Basolateral Amygdala Neurons Facilitate Reward-Seeking Behavior by Exciting Nucleus Accumbens Neurons

Neuron

Volumn 59, Issue 4, 2008, Pages 648-661

  Ambroggi, Frederic ^a   Ishikawa, Akinori ^a   Fields, Howard L ^a   Nicola, Saleem M ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

SIGNALING; SYSBIO; SYSNEURO

Indexed keywords

DOPAMINE; DOPAMINE RECEPTOR;

AMYGDALOID NUCLEUS; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BEHAVIORAL SCIENCE; BRAIN DEPTH STIMULATION; BRAIN FUNCTION; CONTROLLED STUDY; EVOKED BRAIN STEM RESPONSE; MALE; NERVE CELL; NERVE POTENTIAL; NONHUMAN; NUCLEUS ACCUMBENS; PRIORITY JOURNAL; RAT; TASK PERFORMANCE;

AMYGDALA; ANIMALS; APPETITIVE BEHAVIOR; CHOICE BEHAVIOR; DISCRIMINATION LEARNING; DOPAMINE; GLYCOPEPTIDES; MALE; NEURAL PATHWAYS; NEURONS; NUCLEUS ACCUMBENS; RATS; RATS, LONG-EVANS; RATS, SPRAGUE-DAWLEY; REACTION TIME; REWARD;

EID: 50049115556     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuron.2008.07.004     Document Type: Article

References (76)

