Modulation of memory consolidation by the basolateral amygdala or nucleus accumbens shell requires concurrent dopamine receptor activation in both brain regions

Learning and Memory

Volumn 12, Issue 3, 2005, Pages 296-301

  LaLumiere, Ryan T ^a   Nawar, Erene M ^a   McGaugh, James L ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DOPAMINE; DOPAMINE RECEPTOR; DOPAMINE RECEPTOR BLOCKING AGENT; FLUPENTIXOL;

AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AVOIDANCE BEHAVIOR; BRAIN REGION; CANNULA; CONTROLLED STUDY; EXPERIMENTAL TEST; IMPLANTATION; INFUSION; LATENT PERIOD; LONG TERM MEMORY; MALE; MEMORY CONSOLIDATION; MODULATION; NONHUMAN; NUCLEUS ACCUMBENS; PRIORITY JOURNAL; RAT; SHOCK; TASK PERFORMANCE; TIME; TRAINING;

AMYGDALA; ANIMALS; CONDITIONING, OPERANT; DOPAMINE; DOPAMINE AGONISTS; DOPAMINE ANTAGONISTS; FLUPENTHIXOL; FUNCTIONAL LATERALITY; MALE; MEMORY; NUCLEUS ACCUMBENS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, DOPAMINE; REVERSAL LEARNING;

EID: 21844442808     PISSN: 10720502     EISSN: None     Source Type: Journal    
DOI: 10.1101/lm.93205     Document Type: Article

References (49)

