response reinforcement. J Neurosci, 20(21), 8122-30 (2000)
105. R. N. Cardinal: Neural systems implicated in delayed and probabilistic reinforcement. Neural Netw, 19(8), 1277-301 (2006) (Pubitemid 44472601)
106. L. Green and J. Myerson: A discounting framework for choice with delayed and probabilistic rewards. Psychol Bull, 130(5), 769-92 (2004) (Pubitemid 39216582)
107. P. E. Phillips, M. E. Walton and T. C. Jhou: Calculating utility: preclinical evidence for cost-benefit analysis by mesolimbic dopamine. Psychopharmacology (Berl), 191(3), 483-95 (2007) (Pubitemid 46355899)
108. A. Rangel, C. Camerer and P. R. Montague: A framework for studying the neurobiology of value-based decision making. Nat Rev Neurosci, 9(7), 545-56 (2008) (Pubitemid 351873461)
109. R. N. Cardinal and T. H. Cheung: Nucleus accumbens core lesions retard instrumental learning and performance with delayed reinforcement in the rat. BMC Neurosci, 6, 9 (2005)
110. R. N. Cardinal and N. J. Howes: Effects of lesions of the nucleus accumbens core on choice between small certain rewards and large uncertain rewards in rats. BMC Neurosci, 6, 37 (2005)
111. R. N. Cardinal, D. R. Pennicott, C. L. Sugathapala, T. W. Robbins and B. J. Everitt: Impulsive choice induced in rats by lesions of the nucleus accumbens core. Science, 292(5526), 2499-501 (2001) (Pubitemid 32601663)
112. S. B. Floresco, M. T. Tse and S. Ghods-Sharifi: Dopaminergic and glutamatergic regulation of effort-and delay-based decision making. Neuropsychopharmacology, 33(8), 1966-79 (2008) (Pubitemid 351832587)
113. S. Ghods-Sharifi and S. B. Floresco: Differential effects on effort discounting induced by inactivations of the nucleus accumbens core or shell. Behav Neurosci, 124(2), 179-91 (2010)
114. C. Stopper and S. Floresco: Contributions of the nucleus accumbens and its subregions to different aspects of risk-based decision making. Cognitive, Affective, & Behavioral Neuroscience, 11(1), 97-112 (2011)
115. C. D. Fiorillo, P. N. Tobler and W. Schultz: Discrete coding of reward probability and uncertainty by dopamine neurons. Science, 299(5614), 1898-902 (2003) (Pubitemid 36356659)
116. M. R. Roesch, D. J. Calu and G. Schoenbaum: Dopamine neurons encode the better option in rats deciding between differently delayed or sized rewards. Nat Neurosci, 10(12), 1615-24 (2007) (Pubitemid 350175882)
117. P. N. Tobler, C. D. Fiorillo and W. Schultz: Adaptive coding of reward value by dopamine neurons. Science, 307(5715), 1642-5 (2005) (Pubitemid 40354749)
118. K. Ishiwari, S. M. Weber, S. Mingote, M. Correa and J. D. Salamone: Accumbens dopamine and the regulation of effort in food-seeking behavior: modulation of work output by different ratio or force requirements. Behav Brain Res, 151(1-2), 83-91 (2004) (Pubitemid 38501431)
119. S. Mingote, S. M. Weber, K. Ishiwari, M. Correa and J. D. Salamone: Ratio and time requirements on operant schedules: effort-related effects of nucleus accumbens dopamine depletions. Eur J Neurosci, 21(6), 1749-57 (2005) (Pubitemid 40646620)
120. J. R. St Onge and S. B. Floresco: Dopaminergic modulation of risk-based decision making. Neuropsychopharmacology, 34(3), 681-97 (2009)
121. J. St. Onge, Y. Chiu and S. Floresco: Differential effects of dopaminergic manipulations on risky choice. Psychopharmacology (Berl), 211(2), 209-221 (2010)
122. J. J. Day, J. L. Jones, R. M. Wightman and R. M. Carelli: Phasic nucleus accumbens dopamine release encodes effortand delay-related costs. Biol Psychiatry, 68(3), 306-9 (2010)
123. J. O. Gan, M. E. Walton and P. E. Phillips: Dissociable cost and benefit encoding of future rewards by mesolimbic dopamine. Nat Neurosci, 13(1), 25-7 (2010)
124. N. A. Nasrallah, J. J. Clark, A. L. Collins, C. A. Akers, P. E. Phillips and I. L. Bernstein: Risk preference following adolescent alcohol use is associated with corrupted encoding of costs but not rewards by mesolimbic dopamine. Proc Natl Acad Sci U S A, 108(13), 5466-71 (2011)
125. J. A. Sugam, J. J. Day, R. M. Wightman and R. M. Carelli: Phasic nucleus accumbens dopamine encodes riskbased decision-making behavior. Biol Psychiatry, 71, 199-205 (2012)
126. J. F. Cheer, B. J. Aragona, M. L. Heien, A. T. Seipel, R. M. Carelli and R. M. Wightman: Coordinated accumbal dopamine release and neural activity drive goal-directed behavior. Neuron, 54(2), 237-44 (2007) (Pubitemid 46561202)
127. A. Hasbi, B. F. O'Dowd and S. R. George: Heteromerization of dopamine D2 receptors with dopamine D1 or D5 receptors generates intracellular calcium signaling by different mechanisms. Curr Opin Pharmacol, 10(1), 93-9 (2010)
