Stimulus intensity-dependent modulations of hippocampal long-term potentiation by basolateral amygdala priming

Frontiers in Cellular Neuroscience

Volumn , Issue MAY 2012, 2012, Pages

  Li, Zexuan ^a,b   Richter Levin, Gal ^a  

^a UNIVERSITY OF HAIFA   (Israel)

^b CENTRAL SOUTH UNIVERSITY   (China)

Author keywords

Amygdala; Emotional memory; Limbic system; Plasticity; Rat; Stress

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BASOLATERAL AMYGDALA; BRAIN REGION; CONTROLLED STUDY; DENTATE GYRUS; EVOKED RESPONSE; HIPPOCAMPAL CA1 REGION; LONG TERM POTENTIATION; MALE; MEMORY; NERVE CELL PLASTICITY; NERVE STIMULATION; NEUROMODULATION; NONHUMAN; RAT; STIMULUS RESPONSE;

EID: 84864007919     PISSN: 16625102     EISSN: None     Source Type: Journal    
DOI: 10.3389/fncel.2012.00021     Document Type: Article

References (104)

1. Abe, K. (2001). Modulation of hippocampal long-term potentiation by the amygdala: a synaptic mechanism linking emotion and memory. Jpn. J. Pharmacol. 86, 18-22.
2. Abrahams, S., Morris, R. G., Polkey, C. E., Jarosz, J. M., Cox, T. C., Graves, M., and Pickering, A. (1999). Hippocampal involvement in spatial and working memory: a structural MRI analysis of patients with unilateral mesial temporal lobe sclerosis. Brain Cogn. 41, 39-65.
3. Ahmed, T., Frey, J. U., and Korz, V. (2006). Long-term effects of brief acute stress on cellular signaling and hippocampal LTP. J. Neurosci. 26, 3951-3958.
4. Akirav, I., and Richter-Levin, G. (1999a). Biphasic modulation of hippocampal plasticity by behavioral stress and basolateral amygdala stimulation in the rat. J. Neurosci. 19, 10530-10535.
5. Akirav, I., and Richter-Levin, G. (1999b). Priming stimulation in the basolateral amygdala modulates synaptic plasticity in the rat dentate gyrus. Neurosci. Lett. 270, 83-86.
6. Akirav, I., and Richter-Levin, G. (2002). Mechanisms of amygdala modulation of hippocampal plasticity. J. Neurosci. 22, 9912-9921.
7. Akirav, I., and Richter-Levin, G. (2006). Factors that determine the non-linear amygdala influence on hippocampus-dependent memory. Dose Response 4, 22-37.
8. Almaguer-Melian, W., Martinez-Marti, L., Frey, J. U., and Bergado, J. A. (2003). The amygdala is part of the behavioural reinforcement system modulating long-term potentiation in rat hippocampus. Neuroscience 119, 319-322.
9. Almaguer-Melian, W., Rojas-Reyes, Y., Alvare, A., Rosillo, J. C., Frey, J. U., and Bergado, J. A. (2005). Long-term potentiation in the dentate gyrus in freely moving rats is reinforced by intraventricular application of norepinephrine, but not oxotremorine. Neurobiol. Learn. Mem. 83, 72-78.
10. Berretta, S. (2005). Cortico-amygdala circuits: role in the conditioned stress response. Stress 8, 221-232.
11. Bliss, T. V., and Collingridge, G. L. (1993). A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361, 31-39.
12. Bramham, C. R., Southard, T., Ahlers, S. T., and Sarvey, J. M. (1998). Acute cold stress leading to elevated corticosterone neither enhances synaptic efficacy nor impairs LTP in the dentate gyrus of freely moving rats. Brain Res. 789, 245-255.
13. Buffalari, D. M., and Grace, A. A. (2009). Anxiogenic modulation of spontaneous and evoked neuronal activity in the basolateral amygdala. Neuroscience 2163, 1069-1077.