1. Barrot, M., Marinelli, M., Abrous, D.N., Rouge-Pont, F., Le Moal, M., and Piazza, P.V. 2000. The dopaminergic hyper-responsiveness of the shell of the nucleus accumbens is hormone-dependent. Eur. J. Neurosci. 12: 973-979.
2. Carr, G.D. and White, N.M. 1983. Conditioned place preference from intra-accumbens but not intra-caudate amphetamine injections. Life Sci. 33: 2551-2557.
3. Christie, M.J., Summers, R.J., Stephenson, J.A., Cook, C.J., and Beart, P.M. 1987. 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: 425-439.
4. Fallon, J.H. and Loughlin, S.E. 1995. Substantia nigra. In The rat nervous system (ed. G. Paxinos), pp. 215-237. Academic Press, San Diego, CA.
5. Floresco, S.B., Yang, C.R., Phillips, A.G., and Blaha, C.D. 1998. Basolateral amygdala stimulation evokes glutamate receptor-dependent dopamine efflux in the nucleus accumbens of the anaesthetized rat. Eur. J. Neurosci. 10: 1241-1251.
6. Hatfield, T. and McGaugh, J.L. 1999. Norepinephrine infused into the basolateral amygdala posttraining enhances retention in a spatial water maze task. Neurobiol. Learn. Mem. 71: 232-239.
7. Heimer, L., Zahm, D.S., Churchill, L., Kalivas, P.W., and Wohltmann, C. 1991. Specificity in the projection patterns of accumbal core and shell in the rat. Neuroscience. 41: 89-125.
8. Heimer, L., Zahm, D.S., and Alheid, G.F. 1995. Basal ganglia. In The rat nervous system (ed. G. Paxinos), pp. 579-628. Academic Press, San Diego, CA.
9. Hernandez, L. and Hoebel, B.G. 1988. Food reward and cocaine increase extracellular dopamine in the nucleus accumbens as measured by microdialysis. Life Sci. 42: 1705-1712.
10. Howland, J.G., Taepavarapruk, P., and Phillips, A.G. 2002. 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: 1137-1145.
11. Hui, G.K., Figueroa, I.R., Poytress, B.S., Roozendaal, B., McGaugh, J.L., and Weinberger, N.M. 2004. Memory enhancement of classical fear conditioning by post-training injections of corticosterone in rats. Neurobiol Learn Mem. 81: 67-74.
12. Inglis, F.M. and Moghaddam, B. 1999. Dopaminergic innervation of the amygdala is highly responsive to stress. J. Neurochem. 72: 1088-1094.
13. Inoue, T., Tsuchiya, K., and Koyama, T. 1994. Regional changes in dopamine and serotonin activation with various intensity of physical and psychological stress in the rat brain. Pharmacol. Biochem. Behav. 49: 911-920.
14. Kalivas, P.W. and Duffy, P. 1995. Selective activation of dopamine transmission in the shell of the nucleus accumbens by stress. Brain Res. 675: 325-328.
15. Kalivas, P.W., Duffy, P., and Mackler, S.A. 1999. Interrupted expression of nac-1 augments the behavioral responses to cocaine. Synapse. 33: 153-159.
16. Kelley, A.E., Domesick, V.B., and Nauta, W.J. 1982. The amygdalostriatal projection in the rat - an anatomical study by anterograde and retrograde tracing methods. Neuroscience. 7: 615-630.
17. LaLumiere, R.T., Buen, T.V., and McGaugh, J.L. 2003. Post-training intra-basolateral amygdala infusions of norepinephrine enhance consolidation of memory for contextual fear conditioning. J. Neurosci. 23: 6754-6758.
18. LaLumiere, R.T., Nguyen, L.T., and McGaugh, J.L. 2004. Post-training intrabasolateral amygdala infusions of dopamine modulate consolidation of inhibitory avoidance memory: Involvement of noradrenergic and cholinergic systems. Eur. J. Neurosci. 20: 2804-2810.
19. Liang, K.C., McGaugh, J.L., and Yao, H.Y. 1990. Involvement of amygdala pathways in the influence of post-training intra-amygdala norepinephrine and peripheral epinephrine on memory storage. Brain Res. 508: 225-233.
20. McGaugh, J.L. 2004. The amygdala modulates the consolidation of memories of emotionally arousing experiences. Annu. Rev. Neurosci. 27: 1-28.
21. Meredith, G.E., Agolia, R., Arts, M.P., Groenewegen, H.J., and Zahm, D.S. 1992. Morphological differences between projection neurons of the core and shell in the nucleus accumbens of the rat. Neuroscience 50: 149-162.
22. Miranda, M.I. and McGaugh, J.L. 2004. Enhancement of inhibitory avoidance and conditioned taste aversion memory with insular cortex infusions of 8-br-camp: Involvement of the basolateral amygdala. Learn. Mem. 11: 312-317.
23. Miranda, M.I., LaLumiere, R.T., Buen, T.V., Bermudez-Rattoni, F., and McGaugh, J.L. 2003. Blockade of noradrenergic receptors in the basolateral amygdala impairs taste memory. Eur. J. Neurosci. 18: 2605-2610.
24. Moore, H., Fadel, J., Sarter, M., and Bruno, J.P. 1999. Role of accumbens and cortical dopamine receptors in the regulation of cortical acetylcholine release. Neuroscience 88: 811-822.