128. J. K. Dreyer, K. F. Herrik, R. W. Berg and J. D. Hounsgaard: Influence of phasic and tonic dopamine release on receptor activation. J Neurosci, 30(42), 14273-83 (2010)
129. P. W. Kalivas, N. Volkow and J. Seamans: Unmanageable motivation in addiction: a pathology in prefrontal-accumbens glutamate transmission. Neuron, 45(5), 647-50 (2005) (Pubitemid 40320699)
130. L. H. Burns, L. Annett, A. E. Kelley, B. J. Everitt and T. W. Robbins: Effects of lesions to amygdala, ventral subiculum, medial prefrontal cortex, and nucleus accumbens on the reaction to novelty: implication for limbic-striatal interactions. Behav Neurosci, 110(1), 60-73 (1996) (Pubitemid 26068796)
131. L. H. Burns, T. W. Robbins and B. J. Everitt: Differential effects of excitotoxic lesions of the basolateral amygdala, ventral subiculum and medial prefrontal cortex on responding with conditioned reinforcement and locomotor activity potentiated by intra-accumbens infusions of D-amphetamine. Behavioral Brain Research, 55(2), 167-83 (1993) (Pubitemid 23217489)
132. T. R. Franklin and J. P. Druhan: Involvement of the nucleus accumbens and medial prefrontal cortex in the expression of conditioned hyperactivity to a cocaine-associated environment in rats. Neuropsychopharmacology, 23(6), 633-44 (2000)
133. Y. Goto and P. O'Donnell: Prefrontal lesion reverses abnormal mesoaccumbens response in an animal model of schizophrenia. Biol Psychiatry, 55(2), 172-6 (2004) (Pubitemid 38372156)
134. J. E. Krettek and J. L. Price: Amygdaloid projections to subcortical structures within the basal forebrain and brainstem in the rat and cat. Journal of Comparative Neurology, 178(2), 225-54 (1978)
135. D. R. Ramirez and L. M. Savage: Differential involvement of the basolateral amygdala, orbitofrontal cortex, and nucleus accumbens core in the acquisition and use of reward expectancies. Behav Neurosci, 121(5), 896-906 (2007) (Pubitemid 350051293)
136. A. J. McDonald: Organization of amygdaloid projections to the prefrontal cortex and associated striatum in the rat. Neuroscience, 44(1), 1-14 (1991)
137. A. J. McDonald: Topographical organization of amygdaloid projections to the caudatoputamen, nucleus accumbens, and related striatal-like areas of the rat brain. Neuroscience, 44(1), 15-33 (1991)
138. F. Ambroggi, A. Ishikawa, H. L. Fields and S. M. Nicola: Basolateral amygdala neurons facilitate rewardseeking behavior by exciting nucleus accumbens neurons. Neuron, 59(4), 648-61 (2008)
139. J. L. Jones, J. J. Day, R. A. Wheeler and R. M. Carelli: The basolateral amygdala differentially regulates conditioned neural responses within the nucleus accumbens core and shell. Neuroscience, 169(3), 1186-98 (2010)
140. K. Deisseroth: Optogenetics. Nat Methods, 8(1), 26-9 (2011)
141. F. Zhang, V. Gradinaru, A. R. Adamantidis, R. Durand, R. D. Airan, L. de Lecea and K. Deisseroth: Optogenetic interrogation of neural circuits: technology for probing mammalian brain structures. Nat Protoc, 5(3), 439-56 (2010)
142. G. D. Stuber, D. R. Sparta, A. M. Stamatakis, W. A. van Leeuwen, J. E. Hardjoprajitno, S. Cho, K. M. Tye, K. A. Kempadoo, F. Zhang, K. Deisseroth and A. Bonci: Excitatory transmission from the amygdala to nucleus accumbens facilitates reward seeking. Nature, 475(7356), 377-80 (2011)
143. D. S. Zahm, A. Y. Cheng, T. J. Lee, C. W. Ghobadi, Z. M. Schwartz, S. Geisler, K. P. Parsely, C. Gruber and R. W. Veh: Inputs to the midbrain dopaminergic complex in the rat, with emphasis on extended amygdala-recipient sectors. J Comp Neurol, 519(16), 3159-88 (2011)
144. J. L. Jones, J. J. Day, B. J. Aragona, R. A. Wheeler, R. M. Wightman and R. M. Carelli: Basolateral amygdala modulates terminal dopamine release in the nucleus accumbens and conditioned responding. Biol Psychiatry, 67(8), 737-44 (2010)
145. A. Ishikawa, F. Ambroggi, S. M. Nicola and H. L. Fields: Dorsomedial prefrontal cortex contribution to behavioral and nucleus accumbens neuronal responses to incentive cues. J Neurosci, 28(19), 5088-98 (2008)
146. C. M. Stopper and S. B. Floresco: Contributions of the nucleus accumbens and its subregions to different aspects of risk-based decision making. Cogn Affect Behav Neurosci, 11(1), 97-112 (2011)
147. S. V. Albertin, A. B. Mulder, E. Tabuchi, M. B. Zugaro and S. I. Wiener: Lesions of the medial shell of the nucleus accumbens impair rats in finding larger rewards, but spare reward-seeking behavior. Behav Brain Res, 117(1-2), 173-83 (2000)
148. J. J. Day, J. L. Jones and R. M. Carelli: Nucleus accumbens neurons encode predicted and ongoing reward costs in rats. Eur J Neurosci, 33(2), 308-21 (2011)