Requirement of dopamine signaling in the amygdala and striatum for learning and maintenance of a conditioned avoidance response

Learning and Memory

Volumn 18, Issue 3, 2011, Pages 136-143

  Darvas, Martin ^a   Fadok, Jonathan P ^b   Palmiter, Richard D ^a,b  

^a UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DOPAMINE; LEVODOPA;

AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AVOIDANCE BEHAVIOR; CONTROLLED STUDY; CORPUS STRIATUM; DOPAMINE DEFICIENT MOUSE; DOPAMINE METABOLISM; FEMALE; GENE ACTIVATION; LEARNING; MALE; MOUSE; NONHUMAN; OVEREXERTION; PREFRONTAL CORTEX; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; VIRAL GENE THERAPY;

AMYGDALA; ANALYSIS OF VARIANCE; ANIMALS; AVOIDANCE LEARNING; CAFFEINE; CAVEOLIN 2; CENTRAL NERVOUS SYSTEM STIMULANTS; CONDITIONING, CLASSICAL; CORPUS STRIATUM; DOPAMINE; DOPAMINE AGENTS; ESCAPE REACTION; FEAR; LEVODOPA; MICE; MICE, KNOCKOUT; REACTION TIME; SIGNAL TRANSDUCTION; TYROSINE 3-MONOOXYGENASE;

EID: 79952167929     PISSN: 10720502     EISSN: 15495485     Source Type: Journal    
DOI: 10.1101/lm.2041211     Document Type: Article

References (49)