14. Cahill, L. (2000). Neurobiological mechanisms of emotionally influenced, long-term memory. Prog. Brain Res. 126, 29-37.
15. Canli, T., Zhao, Z., Brewer, J., Gabrieli, J. D., and Cahill, L. (2000). Event-related activation in the human amygdala associates with later mem-oryfor individual emotional experience. J. Neurosci. 20, RC99.
16. Day, M., Langston, R., and Morris, R. G. (2003). Glutamate-receptor-mediated encoding and retrieval of paired-associate learning. Nature 424, 205-209.
17. De Kloet, E. R. (2004). Hormones and the stressed brain. Ann. N.Y. Acad. Sci. 1018, 1-15.
18. Diamond, D. M., Bennett, M. C., Stevens, K. E., Wilson, R. L., and Rose, G. M. (1990). Exposure to a novel environment interferes with the induction of hippocampal primed burst potentiation in the behaving rat. Psychobiology 18, 273-281.
19. Diamond, D. M., and Rose, G. M. (1994). Stress impairs LTP and hippocampal-dependent memory. Ann.N.Y. Acad. Sci. 746, 411-414.
20. Dunn, J. D., and Orr, S. E. (1984). Differential plasma corticosterone responses to hippocampal stimulation. Exp. Brain Res. 54, 1-6.
21. Eichenbaum, H., Schoenbaum, G., Young, B., and Bunsey, M. (1996). Functional organization of the hippocampal memory system. Proc. Natl. Acad. Sci. U.S.A. 93, 13500-13507.
22. Feldman, S., Conforti, N., and Siegel, R. A. (1982). Adrenocortical responses following limbic stimulation in rats with hypothalamic deafferenta-tions. Neuroendocrinology 35, 205-211.
23. Foy, M. R., Stanton, M. E., Levine, S., and Thompson, R. F. (1987). Behavioral stress impairs long-term potentiation in rodent hippocampus. Behav. Neural. Biol. 48, 138-149.
24. Frey, S., Bergado-Rosado, J., Seidenbecher, T., Pape, H. C., and Frey, J. U. (2001). Reinforcement of early long-term potentiation (early-LTP) in dentate gyrus by stimulation of the basolateral amygdala: heterosynaptic induction mechanisms of late-LTP. J. Neurosci. 21, 3697-3703.
25. Garcia, R. (2001). Stress, hippocampal plasticity, and spatial learning. Synapse 40, 180-183.
26. Garcia, R., Musleh, W., Tocco, G., Thompson, R. F., and Baudry, M. (1997). Time-dependent blockade of STP and LTP in hippocampal slices following acute stress in mice. Neurosci. Lett. 233, 41-44.
27. Gelinas, J. N., and Nguyen, P. V. (2005). Beta-adrenergic receptor activation facilitates induction of a protein synthesis-dependent late phase of long-term potentiation. J. Neurosci. 25, 3294-3303.
28. Gerges, N. Z., Stringer, J. L., and Alkadhi, K. A. (2001). Combination of hypothyroidism and stress abolishes early LTP in the CA1 but not dentate gyrus of hippocampus of adult rats. Brain Res. 922, 250-260.
29. Gold, P. E., and van Buskirk, R. (1978). Posttraining brain norepinephrine concentrations: correlation with retention performance of avoidance training and with peripheral epinephrine modulation of memory processing. Behav. Biol. 23, 509-520.
30. Goosens, K. A., and Maren, S. (2004). NMDA receptors are essential for the acquisition, but not expression, of conditional fear and associative spike firing in the lateral amygdala. Eur. J. Neurosci. 20, 537-548.
31. Hand, G. A., Hewitt, C. B., Fulk, L. J., Stock, H. S., Carson, J. A., Davis, J. M., and Wilson, M. A. (2002). Differential release of corticotropin-releasing hormone (CRH) in the amygdala during different types of stressors. Brain Res. 949, 122-130.
