Noradrenergic actions in the basolateral complex of the amygdala modulate Arc expression in hippocampal synapses and consolidation of aversive and non-aversive memory

Neurobiology of Learning and Memory

Volumn 115, Issue , 2014, Pages 49-57

  McReynolds, Jayme R ^a   Anderson, Kelly M ^b   Donowho, Kyle M ^c   McIntyre, Christa K ^c  

^a MARQUETTE UNIVERSITY   (United States)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^c UNIVERSITY OF TEXAS AT DALLAS   (United States)

Author keywords

Aversive learning; BLA; Dorsal hippocampus; Emotional arousal; Norepinephrine; Object recognition

Indexed keywords

ACTIVITY REGULATED CYTOSKELETON ASSOCIATED PROTEIN; CLENBUTEROL; NORADRENALIN; ACTIVITY REGULATED CYTOSKELETAL-ASSOCIATED PROTEIN; BETA ADRENERGIC RECEPTOR STIMULATING AGENT; CYTOSKELETON PROTEIN; NERVE PROTEIN;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL TISSUE; AROUSAL; ARTICLE; AVERSION; BASOLATERAL AMYGDALA; CONTROLLED STUDY; EMOTION; HIPPOCAMPUS; IMMUNOBLOTTING; LATENT PERIOD; MALE; MEMORY CONSOLIDATION; NERVE CELL PLASTICITY; NONHUMAN; NORADRENERGIC SYSTEM; NOVEL OBJECT RECOGNITION TEST; PASSIVE AVOIDANCE; PROTEIN DETERMINATION; PROTEIN EXPRESSION; RAT; SYNAPSE; TASK PERFORMANCE; WESTERN BLOTTING; ADRENERGIC NERVE CELL; ANIMAL; BIOSYNTHESIS; DRUG EFFECTS; GENE EXPRESSION REGULATION; MEMORY; METABOLISM; PHYSIOLOGY; SPRAGUE DAWLEY RAT;

ADRENERGIC BETA-AGONISTS; ADRENERGIC NEURONS; ANIMALS; BASOLATERAL NUCLEAR COMPLEX; CLENBUTEROL; CYTOSKELETAL PROTEINS; GENE EXPRESSION REGULATION; HIPPOCAMPUS; MALE; MEMORY; NERVE TISSUE PROTEINS; RATS; RATS, SPRAGUE-DAWLEY; SYNAPSES;

EID: 84908367256     PISSN: 10747427     EISSN: 10959564     Source Type: Journal    
DOI: 10.1016/j.nlm.2014.08.016     Document Type: Article

References (66)