1. Belova M.A., Paton J.J., Morrison S.E., and Salzman C.D. Expectation modulates neural responses to pleasant and aversive stimuli in primate amygdala. Neuron 55 (2007) 970-984
2. Brog J.S., Salyapongse A., Deutch A.Y., and Zahm D.S. 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 (1993) 255-278
3. Cardinal R.N., Parkinson J.A., Hall J., and Everitt B.J. Emotion and motivation: the role of the amygdala, ventral striatum, and prefrontal cortex. Neurosci. Biobehav. Rev. 26 (2002) 321-352
4. Christie M.J., Summers R.J., Stephenson J.A., Cook C.J., and Beart P.M. Excitatory amino acid projections to the nucleus accumbens septi in the rat: a retrograde transport study utilizing D[3H]aspartate and [3H]GABA. Neuroscience 22 (1987) 425-439
5. Collins D.R., and Pare D. Differential fear conditioning induces reciprocal changes in the sensory responses of lateral amygdala neurons to the CS(+) and CS(-). Learn. Mem. 7 (2000) 97-103
6. Corcoran K.A., Desmond T.J., Frey K.A., and Maren S. Hippocampal inactivation disrupts the acquisition and contextual encoding of fear extinction. J. Neurosci. 25 (2005) 8978-8987
7. Cromwell H.C., and Schultz W. Effects of expectations for different reward magnitudes on neuronal activity in primate striatum. J. Neurophysiol. 89 (2003) 2823-2838
8. Day J.J., Wheeler R.A., Roitman M.F., and Carelli R.M. Nucleus accumbens neurons encode Pavlovian approach behaviors: evidence from an autoshaping paradigm. Eur. J. Neurosci. 23 (2006) 1341-1351
9. Day J.J., Roitman M.F., Wightman R.M., and Carelli R.M. Associative learning mediates dynamic shifts in dopamine signaling in the nucleus accumbens. Nat. Neurosci. 10 (2007) 1020-1028
10. Di Ciano P., and Everitt B.J. Direct interactions between the basolateral amygdala and nucleus accumbens core underlie cocaine-seeking behavior by rats. J. Neurosci. 24 (2004) 7167-7173
11. Di Ciano P., Cardinal R.N., Cowell R.A., Little S.J., and Everitt B.J. Differential involvement of NMDA, AMPA/kainate, and dopamine receptors in the nucleus accumbens core in the acquisition and performance of pavlovian approach behavior. J. Neurosci. 21 (2001) 9471-9477
12. Dommett E., Coizet V., Blaha C.D., Martindale J., Lefebvre V., Walton N., Mayhew J.E., Overton P.G., and Redgrave P. How visual stimuli activate dopaminergic neurons at short latency. Science 307 (2005) 1476-1479
13. Everitt B.J., Cardinal R.N., Parkinson J.A., and Robbins T.W. Appetitive behavior: impact of amygdala-dependent mechanisms of emotional learning. Ann. N Y Acad. Sci. 985 (2003) 233-250
14. Finch D.M. Neurophysiology of converging synaptic inputs from the rat prefrontal cortex, amygdala, midline thalamus, and hippocampal formation onto single neurons of the caudate/putamen and nucleus accumbens. Hippocampus 6 (1996) 495-512
15. Floresco S.B. Dopaminergic regulation of limbic-striatal interplay. J. Psychiatry Neurosci. 32 (2007) 400-411
16. Floresco S.B., Yang C.R., Phillips A.G., and Blaha C.D. Basolateral amygdala stimulation evokes glutamate receptor-dependent dopamine efflux in the nucleus accumbens of the anaesthetized rat. Eur. J. Neurosci. 10 (1998) 1241-1251
17. Floresco S.B., Blaha C.D., Yang C.R., and Phillips A.G. Dopamine D1 and NMDA receptors mediate potentiation of basolateral amygdala-evoked firing of nucleus accumbens neurons. J. Neurosci. 21 (2001) 6370-6376
18. Ghitza U.E., Fabbricatore A.T., Prokopenko V., Pawlak A.P., and West M.O. Persistent cue-evoked activity of accumbens neurons after prolonged abstinence from self-administered cocaine. J. Neurosci. 23 (2003) 7239-7245
19. Ghitza U.E., Fabbricatore A.T., Prokopenko V.F., and West M.O. Differences between accumbens core and shell neurons exhibiting phasic firing patterns related to drug-seeking behavior during a discriminative-stimulus task. J. Neurophysiol. 92 (2004) 1608-1614
20. Goosens K.A., Hobin J.A., and Maren S. Auditory-evoked spike firing in the lateral amygdala and Pavlovian fear conditioning: mnemonic code or fear bias?. Neuron 40 (2003) 1013-1022
21. Goto Y., and O'Donnell P. Timing-dependent limbic-motor synaptic integration in the nucleus accumbens. Proc. Natl. Acad. Sci. USA 99 (2002) 13189-13193
22. Hassani O.K., Cromwell H.C., and Schultz W. Influence of expectation of different rewards on behavior-related neuronal activity in the striatum. J. Neurophysiol. 85 (2001) 2477-2489
23. Hatfield T., Han J.S., Conley M., Gallagher M., and Holland P. Neurotoxic lesions of basolateral, but not central, amygdala interfere with Pavlovian second-order conditioning and reinforcer devaluation effects. J. Neurosci. 16 (1996) 5256-5265
24. Herry C., Bach D.R., Esposito F., Di Salle F., Perrig W.J., Scheffler K., Luthi A., and Seifritz E. Processing of temporal unpredictability in human and animal amygdala. J. Neurosci. 27 (2007) 5958-5966