32. Hirata, R., Matsumoto, M., Judo, C., Yamaguchi, T., Izumi, T., Yoshioka, M., and Togashi, H. (2009). Possible relationship between the stress-induced synaptic response and metaplasticity in the hippocampal CA1 field of freely moving rats. Synapse 63, 549-556.
33. Hurlemann, R., Matusch, A., Hawellek, B., Klingmuller, D., Kolsch, H., Maier, W., and Dolan, R. J. (2007a). Emotion-induced retrograde amnesia varies as a function of noradrenergic-glucocorticoid activity. Psychopharmacology (Berl) 194, 261-269.
34. Hurlemann, R., Wagner, M., Hawellek, B., Reich, H., Pieperhoff, P., Amunts, K., Oros-Peusquens, A. M., Shah, N. J., Maier, W., and Dolan, R. J. (2007b). Amygdala control of emotion-induced forgetting and remembering: evidence from Urbach-Wiethe disease. Neuropsychologia 45, 877-884.
35. Ikegaya, Y., Saito, H., and Abe, K. (1995). High-frequency stimulation of the basolateral amygdala facilitates the induction of long-term potentiation in the dentate gyrus in vivo. Neurosci. Res. 22, 203-207.
36. Ikegaya, Y., Saito, H., and Abe, K. (1996). The basomedial and basolateral amygdaloid nuclei contribute to the induction of longterm potentiation in the dentate gyrus in vivo. Eur. J. Neurosci. 8, 1833-1839.
37. Ilin, Y., and Richter-Levin, G. (2009). ERK2 and CREB activation in the amygdala when an event is remembered as "Fearful" and not when it is remembered as "Instructive". J. Neurosci. Res. 87, 1823-1831.
38. Izaki, Y., and Arita, J. (1996). Longterm potentiation in the rat hippocampal CA1 region is inhibited selectively at the acquisition stage of discriminatory avoidance learning. Brain Res. 723, 162-168.
39. Izquierdo, I., and Medina, J. H. (1995). Correlation between the pharmacology of long-term potentiation and the pharmacology of memory. Neurobiol. Learn. Mem. 63, 19-32.
40. Katsuki, H., Izumi, Y., and Zorumski, C. F. (1997). Noradrenergic regulation of synaptic plasticity in the hippocampal CA1 region. J. Neurophysiol. 77, 3013-3020.
41. Kavushansky, A., and Richter-Levin, G. (2006). Effects of stress and corticosterone on activity and plasticity in the amygdala. J. Neurosci. Res. 84, 1580-1587.
42. Kavushansky, A., Vouimba, R. M., Cohen, H., and Richter-Levin, G. (2006). Activity and plasticity in the CA1, the dentate gyrus, and the amygdala following controllable vs uncontrollable water stress. Hippocampus 16, 35-42.
43. Kim, J. J., and Diamond, D. M. (2002). The stressed hippocampus, synaptic plasticity and lost memories. Nat. Rev. Neurosci. 3, 453-462.
44. Kim, J. J., Foy, M. R., and Thompson, R. F. (1996). Behavioral stress modifies hippocampal plasticity through N-methyl-D-aspartate receptor activation. Proc. Natl. Acad. Sci. U.S.A. 93, 4750-4753.
45. Kim, J. J., Koo, J. W., Lee, H. J., and Han, J. S. (2005). Amygdalar inactivation blocks stress-induced impairments in hippocampal long-term potentiation and spatial memory. J. Neurosci. 25, 1532-1539.
46. Kim, J. J., Lee, H. J., Han, J. S., and Packard, M. G. (2001). Amygdala is critical for stress-induced modulation of hippocampal long-term potentiation and learning. J. Neurosci. 21, 5222-5228.
47. Kim, J. J., and Fanselow, M. S. (1992). Modality-specific retrograde amnesia of fear. Science 256, 675-677.
48. Kogan, I., and Richter-Levin, G. (2008). Activation pattern of the limbic system following spatial learning under stress. Eur. J. Neurosci. 27, 715-722.
