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Molecular Neurobiology

, Volume 22, Issue 1–3, pp 11–20 | Cite as

Amygdala-hippocampus dynamic interaction in relation to memory

Article

Abstract

Typically the term “memory” refers to the ability to consciously remember past experiences or previously learned information. This kind of memory is considered to be dependent upon the hippocampal system. However, our emotional state seems to considerably affect the way in which we retain information and the accuracy with which the retention occurs. The amygdala is the most notably involved brain structure in emotional responses and the formation of emotional memories.

In this review we describe a system, composed of the amygdala and the hippocampus, that acts synergistically to form long-term memories of significantly emotional events. These brain structures are activated following an emotional event and cross-talk with each other in the process of consolidation. This dual activation of the amygdala and the hippocampus and the dynamics between them may be what gives emotionally based memories their uniqueness.

Index Entries

Amygdala hippocampus learning emotion stress 

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References

  1. 1.
    Rahman H., Freeman S. J., and Rahman M. (1992) The Neurobiological Basis of Memory and Behavior. Springer-Verlag, New York, NY.Google Scholar
  2. 2.
    Eichenbaum H. (1999) The hippocampus and mechanisms of declarative memory. Behav. Brain Res. 103, 123–133.PubMedCrossRefGoogle Scholar
  3. 3.
    Maguire E. A., Burgess N., and O’Keefe J. (1999) Human spatial navigation: cognitive maps, sexual dimorphism, and neural substrates. Curr. Opin. Neurobiol. 9, 171–177.PubMedCrossRefGoogle Scholar
  4. 4.
    Squire L. R. (1992) Memory and the hippocampus: a synthesis from findings with rats, monkeys, and humans. Psychol. Rev. 99, 195–231.PubMedCrossRefGoogle Scholar
  5. 5.
    Squire L. R. (1998) Memory systems. C.R. Acad. Sci. III. 321, 153–156.PubMedGoogle Scholar
  6. 6.
    Alvarez P., Zola-Morgan S., and Squire L. R. (1995) Damage limited to the hippocampal region produces long-lasting memory impairment in monkeys. J. Neurosci. 15, 3796–3807.PubMedGoogle Scholar
  7. 7.
    Bunsey M. and Eichenbaum H. (1996) Conservation of hippocampal memory function in rats and humans. Nature 18, 255–257.Google Scholar
  8. 8.
    Eichenbaum H. (1992) The hippocampal formation and declarative memory in animals. J. Cog. Neurosci. 4, 217–231.CrossRefGoogle Scholar
  9. 9.
    Morris R. G., Garrud P., Rawlins J. N., and O’Keefe J. (1982) Place navigation impaired in rats with hippocampal lesions. Nature 24, 681–683.CrossRefGoogle Scholar
  10. 10.
    Moser E., Moser M. B., and Andersen P. (1993) Spatial learning impairment parallels the magnitude of dorsal hippocampal lesions, but is hardly present following ventral lesions. J. Neurosci. 13, 3916–3925.PubMedGoogle Scholar
  11. 11.
    O’Keefe J. (1990) A computational theory of the hippocampal cognitive map. Prog. Brain Res. 83, 301–312.PubMedGoogle Scholar
  12. 12.
    McEwen B. S. and Sapolsky R. M. (1995) Stress and cognitive function. Curr. Opin. Neurobiol. 5, 205–216.PubMedCrossRefGoogle Scholar
  13. 13.
    Cahill L. and McGaugh J. L. (1996) Modulation of memory storage. Curr. Opin. Neurobiol. 6, 237–242.CrossRefGoogle Scholar
  14. 14.
    LeDoux J. E. (1993) Emotional memory systems in the brain. Behav. Brain Res. 20, 69–79.CrossRefGoogle Scholar
  15. 15.
    Kluver H. and Bucy P. (1937) “Psychic blindness” and other symptoms following bilateral temporal lobectomy in rhesus monkeys. Am. J. Physiol. 119, 352–353.Google Scholar
  16. 16.
    Weiskrantz L. (1956) Behavioral changes associated with ablation of the amygdaloid complex in monkeys. J. Comp. Physiol. Psychol. 49, 381–391.PubMedCrossRefGoogle Scholar
  17. 17.
    Davis M. (1992) The role of the amygdala in fear-potentiated startle: implications for animal models of anxiety. TIPS 13, 35–41.PubMedGoogle Scholar