1. Bjorklund A, Dunnett SB. 2007. Dopamine neuron systems in the brain: An update. Trends Neurosci 30: 194-202. (Pubitemid 46654237)
2. Brischoux F, Chakraborty S, Brierley DI, Ungless MA. 2009. Phasic excitation of dopamine neurons in ventral VTA by noxious stimuli. Proc Natl Acad Sci 106: 4894-4899.
3. Da Cunha C, Angelucci ME, Canteras NS, Wonnacott S, Takahashi RN. 2002. The lesion of the rat substantia nigra pars compacta dopaminergic neurons as a model for Parkinson's disease memory disabilities. Cell Mol Neurobiol 22: 227-237. (Pubitemid 35364882)
4. Dalley JW, Cardinal RN, Robbins TW. 2004. Prefrontal executive and cognitive functions in rodents: Neural and neurochemical substrates. Neurosci Biobehav Rev 28: 771-784. (Pubitemid 39535871)
5. Darvas M, Palmiter RD. 2009. Restriction of dopamine signaling to the dorsolateral striatum is sufficient for many cognitive behaviors. Proc Natl Acad Sci 106: 14664-14669.
6. Darvas M, Palmiter RD. 2010. Restricting dopaminergic signaling to either dorsolateral or medial striatum facilitates cognition. J Neurosci 30: 1158-1165.
7. Davidson AB, Weidley E. 1976. Differential effects of neuroleptic and other psychotropic agents on acquisition of avoidance in rats. Life Sci 18: 1279-1284.
8. Dayan P, Balleine BW. 2002. Reward, motivation, and reinforcement learning. Neuron 36: 285-298. (Pubitemid 35217892)
9. Denenberg VH, Kim DS, Palmiter RD. 2004. The role of dopamine in learning, memory, and performance of a water escape task. Behav Brain Res 148: 73-78. (Pubitemid 37543657)
10. de Oliveira AR, Reimer AE, Brandao ML. 2009. Role of dopamine receptors in the ventral tegmental area in conditioned fear. Behav Brain Res 199: 271-277.
11. Dickinson A, Smith J, Mirenowicz J. 2000. Dissociation of Pavlovian and instrumental incentive learning under dopamine antagonists. Behav Neurosci 114: 468-483. (Pubitemid 30490894)
12. Ehrlich I, Humeau Y, Grenier F, Ciocchi S, Herry C, Luthi A. 2009. Amygdala inhibitory circuits and the control of fear memory. Neuron 62: 757-771.
13. Fadok JP, Dickerson TM, Palmiter RD. 2009. Dopamine is necessary for cue-dependent fear conditioning. J Neurosci 29: 11089-11097.
14. Fadok JP, Darvas M, Dickerson TM, Palmiter RD. 2010. Long-term memory for Pavlovian fear conditioning requires dopamine in the nucleus accumbens and basolateral amygdala. PLoS ONE 5: doi:10.1371/journal.pone.0012751.
15. Fibiger HC, Phillips AG, Zis AP. 1974. Deficits in instrumental responding after 6-hydroxydopamine lesions of the nigro-neostriatal dopaminergic projection. Pharmacol Biochem Behav 2: 87-96.
16. Floresco SB, Tse MT. 2007. Dopaminergic regulation of inhibitory and excitatory transmission in the basolateral amygdala-prefrontal cortical pathway. J Neurosci 27: 2045-2057.
17. Gabbott PL, Warner TA, Jays PR, Salway P, Busby SJ. 2005. Prefrontal cortex in the rat: Projections to subcortical autonomic, motor, and limbic centers. J Comp Neurol 492: 145-177. (Pubitemid 41443719)
18. Goldman-Rakic PS, Muly 3rd. EC3rd, Williams GV. 2000. D(1) receptors in prefrontal cells and circuits. Brain Res Brain Res Rev 31: 295-301.
19. Greba Q, Gifkins A, Kokkinidis L. 2001. Inhibition of amygdaloid dopamine D2 receptors impairs emotional learning measured with fear-potentiated startle. Brain Res 899: 218-226. (Pubitemid 32324163)
20. Halladay AK, Coyne T, Sharifi J, Seto J, Wagner GC. 2000. Avoidance responding following amphetamine-induced dopamine depletion. Pharmacol Toxicol 87: 211-217.
21. Hnasko TS, Sotak BN, Palmiter RD. 2005. Morphine reward in dopamine-deficient mice. Nature 438: 854-857. (Pubitemid 41753067)
22. Hnasko TS, Perez FA, Scouras AD, Stoll EA, Gale SD, Luquet S, Phillips PE, Kremer EJ, Palmiter RD. 2006. Cre recombinase-mediated restoration of nigrostriatal dopamine in dopamine-deficient mice reverses hypophagia and bradykinesia. Proc Natl Acad Sci 103: 8858-8863. (Pubitemid 43878108)
23. 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. (Pubitemid 350110353)
24. Joshua M, Adler A, Mitelman R, Vaadia E, Bergman H. 2008. Midbrain dopaminergic neurons and striatal cholinergic interneurons encode the difference between reward and aversive events at different epochs of probabilistic classical conditioning trials. J Neurosci 28: 11673-11684.