49. Korol, D. L., and Gold, P. E. (2008). Epinephrine converts long-term potentiation from transient to durable form in awake rats. Hippocampus 18, 81-91.
50. Korz, V., and Frey, J. U. (2003). Stress-related modulation of hippocampal long-term potentiation in rats: Involvement of adrenal steroid receptors. J. Neurosci. 23, 7281-7287.
51. Korz, V., and Frey, J. U. (2005). Bidirectional modulation of hippocampal long-term potentiation under stress and no-stress conditions in basolateral amygdala-lesioned and intact rats. J. Neurosci. 25, 7393-7400.
52. LaBar, K. S., and Cabeza, R. (2006). Cognitive neuroscience of emotional memory. Nat. Rev. Neurosci. 7, 54-64.
53. LeDoux, J. (2003). The emotional brain, fear, and the amygdala. Cell. Mol. Neurobiol. 23, 727-738.
54. LeDoux, J. E. (2000). Emotion circuits in the brain. Annu. Rev. Neurosci. 23, 155-184.
55. Li, Z., Zhou, Q., Li, L., Mao, R., Wang, M., Peng, W., Dong, Z., Xu, L., and Cao, J. (2005). Effects of unconditioned and conditioned aversive stimuli in an intense fear conditioning paradigm on synaptic plasticity in the hippocampal CA1 area in vivo. Hippocampus 15, 815-824.
56. Lupien, S. J., Maheu, F., Tu, M., Fiocco, A., and Schramek, T. E. (2007). The effects of stress and stress hormones on human cognition: Implications for the field of brain and cognition. Brain Cogn. 65, 209-237.
57. Malenka, R. C., and Bear, M. F. (2004). LTP and LTD: an embarrassment of riches. Neuron 44, 5-21.
58. Malenka, R. C., and Nicoll, R. A. (1999). Long-term potentiation-a decade of progress? Science 285, 1870-1874.
59. Maroun, M., and Akirav, I. (2008). Arousal and stress effects on consolidation and reconsolidation of recognition memory. Neuropsychopharmacology 33, 394-405.
60. Maroun, M., and Richter-Levin, G. (2003). Exposure to acute stress blocks the induction of long-term potentiation of the amygdala-prefrontal cortex pathway in vivo. J. Neurosci. 23, 4406-4409.
61. Martin, S. J., Grimwood, P. D., and Morris, R. G. (2000). Synaptic plasticity and memory: an evaluation of the hypothesis. Annu. Rev. Neurosci. 23, 649-711.
62. McGaugh, J. L. (2000). Memory-a century of consolidation. Science 287, 248-251.
63. McGaugh, J. L. (2004). The amygdala modulates the consolidation of memories of emotionally arousing experiences. Annu. Rev. Neurosci. 27, 1-28.
64. Mesches, M. H., Fleshner, M., Heman, K. L., Rose, G. M., and Diamond, D. M. (1999). Exposing rats to a predator blocks primed burst potentiation in the hippocampus in vitro. J. Neurosci. 19, RC18.
65. Miyashita, T., and Williams, C. L. (2004). Peripheral arousal-related hormones modulate norepinephrine release in the hippocampus via influences on brainstem nuclei. Behav. Brain Res. 153, 87-95.
66. Morris, R. G. (2001). Episodic-like memory in animals: psychological criteria, neural mechanisms and the value of episodic-like tasks to investigate animal models of neurode-generative disease. Philos. Trans. R. Soc. Lond. B Biol. Sci. 356, 1453-1465.
67. Morris, R. G., Garrud, P., Rawlins, J. N., and O'Keefe, J. (1982). Place navigation impaired in rats with hippocampal lesions. Nature 297, 681-683.
68. Nakao, K., Matsuyama, K., Matsuki, N., and Ikegaya, Y. (2004). Amygdala stimulation modulates hippocampal synaptic plasticity. Proc. Natl. Acad. Sci. U.S.A. 101, 14270-14275.
