Rapid dopamine signaling differentially modulates distinct microcircuits within the nucleus accumbens during sucrose-directed behavior

Journal of Neuroscience

Volumn 31, Issue 39, 2011, Pages 13860-13869

  Cacciapaglia, Fabio ^a   Mark Wightman, R ^a,b   Carelli, Regina M ^a,b  

^a UNIVERSITY OF NORTH CAROLINA   (United States)

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

Author keywords

[No Author keywords available]

Indexed keywords

2 AMINO 5 PHOSPHONOVALERIC ACID; DOPAMINE; SUCROSE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL POPULATION; CONTROLLED STUDY; DOPAMINE RELEASE; ELECTROCHEMISTRY; ELECTROPHYSIOLOGY; HELP SEEKING BEHAVIOR; MALE; NERVE CELL STIMULATION; NEUROMODULATION; NONHUMAN; NUCLEUS ACCUMBENS; PHARMACOLOGICAL BLOCKING; PRIORITY JOURNAL; RAT; SIGNAL TRANSDUCTION;

ANIMALS; DOPAMINE; FEEDING BEHAVIOR; MALE; NERVE NET; NUCLEUS ACCUMBENS; RATS; RATS, SPRAGUE-DAWLEY; REWARD; SELF ADMINISTRATION; SIGNAL TRANSDUCTION; SUCROSE; TIME FACTORS;

EID: 80053283185     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1340-11.2011     Document Type: Article

References (53)