25. Kalivas PW, Duffy P. 1995. Selective activation of dopamine transmission in the shell of the nucleus accumbens by stress. Brain Res 675: 325-328.
26. Koob GF, Simon H, Herman JP, Le Moal M. 1984. Neuroleptic-like disruption of the conditioned avoidance response requires destruction of both the mesolimbic and nigrostriatal dopamine systems. Brain Res 303: 319-329. (Pubitemid 14119382)
27. Kremer EJ, Boutin S, Chillon M, Danos O. 2000. Canine adenovirus vectors: An alternative for adenovirus-mediated gene transfer. J Virol 74: 505-512. (Pubitemid 30002932)
28. Lamont EW, Kokkinidis L. 1998. Infusion of the dopamine D1 receptor antagonist SCH 23390 into the amygdala blocks fear expression in a potentiated startle paradigm. Brain Res 795: 128-136. (Pubitemid 28337824)
29. Maren S, Quirk GJ. 2004. Neuronal signalling of fear memory. Nat Rev Neurosci 5: 844-852. (Pubitemid 39482153)
30. McGaugh JL. 2004. The amygdala modulates the consolidation of memories of emotionally arousing experiences. Annu Rev Neurosci 27: 1-28. (Pubitemid 39050395)
31. Mowrer OH. 1947. On the dual nature of learning - a reinterpretation of conditioning and problem solving. Harv Educ Rev 17: 102-148.
32. Negyessy L, Goldman-Rakic PS. 2005. Subcellular localization of the dopamine D2 receptor and coexistence with the calcium-binding protein neuronal calcium sensor-1 in the primate prefrontal cortex. J Comp Neurol 488: 464-475. (Pubitemid 40934683)
33. Packard MG. 2009. Anxiety, cognition, and habit: A multiple memory systems perspective. Brain Res 1293: 121-128.
34. Packard MG, Teather LA. 1998. Amygdala modulation of multiple memory systems: Hippocampus and caudate-putamen. Neurobiol Learn Mem 69: 163-203. (Pubitemid 28364515)
35. Packard MG, Cahill L, McGaugh JL. 1994. Amygdala modulation of hippocampal-dependent and caudate nucleus-dependent memory processes. Proc Natl Acad Sci 91: 8477-8481. (Pubitemid 24273687)
36. Palmiter RD. 2008. Dopamine signaling in the dorsal striatum is essential for motivated behaviors: Lessons from dopamine-deficient mice. Ann N Y Acad Sci 1129: 35-46. (Pubitemid 351990274)
37. Pezze MA, Feldon J. 2004. Mesolimbic dopaminergic pathways in fear conditioning. Prog Neurobiol 74: 301-320. (Pubitemid 39586721)
38. Posluns D. 1962. An analysis of chlorpromazine-induced suppression of the avoidance response. Psychopharmacologia 3: 361-373.
39. Robinson S, Sandstrom SM, Denenberg VH, Palmiter RD. 2005. Distinguishing whether dopamine regulates liking, wanting, and/or learning about rewards. Behav Neurosci 119: 5-15. (Pubitemid 40279492)
40. Schultz W. 2002. Getting formal with dopamine and reward. Neuron 36: 241-263. (Pubitemid 35217890)
41. Schultz W. 2007. Behavioral dopamine signals. Trends Neurosci 30: 203-210. (Pubitemid 46654238)
42. Seamans JK, Gorelova N, Durstewitz D, Yang CR. 2001. Bidirectional dopamine modulation of GABAergic inhibition in prefrontal cortical pyramidal neurons. J Neurosci 21: 3628-3638. (Pubitemid 32422827)
43. Seymour B, Dolan R. 2008. Emotion, decision making, and the amygdala. Neuron 58: 662-671. (Pubitemid 351778475)
44. Shionoya K, Datiche F. 2009. Inactivation of the basolateral amygdala impairs the retrieval of recent and remote taste-potentiated odor aversion memory. Neurobiol Learn Mem 92: 590-596.
45. Smith AJ, Li M, Becker S, Kapur S. 2007. Linking animal models of psychosis to computational models of dopamine function. Neuropsychopharmacology 32: 54-66. (Pubitemid 44967784)
46. Tseng KY, O'Donnell P. 2004. Dopamine-glutamate interactions controlling prefrontal cortical pyramidal cell excitability involve multiple signaling mechanisms. J Neurosci 24: 5131-5139. (Pubitemid 38728985)
47. Ungerstedt U. 1971. Adipsia and aphagia after 6-hydroxydopamine induced degeneration of the nigro-striatal dopamine system. Acta Physiol Scand Suppl 367: 95-122.
48. van der Heyden JA, Bradford LD. 1988. A rapidly acquired one-way conditioned avoidance procedure in rats as a primary screening test for antipsychotics: Influence of shock intensity on avoidance performance. Behav Brain Res 31: 61-67.
49. Wise RA. 2004. Dopamine, learning and motivation. Nat Rev Neurosci 5: 483-494. (Pubitemid 38715515)