69. Packard, M. G., and Cahill, L. (2001). Affective modulation of multiple memory systems. Curr. Opin. Neurobiol. 11, 752-756.
70. Pavlides, C., Nivon, L. G., and McEwen, B. S. (2002). Effects of chronic stress on hippocampal long-term potentiation. Hippocampus 12, 245-257.
71. Paxinos, G., and Watson, C. (1997). The RatBrain in StereotaxicCoordinates, 3rd Ed. New York, NY: Academic Press.
72. Pelletier, J. G., Likhtik, E., Filali, M., and Pare, D. (2005). Lasting increases in basolateral amygdala activity after emotional arousal: implications for facilitated consolidation of emotional memories. Learn. Mem. 12, 96-102.
73. Phelps, E. A. (2004). Human emotion and memory: interactions of the amygdala and hippocampal complex. Curr. Opin. Neurobiol. 14, 198-202.
74. Phelps, E. A., and LeDoux, J. E. (2005). Contributions of the amygdala to emotion processing: from animal models to human behavior. Neuron 48, 175-187.
75. Phillips, R. G., and LeDoux, J. E. (1992). Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning. Behav. Neurosci. 106, 274-285.
76. Prickaerts, J., and Steckler, T. (2005). "Effects of glucocorticoids on emotion and cognitive processes in animals" in Handbook of Stress and the Brain, eds T. S. Steckler, N. H. Kalin, and J. M. H. M. Ruel (Amsterdam, The Netherlands: Elsevier), 359-385.
77. Richter-Levin, G. (2004). The amygdala, the hippocampus, and emotional modulation of memory. Neuroscientist 10, 31-39.
78. Richter-Levin, G., and Akirav, I. (2000). Amygdala-hippocampus dynamic interaction in relation to memory. Mol. Neurobiol. 22, 11-20.
79. Richter-Levin, G., and Maroun, M. (2010). Stress and amygdala suppression of metaplasticity in the medial prefrontal cortex. Cereb. Cortex20, 2433-2441.
80. Roozendaal, B. (2000). (1999) Curt, P. Richter award. Glucocorticoids and the regulation of memory consolidation. Psychoneuroendocrinology 25, 213-238.
81. Roozendaal, B. (2002). Stress and memory: opposing effects of glucocorticoids on memory consolidation and memory retrieval. Neurobiol. Learn. Mem. 78, 578-595.
82. Roozendaal, B., McEwen, B. S., and Chattarji, S. (2009). Stress, memory and the amygdala. Nat. Rev. Neurosci. 10, 423-433.
83. Rubin, R. T., Mandell, A. J., and Crandall, P. H. (1966). Corticosteroid responses to limbic stimulation in man: localization of stimulus sites. Science 153, 767-768.
84. Sacchetti, B., Lorenzini, C. A., Baldi, E., Bucherelli, C., Roberto, M., Tassoni, G., and Brunelli, M. (2002). Time-dependent inhibition of hippocampal LTP in vitro following contextual fear conditioning in the rat. Eur. J. Neurosci. 15, 143-150.
85. Seidenbecher, T., Reymann, K. G., and Balschun, D. (1997). A post-tetanic time window for the reinforcement of long-term potentiation by appetitive and aversive stimuli. Proc. Natl. Acad. Sci. U.S.A. 94, 1494-1499.
86. Shors, T. J., and Dryver, E. (1994). Effect of stress and long-term potentiation (LTP) on subsequent LTP and the theta burst response in the dentate gyrus. Brain Res. 666, 232-238.
87. Shors, T. J., Gallegos, R. A., and Breindl, A. (1997). Transient and persistent consequences of acute stress on long-term potentiation (LTP), synaptic efficacy, theta rhythms and bursts in area CA1 of the hippocampus. Synapse 26, 209-217.