1. Abercrombie E.D., Jacobs B.L. Single-unit response of noradrenergic neurons in the locus coeruleus of freely moving cats. I. Acutely presented stressful and nonstressful stimuli. Journal of Neuroscience 1987, 7:2837-2843.
2. Bergado J.A., Lucas M., Richter-Levin G. Emotional tagging - A simple hypothesis in a complex reality. Progress in Neurobiology 2011, 94:64-76.
3. Bramham C.R. Local protein synthesis, actin dynamics, and LTP consolidation. Current Opinion in Neurobiology 2008, 18:524-531.
4. Broadbent N.J., Squire L.R., Clark R.E. Spatial memory, recognition memory, and the hippocampus. Proceedings of the National Academy of Sciences of the United States of America 2004, 101:14515-14520.
5. Cahill L., Haier R.J., Fallon J., Alkire M.T., Tang C., Keator D., et al. Amygdala activity at encoding correlated with long-term, free recall of emotional information. Proceedings of the National Academy of Sciences of the United States of America 1996, 93:8016-8021.
6. Clarke J.R., Rossato J.I., Monteiro S., Bevilaqua L.R., Izquierdo I., Cammarota M. Posttraining activation of CB1 cannabinoid receptors in the CA1 region of the dorsal hippocampus impairs object recognition long-term memory. Neurobiology of Learning and Memory 2008, 90:374-381.
7. Cohen S.J., Munchow A.H., Rios L.M., Zhang G., Asgeirsdottir H.N., Stackman R.W. The rodent hippocampus is essential for nonspatial object memory. Current Biology 2013, 23:1685-1690.
8. Crystal J.D. Elements of episodic-like memory in animal models. Behavioural Processes 2009, 80:269-277.
9. Czerniawski J., Ree F., Chia C., Ramamoorthi K., Kumata Y., Otto T.A. The importance of having Arc: Expression of the immediate-early gene Arc is required for hippocampus-dependent fear conditioning and blocked by NMDA receptor antagonism. Journal of Neuroscience 2011, 31:11200-11207.
10. Da Cunha C., Roozendaal B., Vazdarjanova A., McGaugh J.L. Microinfusions of flumazenil into the basolateral but not the central nucleus of the amygdala enhance memory consolidation in rats. Neurobiology of Learning and Memory 1999, 72:1-7.
11. da Silveira C.K., Furini C.R., Benetti F., Monteiro Sda C., Izquierdo I. The role of histamine receptors in the consolidation of object recognition memory. Neurobiology of Learning and Memory 2013, 103:64-71.
12. Dong E., Caruncho H., Liu W.S., Smalheiser N.R., Grayson D.R., Costa E., et al. A reelin-integrin receptor interaction regulates Arc mRNA translation in synaptoneurosomes. Proceedings of the National Academy of Sciences of the United States of America 2003, 100:5479-5484.
13. Dziembowska M., Milek J., Janusz A., Rejmak E., Romanowska E., Gorkiewicz T., Tiron A., Bramham C.R., Kaczmarek L. Activity-dependent local translation of matrix metalloproteinase-9. Journal of Neuroscience 2012, 32:14538-14547.
14. Farris S., Lewandowski G., Cox C.D., Steward O. Selective localization of Arc mRNA in dendrites involves activity - And translation-dependent mRNA degradation. Journal of Neuroscience 2014, 34:4481-4493.
15. Ferbinteanu J., McDonald R.J. Dorsal/ventral hippocampus, fornix, and conditioned place preference. Hippocampus 2001, 11:187-200.
16. Ferry B., Roozendaal B., McGaugh J.L. Basolateral amygdala noradrenergic influences on memory storage are mediated by an interaction between beta- and alpha1-adrenoceptors. Journal of Neuroscience 1999, 19:5119-5123.
17. Frey U., Morris R.G. Synaptic tagging: Implications for late maintenance of hippocampal long-term potentiation. Trends in Neurosciences 1998, 21:181-188.
18. Galvez R., Mesches M.H., McGaugh J.L. Norepinephrine release in the amygdala in response to footshock stimulation. Neurobiology of Learning and Memory 1996, 66:253-257.
19. Guzowski J.F., Lyford G.L., Stevenson G.D., Houston F.P., McGaugh J.L., Worley P.F., et al. Inhibition of activity-dependent Arc protein expression in the rat hippocampus impairs the maintenance of long-term potentiation and the consolidation of long-term memory. Journal of Neuroscience 2000, 20:3993-4001.
20. Hamann S.B., Ely T.D., Grafton S.T., Kilts C.D. Amygdala activity related to enhanced memory for pleasant and aversive stimuli. Nature Neuroscience 1999, 2:289-293.
21. Hammond R.S., Tull L.E., Stackman R.W. On the delay-dependent involvement of the hippocampus in object recognition memory. Neurobiology of Learning and Memory 2004, 82:26-34.
22. Holloway-Erickson C.M., McReynolds J.R., McIntyre C.K. Memory-enhancing intra-basolateral amygdala infusions of clenbuterol increase Arc and CaMKIIalpha protein expression in the rostral anterior cingulate cortex. Frontiers in Behavioral Neuroscience 2012, 6:17.