25. Hjelmstad G.O. Dopamine excites nucleus accumbens neurons through the differential modulation of glutamate and GABA release. J. Neurosci. 24 (2004) 8621-8628
26. Holland P.C., Hatfield T., and Gallagher M. Rats with basolateral amygdala lesions show normal increases in conditioned stimulus processing but reduced conditioned potentiation of eating. Behav. Neurosci. 115 (2001) 945-950
27. Hollerman J.R., Tremblay L., and Schultz W. Influence of reward expectation on behavior-related neuronal activity in primate striatum. J. Neurophysiol. 80 (1998) 947-963
28. Horvitz J.C. Mesolimbocortical and nigrostriatal dopamine responses to salient non-reward events. Neuroscience 96 (2000) 651-656
29. Howland J.G., Taepavarapruk P., and Phillips A.G. Glutamate receptor-dependent modulation of dopamine efflux in the nucleus accumbens by basolateral, but not central, nucleus of the amygdala in rats. J. Neurosci. 22 (2002) 1137-1145
30. Ishikawa A., Ambroggi F., Nicola S.M., and Fields H.L. Contributions of the amygdala and medial prefrontal cortex to incentive cue responding. Neuroscience 155 (2008) 573-584
31. Ishikawa A., Ambroggi F., Nicola S.M., and Fields H.L. Dorsomedial prefrontal cortex contribution to behavioral and nucleus accumbens neuronal responses to incentive cues. J. Neurosci. 28 (2008) 5088-5098
32. Jodo E., Suzuki Y., and Kayama Y. Selective responsiveness of medial prefrontal cortex neurons to the meaningful stimulus with a low probability of occurrence in rats. Brain Res. 856 (2000) 68-74
33. Johnson L.R., Aylward R.L., Hussain Z., and Totterdell S. Input from the amygdala to the rat nucleus accumbens: its relationship with tyrosine hydroxylase immunoreactivity and identified neurons. Neuroscience 61 (1994) 851-865
34. Kobayashi S., Nomoto K., Watanabe M., Hikosaka O., Schultz W., and Sakagami M. Influences of rewarding and aversive outcomes on activity in macaque lateral prefrontal cortex. Neuron 51 (2006) 861-870
35. LeDoux J. The emotional brain, fear, and the amygdala. Cell. Mol. Neurobiol. 23 (2003) 727-738
36. Leon M.I., and Shadlen M.N. Effect of expected reward magnitude on the response of neurons in the dorsolateral prefrontal cortex of the macaque. Neuron 24 (1999) 415-425
37. Maren S., and Quirk G.J. Neuronal signalling of fear memory. Nat. Rev. Neurosci. 5 (2004) 844-852
38. Martin J.H. Autoradiographic estimation of the extent of reversible inactivation produced by microinjection of lidocaine and muscimol in the rat. Neurosci. Lett. 127 (1991) 160-164
39. McDonald A.J. Topographical organization of amygdaloid projections to the caudatoputamen, nucleus accumbens, and related striatal-like areas of the rat brain. Neuroscience 44 (1991) 15-33
40. McGinty V.B., and Grace A.A. Selective activation of medial prefrontal-to-accumbens projection neurons by amygdala stimulation and pavlovian conditioned stimuli. Cereb. Cortex 18 (2008) 1961-1972
41. Mogenson G.J., Wu M., and Jones D.L. 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 (1980) 569-571
42. Morris G., Arkadir D., Nevet A., Vaadia E., and Bergman H. Coincident but distinct messages of midbrain dopamine and striatal tonically active neurons. Neuron 43 (2004) 133-143
43. Mulder A.B., Hodenpijl M.G., and Lopes da Silva F.H. Electrophysiology of the hippocampal and amygdaloid projections to the nucleus accumbens of the rat: convergence, segregation, and interaction of inputs. J. Neurosci. 18 (1998) 5095-5102
44. Nakahara H., Itoh H., Kawagoe R., Takikawa Y., and Hikosaka O. Dopamine neurons can represent context-dependent prediction error. Neuron 41 (2004) 269-280
45. Nicola S.M. The nucleus accumbens as part of a basal ganglia action selection circuit. Psychopharmacology (Berl.) 191 (2007) 521-550
46. Nicola S.M., Surmeier J., and Malenka R.C. Dopaminergic modulation of neuronal excitability in the striatum and nucleus accumbens. Annu. Rev. Neurosci. 23 (2000) 185-215
47. Nicola S.M., Woodward Hopf F., and Hjelmstad G.O. Contrast enhancement: a physiological effect of striatal dopamine?. Cell Tissue Res. 318 (2004) 93-106
48. Nicola S.M., Yun I.A., Wakabayashi K.T., and Fields H.L. Cue-evoked firing of nucleus accumbens neurons encodes motivational significance during a discriminative stimulus task. J. Neurophysiol. 91 (2004) 1840-1865
49. Nicola S.M., Yun I.A., Wakabayashi K.T., and Fields H.L. Firing of nucleus accumbens neurons during the consummatory phase of a discriminative stimulus task depends on previous reward predictive cues. J. Neurophysiol. 91 (2004) 1866-1882
50. O'Donnell P., and Grace A.A. Synaptic interactions among excitatory afferents to nucleus accumbens neurons: hippocampal gating of prefrontal cortical input. J. Neurosci. 15 (1995) 3622-3639