1. Aragona BJ, Day JJ, Roitman MF, Cleaveland NA, Wightman RM, Carelli RM (2009) Regional specificity in the real-time development of phasic dopamine transmission patterns during acquisition of a cue-cocaine association in rats. Eur J Neurosci 30:1889-1899
2. Berke JD (2008) Uncoordinated firing rate changes of striatal fast-spiking interneurons during behavioral task performance. J Neurosci 28: 10075-10080
3. Carelli RM (2000) Activation of accumbens cell firing by stimuli associated with cocaine delivery during self-administration. Synapse 35:238-242
4. Carelli RM (2002) Nucleus accumbens cell firing during goal-directed behaviors for cocaine vs 'natural' reinforcement. Physiol Behav 76:379-387
5. Carelli RM, Wightman RM (2004) Functional microcircuitry in the accumbens underlying drug addiction: insights from real-time signaling during behavior. Curr Opin Neurobiol 14:763-768
6. Carelli RM, King VC, Hampson RE, Deadwyler SA (1993) Firing patterns of nucleus accumbens neurons during cocaine self-administration in rats. Brain Res 626:14-22
7. Carelli RM, Ijames SG, Crumling AJ (2000) Evidence that separate neural circuits in the nucleus accumbens encode cocaine versus "natural" (water and food) reward. J Neurosci 20:4255-4266
8. Cheer JF, Heien ML, Garris PA, Carelli RM, Wightman RM (2005) Simultaneous dopamine and single-unit recordings reveal accumbens GABAergic responses: implications for intracranial self-stimulation. Proc Natl Acad Sci U S A 102:19150-19155
9. Cheer JF, Aragona BJ, Heien ML, Seipel AT, Carelli RM, Wightman RM (2007) Coordinated accumbal dopamine release and neural activity drive goal-directed behavior. Neuron 54:237-244
10. Chergui K, Charléty PJ, Akaoka H, Saunier CF, Brunet JL, Buda M, Svensson TH, Chouvet G (1993) Tonic activation of NMDA receptors causes spontaneous burst discharge of rat midbrain dopamine neurons in vivo. Eur J Neurosci 5:137-144
11. Day JJ, Wheeler RA, Roitman MF, Carelli RM (2006) Nucleus accumbens neurons encode Pavlovian approach behaviors: evidence from an autoshaping paradigm. Eur J Neurosci 23:1341-1351
12. Day JJ, Roitman MF, Wightman RM, Carelli RM (2007) Associative learning mediates dynamic shifts in dopamine signaling in the nucleus accumbens. Nat Neurosci 10:1020-1028
13. Deister CA, Teagarden MA, Wilson CJ, Paladini CA (2009) An intrinsic neuronal oscillator underlies dopaminergic neuron bursting. J Neurosci 29:15888-15897
14. Di Ciano P, Everitt BJ (2001) Dissociable effects of antagonism of NMDA and AMPA/KA receptors in the nucleus accumbens core and shell on cocaine-seeking behavior. Neuropsychopharmacology 25:341-360
15. Dreyer JK, Herrik KF, Berg RW, Hounsgaard JD (2010) Influence of phasic and tonic dopamine release on receptor activation. J Neurosci 30:14273-14283
16. Erhardt S, Mathé JM, Chergui K, Engberg G, Svensson TH (2002) GABA(B) receptor-mediated modulation of the firing pattern of ventral tegmental area dopamine neurons in vivo. Naunyn Schmiedebergs Arch Pharmacol 365:173-180
17. Fuchs RA, Evans KA, Parker MC, See RE (2004) Differential involvement of the core and shell subregions of the nucleus accumbens in conditioned cue-induced reinstatement of cocaine seeking in rats. Psychopharmacology (Berl) 176:459-465
18. Goto Y, O'Donnell P (2001) Network synchrony in the nucleus accumbens in vivo. J Neurosci 21:4498-4504
19. Hasbi A, O'Dowd BF, George SR (2010) Heteromerization of dopamine D2 receptors with dopamine D1 or D5 receptors generates intracellular calcium signaling by different mechanisms. Curr Opin Pharmacol 10:93-99
20. Heien ML, Khan AS, Ariansen JL, Cheer JF, Phillips PE, Wassum KM, Wightman RM (2005) Real-time measurement of dopamine fluctuations after cocaine in the brain of behaving rats. Proc Natl Acad Sci U S A 102:10023-10028
21. Hollander JA, Carelli RM (2005) Abstinence from cocaine self-administration heightens neural encoding of goal-directed behaviors in the accumbens. Neuropsychopharmacology 30:1464-1474
22. Ikemoto S (2007) Dopamine reward circuitry: Two projection systems from the ventral midbrain to the nucleus accumbens-olfactory tubercle complex. Brain Res Rev 56:27-78
23. Ito R, Dalley JW, Howes SR, Robbins TW, Everitt BJ (2000) Dissociation in conditioned dopamine release in the nucleus accumbens core and shell in response to cocaine cues and during cocaine-seeking behavior in rats. J Neurosci 20:7489-7495
24. Ito R, Robbins TW, Everitt BJ (2004) Differential control over cocaineseeking behavior by nucleus accumbens core and shell. Nat Neurosci 7:389-397
25. Johnson SW, North RA (1992) Two types of neurone in the rat ventral tegmental area and their synaptic inputs. J Physiol 450:455-468
26. Jones JL, Wheeler RA, Carelli RM (2008) Behavioral responding and nucleus accumbens cell firing are unaltered following periods of abstinence from sucrose. Synapse 62:219-228
27. Jones JL, Day JJ, Aragona BJ, Wheeler RA, Wightman RM, Carelli RM (2010) Basolateral amygdala modulates terminal dopamine release in the nucleus accumbens and conditioned responding. Biol Psychiatry 67:737-744