  18. 18.
    McGaugh J. L., Introini-Collison I. B., Nagahara A. H., Cahill L., Brioni J. D., and Castellano C. (1990) Involvement of the amygdaloid complex in neuromodulatory influences on memory storage. Neurosci. Biobehav. Rev. 14, 425–431.PubMedCrossRefGoogle Scholar
  19. 19.
    Adolphs R., Tranel D., Damasio H., and Damasio A. R. (1995) Fear and the human amygdala. J. Neurosci. 15, 5879–5891.PubMedGoogle Scholar
  20. 20.
    Davis M. (1994) The role of the amygdala in emotional learning. Int. Rev. Neurobiol. 36, 225–266.PubMedCrossRefGoogle Scholar
  21. 21.
    LaBar K. S., LeDoux J. E., Spencer D. D., and Phelps E. A. (1995) Impaired fear conditioning following unilateral temporal lobectomy in humans. J. Neurosci. 15, 6846–6855.PubMedGoogle Scholar
  22. 22.
    Maren S., Aharonov G., and Fanselow M. S. (1996) Retrograde abolition of conditional fear after excitotoxic lesions in the basolateral amygdala of rats: absence of a temporal gradient. Behav. Neurosci. 110, 718–726.CrossRefGoogle Scholar
  23. 23.
    Conrad C. D., Galea L. A. M., Kuroda Y., and McEwen B. S. (1996) Chronic stress impairs rat spatial memory on the Y maze, and this effect is blocked by tianeptine pretreatment. Behav. Neurosci. 6, 1321–1334.Google Scholar
  24. 24.
    Conrad C. D., Lupien S. J., and McEwen B. S. (1999) Support for a bimodal role for type 2 adrenal steroid receptors in spatial memory. Neurobiol. Learn. Mem. 72, 39–46.PubMedCrossRefGoogle Scholar
  25. 25.
    Diamond D. M., Fleshner M., and Rose G. M. (1994) Psychological stress repeatedly blocks hippocampal primed burst potentiation in behaving rats. Behav. Brain Res. 30, 1–9.CrossRefGoogle Scholar
  26. 26.
    Diamond D. M., Park C. R., Heman K. L., and Rose G. M. (1999) Exposing rats to a predator impairs spatial working memory in the radial arm water maze. Hippocampus 9, 542–552.PubMedCrossRefGoogle Scholar
  27. 27.
    Diamond D. M. and Rose G. M. (1994) Stress impairs LTP and hippocampal-dependent memory. Ann. NY Acad. Sci. 746, 411–414.PubMedCrossRefGoogle Scholar
  28. 28.
    Luine V., Villegas M., Martinez C., and McEwen B. S. (1994) Repeated stress causes reversible impairments of spatial memory performance. Brain Res. 639, 167–170.PubMedCrossRefGoogle Scholar
  29. 29.
    Pavlides C., Ogawa S., Kimura A., and McEwen B. S. (1996) Role of adrenal steroid mineralocorticoid and glucocorticoid receptors in long-term potentiation in the CA1 field of hippocampal slices. Brain Res. 4, 229–235.Google Scholar
  30. 30.
    Pavlides C., Watanabe Y., and McEwen B. S. (1993) Effects of glucocorticoids on hippocampal long-term potentiation. Hippocampus 3, 183–192.PubMedCrossRefGoogle Scholar
  31. 31.
    Oitzl M. S. and de Kloet E. R. (1992) Selective corticosteroid antagonists modulate specific aspects of spatial orientation learning. Behav. Neurosci. 106, 62–71.PubMedCrossRefGoogle Scholar
  32. 32.
    Pugh C. R., Fleshner M., and Rudy J. W. (1997) Type II glucocorticoid receptor antagonists impair contextual but not auditory-cue fear conditioning in juvenile rats. Neurobiol. Learn. Mem. 67, 75–9.PubMedCrossRefGoogle Scholar
  33. 33.
    de Quervain D. J., Roozendaal B., and McGaugh J. L. (1998) Stress and glucocorticoids impair retrieval of long-term spatial memory. Nature 20, 787–790.Google Scholar
  34. 34.
    Sandi C. and Rose S. P. R. (1994a) Corticosteroid receptor antagonists are amnestic for passive avoidance learning in day-old chicks. Eur. J. Neurosci. 6, 1292–1297.PubMedCrossRefGoogle Scholar
  35. 35.
    Sandi C., Loscertales M., and Guaza C. (1997) Experience-dependent facilitating effect of corticosterone on spatial memory formation in the water maze. Eur. J. Neurosci. 9, 637–642.PubMedCrossRefGoogle Scholar
  36. 36.
    Akirav I. and Richter-Levin G. (1999b) Biphasic modulation of hippocampal plasticity by behavioral stress and basolateral amygdala stimulation in the rat. J. Neurosci. 1, 10,530–10,535.Google Scholar