23. Hu H., Real E., Takamiya K., Kang M.G., Ledoux J., Huganir R.L., et al. Emotion enhances learning via norepinephrine regulation of AMPA-receptor trafficking. Cell 2007, 131:160-173.
24. Huang F., Chotiner J.K., Steward O. Actin polymerization and ERK phosphorylation are required for Arc/Arg3.1 mRNA targeting to activated synaptic sites on dendrites. Journal of Neuroscience 2007, 27:9054-9067.
25. Huff N.C., Frank M., Wright-Hardesty K., Sprunger D., Matus-Amat P., Higgins E., et al. Amygdala regulation of immediate-early gene expression in the hippocampus induced by contextual fear conditioning. Journal of Neuroscience 2006, 26:1616-1623.
26. Ihalainen J.A., Riekkinen P., Feenstra M.G. Comparison of dopamine and noradrenaline release in mouse prefrontal cortex, striatum and hippocampus using microdialysis. Neuroscience Letters 1999, 277:71-74.
27. Ikegaya Y., Nakanishi K., Saito H., Abe K. Amygdala beta-noradrenergic influence on hippocampal long-term potentiation in vivo. NeuroReport 1997, 8:3143-3146.
28. Jobim P.F., Pedroso T.R., Werenicz A., Christoff R.R., Maurmann N., Reolon G.K., et al. Impairment of object recognition memory by rapamycin inhibition of mTOR in the amygdala or hippocampus around the time of learning or reactivation. Behavioural Brain Research 2012, 228:151-158.
29. Kelly M.P., Deadwyler S.A. Acquisition of a novel behavior induces higher levels of Arc mRNA than does overtrained performance. Neuroscience 2002, 110:617-626.
30. LaLumiere R.T., Buen T.V., McGaugh J.L. Post-training intra-basolateral amygdala infusions of norepinephrine enhance consolidation of memory for contextual fear conditioning. Journal of Neuroscience 2003, 23:6754-6758.
31. Lenck-Santini P.P., Rivard B., Muller R.U., Poucet B. Study of CA1 place cell activity and exploratory behavior following spatial and nonspatial changes in the environment. Hippocampus 2005, 15:356-369.
32. McGaugh J.L. Memory - A century of consolidation. Science 2000, 287:248-251.
33. McGaugh J.L. The amygdala modulates the consolidation of memories of emotionally arousing experiences. Annual Review of Neuroscience 2004, 27:1-28.
34. McIntyre C.K., Hatfield T., McGaugh J.L. Amygdala norepinephrine levels after training predict inhibitory avoidance retention performance in rats. European Journal of Neuroscience 2002, 16:1223-1226.
35. McIntyre C.K., Miyashita T., Setlow B., Marjon K.D., Steward O., Guzowski J.F., et al. Memory-influencing intra-basolateral amygdala drug infusions modulate expression of Arc protein in the hippocampus. Proceedings of the National Academy of Sciences of the United States of America 2005, 102:10718-10723.
36. McIntyre C.K., Ragozzino M.E., Gold P.E. Intra-amygdala infusions of scopolamine impair performance on a conditioned place preference task but not a spatial radial maze task. Behavioural Brain Research 1998, 95:219-226.
37. McReynolds J.R., Donowho K., Abdi A., McGaugh J.L., Roozendaal B., McIntyre C.K. Memory-enhancing corticosterone treatment increases amygdala norepinephrine and Arc protein expression in hippocampal synaptic fractions. Neurobiology of Learning and Memory 2010, 93:312-321.
38. McReynolds J.R., McIntyre C.K. Emotional modulation of the synapse. Reviews in the Neurosciences 2012, 23:449-461.
39. Messaoudi E., Kanhema T., Soule J., Tiron A., Dagyte G., da Silva B., et al. Sustained Arc/Arg3.1 synthesis controls long-term potentiation consolidation through regulation of local actin polymerization in the dentate gyrus in vivo. Journal of Neuroscience 2007, 27:10445-10455.
40. Miller S., Yasuda M., Coats J.K., Jones Y., Martone M.E., Mayford M. Disruption of dendritic translation of CaMKIIalpha impairs stabilization of synaptic plasticity and memory consolidation. Neuron 2002, 36:507-519.
41. Miranda M.I., Quirarte G.L., Rodriguez-Garcia G., McGaugh J.L., Roozendaal B. Glucocorticoids enhance taste aversion memory via actions in the insular cortex and basolateral amygdala. Learning & Memory 2008, 15:468-476.
42. Miyashita T., Williams C.L. Peripheral arousal-related hormones modulate norepinephrine release in the hippocampus via influences on brainstem nuclei. Behavioural Brain Research 2004, 153:87-95.
43. Okuda S., Roozendaal B., McGaugh J.L. Glucocorticoid effects on object recognition memory require training-associated emotional arousal. Proceedings of the National Academy of Sciences of the United States of America 2004, 101:853-858.