28. Kawagoe KT, Garris PA, Wiedemann DJ, Wightman RM (1992) Regulation of transient dopamine concentration gradients in the microenvironment surrounding nerve terminals in the rat striatum. Neuroscience 51:55-64
29. Keithley RB, Carelli RM, Wightman RM (2010) Rank estimation and the multivariate analysis of in vivo fast-scan cyclic voltammetric data. Anal Chem 82:5541-5551
30. Lacey MG, Mercuri NB, North RA (1988) On the potassium conductance increase activated by GABAB and dopamine D2 receptors in rat substantia nigra neurones. J Physiol 401:437-453
31. Mogenson GJ, Wu M, Jones DL (1980) Locomotor activity elicited by injections of picrotoxin into the ventral tegmental area is attenuated by injections of GABA into the globus pallidus. Brain Res 191:569-571
32. Nicola SM, Surmeier J, Malenka RC (2000) Dopaminergic modulation of neuronal excitability in the striatum and nucleus accumbens. Annu Rev Neurosci 23:185-215
33. O'Donnell P (2003) Dopamine gating of forebrain neural ensembles. Eur J Neurosci 17:429-435
34. Olpe HR, Koella WP, Wolf P, Haas HL (1977) The action of Baclofen on neurons of the substantia nigra and of the ventral tegmental area. Brain Res 134:577-580
35. Overton P, Clark D (1992) Iontophoretically administered drugs acting at the N-methyl-D-aspartate receptor modulate burst firing in A9 dopamine neurons in the rat. Synapse 10:131-140
36. Owesson-White CA, Cheer JF, Beyene M, Carelli RM, Wightman RM (2008) Dynamic changes in accumbens dopamine correlate with learning during intracranial self-stimulation. Proc Natl Acad Sci U S A 105:11957-11962
37. Owesson-White CA, Ariansen J, Stuber GD, Cleaveland NA, Cheer JF, Wightman RM, Carelli RM (2009) Neural encoding of cocaine-seeking behavior is coincident with phasic dopamine release in the accumbens core and shell. Eur J Neurosci 30:1117-1127
38. Parkinson JA, Olmstead MC, Burns LH, Robbins TW, Everitt BJ (1999) Dissociation in effects of lesions of the nucleus accumbens core and shell on appetitive pavlovian approach behavior and the potentiation of conditioned reinforcement and locomotor activity by D-amphetamine. J Neurosci 19:2401-2411
39. Parkinson JA, Dalley JW, Cardinal RN, Bamford A, Fehnert B, Lachenal G, Rudarakanchana N, Halkerston KM, Robbins TW, Everitt BJ (2002) Nucleus accumbens dopamine depletion impairs both acquisition and performance of appetitive Pavlovian approach behaviour: implications for mesoaccumbens dopamine function. Behav Brain Res 137:149-163
40. Paxinos G, Watson C (2005) The rat brain in stereotaxic coordinates. San Diego: Elsevier Academic.
41. Pennartz CM, Groenewegen HJ, Lopes da Silva FH (1994) The nucleus accumbens as a complex of functionally distinct neuronal ensembles: an integration of behavioural, electrophysiological and anatomical data. Prog Neurobiol 42:719-761
42. Phillips PE, Stuber GD, Heien ML, Wightman RM, Carelli RM (2003) Subsecond dopamine release promotes cocaine seeking. Nature 422:614-618.
43. Prensa L, Parent A (2001) The nigrostriatal pathway in the rat: a single-axon study of the relationship between dorsal and ventral tier nigral neurons and the striosome/matrix striatal compartments. J Neurosci 21:7247-7260.
44. Richfield EK, Penney JB, Young AB (1989) Anatomical and affinity state comparisons between dopamine D1 and D2 receptors in the rat central nervous system. Neuroscience 30:767-777
45. Roitman MF, Stuber GD, Phillips PE, Wightman RM, Carelli RM (2004) Dopamine operates as a subsecond modulator of food seeking. J Neurosci 24:1265-1271
46. Roitman MF, Wheeler RA, Carelli RM (2005) Nucleus accumbens neurons are innately tuned for rewarding and aversive taste stimuli, encode their predictors, and are linked to motor output. Neuron 45:587-597
47. Shen W, Flajolet M, Greengard P, Surmeier DJ (2008) Dichotomous dopaminergic control of striatal synaptic plasticity. Science 321:848-851
48. Sombers LA, Beyene M, Carelli RM, Wightman RM (2009) Synaptic overflow of dopamine in the nucleus accumbens arises from neuronal activity in the ventral tegmental area. J Neurosci 29:1735-1742
49. Suaud-Chagny MF, Chergui K, Chouvet G, Gonon F (1992) Relationship between dopamine release in the rat nucleus accumbens and the discharge activity of dopaminergic neurons during local in vivo application of amino acids in the ventral tegmental area. Neuroscience 49:63-72
50. Surmeier DJ, Ding J, Day M, Wang Z, Shen W (2007) D1 and D2 dopaminereceptor modulation of striatal glutamatergic signaling in striatal medium spiny neurons. Trends Neurosci 30:228-235
51. Wheeler RA, Twining RC, Jones JL, Slater JM, Grigson PS, Carelli RM (2008) Behavioral and electrophysiological indices of negative affect predict cocaine self-administration. Neuron 57:774-785
52. Wickens JR, Wilson CJ (1998) Regulation of action-potential firing in spiny neurons of the rat neostriatum in vivo. J Neurophysiol 79:2358-2364
53. Yun IA, Wakabayashi KT, Fields HL, Nicola SM (2004) The ventral tegmental area is required for the behavioral and nucleus accumbens neuronal firing responses to incentive cues. J Neurosci 24:2923-2933.