88. Shors, T. J., Seib, T. B., Levine, S., and Thompson, R. F. (1989). Inescapable versus escapable shock modulates long-term potentiation in the rat hippocampus. Science 244, 224-226.
89. Spyrka, J., and Hess, G. (2010). Repeated restraint-induced modulation of long-term potentiation in the dentate gyrus of the mouse. Brain Res. 1320, 28-33.
90. Squire, L. R., and Zola, S. M. (1996). Structure and function of declarative and nondeclarative memory systems. Proc. Natl. Acad. Sci. U.S.A. 93, 13515-13522.
91. Thomas, M. J., Moody, T. D., Makhinson, M., and O'Dell, T. J. (1996). Activity-dependent beta-adrenergic modulation of low frequency stimulation induced LTP in the hippocampal CA1 region. Neuron 17, 475-482.
92. Thompson, R. F., and Kim, J. J. (1996). Memory systems in the brain and localization of a memory. Proc. Natl. Acad. Sci. U.S.A. 93, 13438-13444.
93. Tsoory, M. M., Vouimba, R. M., Akirav, I., Kavushansky, A., Avital, A., and Richter-Levin, G. (2008). Amygdala modulation of memory-related processes in the hippocampus: potential relevance to PTSD. Prog. Brain Res. 167, 35-51.
94. Vouimba, R. M., and Richter-Levin, G. (2005). Physiological dissociation in hippocampal subregions in response to amygdala stimulation. Cereb. Cortex 15, 1815-1821.
95. Vouimba, R. M., Yaniv, D., Diamond, D., and Richter-Levin, G. (2004). Effects of inescapable stress on LTP in the amygdala versus the dentate gyrus of freely behaving rats. Eur. J. Neurosci. 19, 1887-1894.
96. Vouimba, R. M., Yaniv, D., and Richter-Levin, G. (2007). Glucocorticoid receptors and beta-adrenoceptors in basolateral amygdala modulate synaptic plasticity in hippocampal dentate gyrus, but not in area CA1. Neuropharmacology 52, 244-252.
97. Wang, J., Akirav, I., and Richter-Levin, G. (2000). Short-term behavioral and electrophysiological consequences of underwater trauma. Physiol. Behav. 70, 327-332.
98. Watabe, A. M., Zaki, P. A., and O'Dell, T. J. (2000). Coactivation of beta-adrenergic and cholinergic receptors enhances the induction of long-term potentiation and syner-gisticallyactivatesmitogen-activated protein kinase in the hippocampal CA1 region. J. Neurosci. 20, 5924-5931.
99. Williams, C. L., Men, D., Clayton, E. C., and Gold, P. E. (1998). Norepinephrine release in the amygdala after systemic injection of epinephrine or escapable footshock: contribution of the nucleus of the solitary tract. Behav. Neurosci. 112, 1414-1422.
100. Xu, L., Anwyl, R., and Rowan, M. J. (1997). Behavioural stress facilitates the induction of long-term depression in the hippocampus. Nature 387, 497-500.
101. Yamada, K., McEwen, B. S., and Pavlides, C. (2003). Site and time dependent effects of acute stress on hippocampal long-term potentiation in freely behaving rats. Exp. Brain Res. 152, 52-59.
102. Yang, C. H., Huang, C. C., and Hsu, K. S. (2008). Differential roles of basolateral and central amygdala on the effects of uncontrollable stress on hippocampal synaptic plasticity. Hippocampus 18, 548-563.
103. Yarom, O., Maroun, M., and Richter-Levin, G. (2008). Exposure to forced swim stress alters local circuit activity and plasticity in the dentate gyrus of the hippocampus. Neural Plast. 2008, 194097.
104. van Marle, H. J., Hermans, E. J., Qin, S., and Fernández, G. (2009). From specificity to sensitivity: how acute stress affects amygdala processing of biologically salient stimuli. Biol. Psychiatry 66, 649-655.