25. Neigh, G.N., Arnold, H.M., Rabenstein, R.L., Sarter, M., and Bruno, J.P. 2004. Neuronal activity in the nucleus accumbens is necessary for performance-related increases in cortical acetylcholine release. Neuroscience 123: 635-645.
26. Packard, M.G., Cahill, L., and McGaugh, J.L. 1994. Amygdala modulation of hippocampal-dependent and caudate nucleus-dependent memory processes. Proc. Natl. Acad. Sci. 91: 8477-8481.
27. Packard, M.G., Introini-Collison, I., and McGaugh, J.L. 1996. Stria terminalis lesions attenuate memory enhancement produced by intracaudate nucleus injections of oxotremorine. Neurobiol. Learn. Mem. 65: 278-282.
28. Paxinos, G. and Watson, C. 1997. The rat brain in stereotaxic coordinates. Academic Press, San Diego, CA.
29. _. 2005. The rat brain in stereotaxic coordinates. Elsevier Academic Press, Amsterdam.
30. Pezze, M.A. and Feldon, J. 2004. Mesolimbic dopaminergic pathways in fear conditioning. Prog. Neurobiol. 74: 301-320.
31. Pezze, M.A., Feldon, J., and Murphy, C.A. 2002. Increased conditioned fear response and altered balance of dopamine in the shell and core of the nucleus accumbens during amphetamine withdrawal. Neuropharmacology 42: 633-643.
32. Power, A.E. and McGaugh, J.L. 2002. Phthalic acid amygdalopetal lesion of the nucleus basalis magnocellularis induces reversible memory deficits in rats. Neurobiol. Learn. Mem. 77: 372-388.
33. Power, A.E., Thal, L.J., and McGaugh, J.L. 2002. Lesions of the nucleus basalis magnocellularis induced by 192 igg-saporin block memory enhancement with posttraining norepinephrine in the basolateral amygdala. Proc. Natl. Acad. Sci. 99: 2315-2319.
34. Power, A.E., McIntyre, C.K., Litmanovich, A., and McGaugh, J.L. 2003. Cholinergic modulation of memory in the basolateral amygdala involves activation of both m1 and m2 receptors. Behav. Pharmacol. 14: 207-213.
35. Robinson, T.G. and Beart, P.M. 1988. Excitant amino acid projections from rat amygdala and thalamus to nucleus accumbens. Brain Res. Bull. 20: 467-471.
36. Roozendaal, B. 2000. 1999 Curt P. Richter award. Glucocorticoids and the regulation of memory consolidation. Psychoneuroendocrinology. 25: 213-238.
37. Roozendaal, B. and McGaugh, J.L. 1996. Amygdaloid nuclei lesions differentially affect glucocorticoid-induced memory enhancement in an inhibitory avoidance task. Neurobiol. Learn Mem. 65: 1-8.
38. Roozendaal, B., Nguyen, B.T., Power, A.E., and McGaugh, J.L. 1999. Basolateral amygdala noradrenergic influence enables enhancement of memory consolidation induced by hippocampal glucocorticoid receptor activation. Proc. Natl. Acad. Sci. 96: 11642-11647.
39. Roozendaal, B., de Quervain, D.J., Ferry, B., Setlow, B., and McGaugh, J.L. 2001. Basolateral amygdala-nucleus accumbens interactions in mediating glucocorticoid enhancement of memory consolidation. J. Neurosci. 21: 2518-2525.
40. Salamone, J.D. 1994. The involvement of nucleus accumbens dopamine in appetitive and aversive motivation. Behav. Brain Res.. 61: 117-133.
41. Schwienbacher, I., Fendt, M., and Schnitzler, H.U. 2005. Amphetamine injections into the nucleus accumbens affect neither acquisition/expression of conditioned fear nor baseline startle response. Exp. Brain Res. 160: 538-544.
42. Setlow, B. and McGaugh, J.L. 1998. Sulpiride infused into the nucleus accumbens posttraining impairs memory of spatial water maze training. Behav. Neurosci. 112: 603-610.
43. _. 1999. Differential effects of immediate posttraining sulpiride microinfusions into the nucleus accumbens shell and core on morris water maze retention. Psychobiology 27: 248-255.
44. Setlow, B., Roozendaal, B., and McGaugh, J.L. 2000. Involvement of a basolateral amygdala complex-nucleus accumbens pathway in glucocorticoid-induced modulation of memory consolidation. Eur. J. Neurosci. 12: 367-375.
45. Ungless, M.A. 2004. Dopamine: The salient issue. Trends Neurosci. 27: 702-706.
46. Wise, R.A. and Rompre, P.P. 1989. Brain dopamine and reward. Annu. Rev. Psychol. 40: 191-225.
47. Woolf, N.J. 1991. Cholinergic systems in mammalian brain and spinal cord. Prog. Neurobiol. 37: 475-524.
48. Zaborsky, L., Cullinan, W.E., and Braun, A. 1991. Afferents to basal forebrain cholinergic projection neurons: An update. In The basal forebrain: Anatomy to function (ed. T.C. Napier et al.), pp. 43-100. Plenum Press, New York.
49. Zahm, D.S. and Heimer, L. 1990. Two transpallidal pathways originating in the rat nucleus accumbens. J. Comp. Neurol. 302: 437-446.