  37. 37.
    Diamond D. M., Bennett M. C., Fleshner M., and Rose G. M. (1992) Inverted-U relationship between the level of peripheral corticosterone and the magnitude of hippocampal primed burst potentiation. Hippocampus 2, 421–430.PubMedCrossRefGoogle Scholar
  38. 38.
    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.PubMedCrossRefGoogle Scholar
  39. 39.
    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. 12, 41–44.CrossRefGoogle Scholar
  40. 40.
    Rey M., Carlier E., Talmi M., and Soumireu-Mourat B. (1994) Corticosterone effects on long-term potentiation in mouse hippocampal slices. Neuroendocrinology 60, 36–41.PubMedGoogle Scholar
  41. 41.
    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 14, 224–226.CrossRefGoogle Scholar
  42. 42.
    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.PubMedCrossRefGoogle Scholar
  43. 43.
    Wang J., Akirav I., and Richter-Levin G. (2000) Short-term behavioral and electrophysiological consequences of underwater trauma in the rat. Physiol. Behav. 70, 327–332.PubMedCrossRefGoogle Scholar
  44. 44.
    Xu L., Anwyl R., and Rowan M. J. (1997) Behavioral stress facilitates the induction of long-term depression in the hippocampus. Nature 29, 497–500.CrossRefGoogle Scholar
  45. 45.
    Xu L., Anwyl R., and Rowan M. J. (1998) Spatial exploration induces a persistent reversal of long-term potentiation in rat hippocampus. Nature 27, 891–894.CrossRefGoogle Scholar
  46. 46.
    Kerr D. S., Huggett A. M., and Abraham W. C. (1994) Modulation of hippocampal long-term potentiation and long-term depression by corticosteroid receptors activation. Psychobiology 22, 123–133.Google Scholar
  47. 47.
    Pavlides C., Kimura A., Magarinos A. M., and McEwen B. S. (1994) Type I adrenal steroid receptors prolong hippocampal long-term potentiation. Neuroreport 20, 2673–2677.CrossRefGoogle Scholar
  48. 48.
    Rose S. P. (1995) Cell-adhesion molecules, glucocorticoids and long-term-memory formation. TINS 18, 502–506.PubMedGoogle Scholar
  49. 49.
    Sandi C. and Rose S. P. R. (1994b) Corticosterone enhances long-term retention in one-day-old chicks trained in a weak passive avoidance learning paradigm. Brain Res. 647, 106–112.PubMedCrossRefGoogle Scholar
  50. 50.
    Diamond D. M., Fleshner M., Ingersoll N., and Rose G. M. (1996) Psychological stress impairs spatial working memory: relevance to electrophysiological studies of hippocampal function. Behav Neurosci. 110, 661–672.CrossRefGoogle Scholar
  51. 51.
    McGaugh J. L. (2000) Memory: a century of consolidation. Science 14, 248–251.CrossRefGoogle Scholar
  52. 52.
    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. 5, 225–233.CrossRefGoogle Scholar
  53. 53.
    Roozendaal B. and McGaugh J. L. (1996a) Amygdaloid nuclei lesions differentially affect glucocorticoid-induced memory enhancement in an inhibitory avoidance task. Neurobiol. Learn. Mem. 65, 1–8.CrossRefGoogle Scholar
  54. 54.
    Pikkarainen M., Ronkko S., Savander V., Insausti R., and Pitkanen A. (1999) Projections from the lateral, basal, and accessory basal nuclei of the amygdala to the hippocampal formation in rat. J. Comp. Neurol. 11, 229–260.CrossRefGoogle Scholar
  55. 55.
    Ikegaya Y., Saito H., and Abe K. (1994) Attenuated hippocampal long-term potentiation in basolateral amygdala-lesioned rats. Brain Res. 5, 157–164.CrossRefGoogle Scholar
  56. 56.
    Ikegaya Y., Saito H., and Abe K. (1995) Requirement of basolateral amygdala neuron activity for the induction of long-term potentiation in the dentate gyrus in vivo. Brain Res. 13, 351–354.CrossRefGoogle Scholar
  57. 57.
    Ikegaya Y., Abe K., Saito H., and Nishiyama N. (1995) Medial amygdala enhances synaptic transmission and synaptic plasticity in the dentate gyrus of rats in vivo. J. Neurophysiol. 74, 2201–2203.PubMedGoogle Scholar
  58. 58.