44. Packard M.G., Cahill L., McGaugh J.L. Amygdala modulation of hippocampal-dependent and caudate nucleus-dependent memory processes. Proceedings of the National Academy of Sciences of the United States of America 1994, 91:8477-8481.
45. Paxinos G., Watson C. The rat brain in stereotaxic coordinates 2005, Elsevier Academic Press, Amsterdam; Boston. 5th ed.
46. Quirarte G.L., Galvez R., Roozendaal B., McGaugh J.L. Norepinephrine release in the amygdala in response to footshock and opioid peptidergic drugs. Brain Research 1998, 808:134-140.
47. Ramirez-Amaya V., Vazdarjanova A., Mikhael D., Rosi S., Worley P.F., Barnes C.A. Spatial exploration-induced Arc mRNA and protein expression: Evidence for selective, network-specific reactivation. Journal of Neuroscience 2005, 25:1761-1768.
48. Redondo R.L., Morris R.G. Making memories last: The synaptic tagging and capture hypothesis. Nature Reviews Neuroscience 2011, 12:17-30.
49. Richter J.D., Lorenz L.J. Selective translation of mRNAs at synapses. Current Opinion in Neurobiology 2002, 12:300-304.
50. Richter-Levin G., Akirav I. Emotional tagging of memory formation - In the search for neural mechanisms. Brain Research Reviews 2003, 43:247-256.
51. Roozendaal B., Castello N.A., Vedana G., Barsegyan A., McGaugh J.L. Noradrenergic activation of the basolateral amygdala modulates consolidation of object recognition memory. Neurobiology of Learning and Memory 2008, 90:576-579.
52. Roozendaal B., Hui G.K., Hui I.R., Berlau D.J., McGaugh J.L., Weinberger N.M. Basolateral amygdala noradrenergic activity mediates corticosterone-induced enhancement of auditory fear conditioning. Neurobiology of Learning and Memory 2006, 86:249-255.
53. Roozendaal B., McGaugh J.L. Amygdaloid nuclei lesions differentially affect glucocorticoid-induced memory enhancement in an inhibitory avoidance task. Neurobiology of Learning and Memory 1996, 65:1-8.
54. Roozendaal B., Nguyen B.T., Power A.E., McGaugh J.L. Basolateral amygdala noradrenergic influence enables enhancement of memory consolidation induced by hippocampal glucocorticoid receptor activation. Proceedings of the National Academy of Sciences of the United States of America 1999, 96:11642-11647.
55. Roozendaal B., Okuda S., Van der Zee E.A., McGaugh J.L. Glucocorticoid enhancement of memory requires arousal-induced noradrenergic activation in the basolateral amygdala. Proceedings of the National Academy of Sciences of the United States of America 2006, 103:6741-6746.
56. Shin C.Y., Kundel M., Wells D.G. Rapid, activity-induced increase in tissue plasminogen activator is mediated by metabotropic glutamate receptor-dependent mRNA translation. Journal of Neuroscience 2004, 24:9425-9433.
57. Steward O., Wallace C.S., Lyford G.L., Worley P.F. Synaptic activation causes the mRNA for the IEG Arc to localize selectively near activated postsynaptic sites on dendrites. Neuron 1998, 21:741-751.
58. Steward O., Worley P.F. Selective targeting of newly synthesized Arc mRNA to active synapses requires NMDA receptor activation. Neuron 2001, 30:227-240.
59. Steward O., Worley P. Local synthesis of proteins at synaptic sites on dendrites: Role in synaptic plasticity and memory consolidation?. Neurobiology of Learning and Memory 2002, 78:508-527.
60. Sutton M.A., Schuman E.M. Dendritic protein synthesis, synaptic plasticity, and memory. Cell 2006, 127:49-58.
61. Tanaka M. Emotional stress and characteristics of brain noradrenaline release in the rat. Industrial Health 1999, 37:143-156.
62. Tanaka M., Kohno Y., Nakagawa R., Ida Y., Takeda S., Nagasaki N., et al. Regional characteristics of stress-induced increases in brain noradrenaline release in rats. Pharmacology, Biochemistry and Behavior 1983, 19:543-547.
63. Thomas M.J., Moody T.D., Makhinson M., O'Dell T.J. Activity-dependent beta-adrenergic modulation of low frequency stimulation induced LTP in the hippocampal CA1 region. Neuron 1996, 17:475-482.
64. Waung M.W., Pfeiffer B.E., Nosyreva E.D., Ronesi J.A., Huber K.M. Rapid translation of Arc/Arg3.1 selectively mediates mGluR-dependent LTD through persistent increases in AMPAR endocytosis rate. Neuron 2008, 59:84-97.
65. Yin Y., Edelman G.M., Vanderklish P.W. The brain-derived neurotrophic factor enhances synthesis of Arc in synaptoneurosomes. Proceedings of the National Academy of Sciences of the United States of America 2002, 99:2368-2373.
66. Zigmond R.E., Schon F., Iversen L.L. Increased tyrosine hydroxylase activity in the locus coeruleus of rat brain stem after reserpine treatment and cold stress. Brain Research 1974, 70:547-552.