51. Pan W.X., and Hyland B.I. Pedunculopontine tegmental nucleus controls conditioned responses of midbrain dopamine neurons in behaving rats. J. Neurosci. 25 (2005) 4725-4732
52. Pan W.X., Schmidt R., Wickens J.R., and Hyland B.I. Dopamine cells respond to predicted events during classical conditioning: evidence for eligibility traces in the reward-learning network. J. Neurosci. 25 (2005) 6235-6242
53. Parkinson J.A., Robbins T.W., and Everitt B.J. Dissociable roles of the central and basolateral amygdala in appetitive emotional learning. Eur. J. Neurosci. 12 (2000) 405-413
54. Parkinson J.A., Dalley J.W., Cardinal R.N., Bamford A., Fehnert B., Lachenal G., Rudarakanchana N., Halkerston K.M., Robbins T.W., and Everitt B.J. Nucleus accumbens dopamine depletion impairs both acquisition and performance of appetitive Pavlovian approach behaviour: implications for mesoaccumbens dopamine function. Behav. Brain Res. 137 (2002) 149-163
55. Paton J.J., Belova M.A., Morrison S.E., and Salzman C.D. The primate amygdala represents the positive and negative value of visual stimuli during learning. Nature 439 (2006) 865-870
56. Repa J.C., Muller J., Apergis J., Desrochers T.M., Zhou Y., and LeDoux J.E. Two different lateral amygdala cell populations contribute to the initiation and storage of memory. Nat. Neurosci. 4 (2001) 724-731
57. Robbins T.W., and Everitt B.J. A role for mesencephalic dopamine in activation: commentary on Berridge (2006). Psychopharmacology (Berl.) 191 (2007) 433-437
58. Roitman M.F., Stuber G.D., Phillips P.E., Wightman R.M., and Carelli R.M. Dopamine operates as a subsecond modulator of food seeking. J. Neurosci. 24 (2004) 1265-1271
59. Roitman M.F., Wheeler R.A., and Carelli R.M. Nucleus accumbens neurons are innately tuned for rewarding and aversive taste stimuli, encode their predictors, and are linked to motor output. Neuron 45 (2005) 587-597
60. Saddoris M.P., Gallagher M., and Schoenbaum G. Rapid associative encoding in basolateral amygdala depends on connections with orbitofrontal cortex. Neuron 46 (2005) 321-331
61. Schoenbaum G., Chiba A.A., and Gallagher M. Orbitofrontal cortex and basolateral amygdala encode expected outcomes during learning. Nat. Neurosci. 1 (1998) 155-159
62. Schoenbaum G., Chiba A.A., and Gallagher M. Neural encoding in orbitofrontal cortex and basolateral amygdala during olfactory discrimination learning. J. Neurosci. 19 (1999) 1876-1884
63. Schultz W. Multiple dopamine functions at different time courses. Annu. Rev. Neurosci. 30 (2007) 259-288
64. Schultz W., Dayan P., and Montague P.R. A neural substrate of prediction and reward. Science 275 (1997) 1593-1599
65. Setlow B., Holland P.C., and Gallagher M. Disconnection of the basolateral amygdala complex and nucleus accumbens impairs appetitive pavlovian second-order conditioned responses. Behav. Neurosci. 116 (2002) 267-275
66. Sugase-Miyamoto Y., and Richmond B.J. Neuronal signals in the monkey basolateral amygdala during reward schedules. J. Neurosci. 25 (2005) 11071-11083
67. Taha S.A., and Fields H.L. Inhibitions of nucleus accumbens neurons encode a gating signal for reward-directed behavior. J. Neurosci. 26 (2006) 217-222
68. Taha S.A., Nicola S.M., and Fields H.L. Cue-evoked encoding of movement planning and execution in the rat nucleus accumbens. J. Physiol. 584 (2007) 801-818
69. Takenouchi K., Nishijo H., Uwano T., Tamura R., Takigawa M., and Ono T. Emotional and behavioral correlates of the anterior cingulate cortex during associative learning in rats. Neuroscience 93 (1999) 1271-1287
70. Uwano T., Nishijo H., Ono T., and Tamura R. Neuronal responsiveness to various sensory stimuli, and associative learning in the rat amygdala. Neuroscience 68 (1995) 339-361
71. Wan X., and Peoples L.L. Firing patterns of accumbal neurons during a pavlovian-conditioned approach task. J. Neurophysiol. 96 (2006) 652-660
72. Wright C.I., Beijer A.V., and Groenewegen H.J. Basal amygdaloid complex afferents to the rat nucleus accumbens are compartmentally organized. J. Neurosci. 16 (1996) 1877-1893
73. Yim C.Y., and Mogenson G.J. Mesolimbic dopamine projection modulates amygdala-evoked EPSP in nucleus accumbens neurons: an in vivo study. Brain Res. 369 (1986) 347-352
74. Yun I.A., and Fields H.L. Basolateral amygdala lesions impair both cue- and cocaine-induced reinstatement in animals trained on a discriminative stimulus task. Neuroscience 121 (2003) 747-757
75. Yun I.A., Nicola S.M., and Fields H.L. Contrasting effects of dopamine and glutamate receptor antagonist injection in the nucleus accumbens suggest a neural mechanism underlying cue-evoked goal-directed behavior. Eur. J. Neurosci. 20 (2004) 249-263
76. Yun I.A., Wakabayashi K.T., Fields H.L., and Nicola S.M. The ventral tegmental area is required for the behavioral and nucleus accumbens neuronal firing responses to incentive cues. J. Neurosci. 24 (2004) 2923-2933