    Ikegaya Y., Saito H., and Abe K. (1996) The basomedial and basolateral amygdaloid nuclei contribute to the induction of long-term potentiation in the dentate gyrus in vivo. Eur. J. Neurosci. 8, 1833–1839.CrossRefGoogle Scholar
  59. 59.
    Jas J., Almaguer W., Frey J. U., and Bergado J. (2000) Lesioning the fimbriafornix impairs basolateral amygdala induced reinforcement of LTP in the dentate gyrus. Brain Res. 7, 186–189.CrossRefGoogle Scholar
  60. 60.
    Akirav I. and Richter-Levin G. (1999a) Priming stimulation in the basolateral amygdala modulates synaptic plasticity in the rat dentate gyrus. Neurosci. Lett. 30, 83–86.CrossRefGoogle Scholar
  61. 61.
    McGaugh J. L., Cahill L., and Roozendaal B. (1996) Involvement of the amygdala in memory storage: interaction with other brain systems. PNAS 26, 13,508–13,514.Google Scholar
  62. 62.
    Roozendaal B. and McGaugh J. L. (1996b) The memory-modulatory effects of glucocorticoids depend on an intact stria terminalis. Brain Res. 19, 243–250.Google Scholar
  63. 63.
    Packard M. G., Williams C. L., Cahill L., and McGaugh J. L. (1995) The anatomy of a memory modulatory system: from periphery to brain, in Neurobehavioral Plasticity: Learning, Development, and Response to Brain Insults (Speer N. E., Speer L., and Woodruff M., eds.), Erlbaum, Mahwah, NJ, pp. 149–184.Google Scholar
  64. 64.
    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. USA 30, 8477–8481.CrossRefGoogle Scholar
  65. 65.
    Roozendaal B. and McGaugh J. L. (1997) Basolateral amygdala lesions block the memory-enhancing effect of glucocorticoid administration in the dorsal hippocampus of rats. Eur. J. Neurosci. 9, 76–83.PubMedCrossRefGoogle Scholar
  66. 66.
    Roozendaal B., Portillo-Marquez G., and McGaugh J. L. (1996) Basolateral amygdala lesions block glucocorticoid-induced modulation of memory for spatial learning. Behav. Neurosci. 110, 1074–1083.CrossRefGoogle Scholar
  67. 67.
    Roozendaal B., Sapolsky R. M., and McGaugh J. L. (1998) Basolateral amygdala lesions block the disruptive effects of long-term adrenalectomy on spatial memory. Neuroscience 84, 453–465.PubMedCrossRefGoogle Scholar
  68. 68.
    Cahill L., Weinberger N. M., Roozendaal B., and McGaugh J. L. (1999) Is the amygdala a locus of “conditioned fear”? Some questions and caveats. Neuron 23, 227–228.PubMedCrossRefGoogle Scholar
  69. 69.
    Fanselow M. S. and LeDoux J. E. (1999) Why we think plasticity underlying Pavlovian fear conditioning occurs in the basolateral amygdala. Neuron 23, 229–232.PubMedCrossRefGoogle Scholar
  70. 70.
    Diamond D. M., Puls J. M., Park C. R., and Rose M. G. (2000) Differential effects of stress on hippocampal and amygdaloid LTP: insight into the neurobiology of traumatic memories, in Neuronal Mechanisms of Memory Formation: Concepts of Long-Term Potentiation and Beyond (Holscher C., ed.), Cambridge University Press, Cambridge, UK, pp. 379–404.Google Scholar
  71. 71.
    Lee Y., Walker D., and Davis M. (1996) Lack of a temporal gradient of retrograde amnesia following NMDA-induced lesions of the basolateral amygdala assessed with the fear-potentiated startle paradigm. Behav. Neurosci. 110, 836–839.CrossRefGoogle Scholar
  72. 72.
    Maren S., Aharonov G., and Fanselow M. S. (1996) Retrograde abolition of conditional fear after excitotoxic lesions in the basolateral amygdala of rats: absence of a temporal gradient. Behav. Neurosci. 110, 718–726.CrossRefGoogle Scholar
  73. 73.
    Wilensky A. E., Schafe G. E., and LeDoux J. E. (1999) Functional inactivation of the amygdala before but not after auditory fear conditioning prevents memory formation. J. Neurosci. 15, RC 48.Google Scholar
  74. 74.
    Liang K. C., McGaugh J. L., Martinez J. L. Jr., Jensen R. A., Vasquez B. J., and Messing R. B. (1982) Post-training amygdaloid lesions impair retention of an inhibitory avoidance response. Behav. Brain Res. 4, 237–249.PubMedCrossRefGoogle Scholar
  75. 75.
    Parent M. B., Quirarte G. L., Cahill L., and McGaugh J. L. (1995) Spared retention of inhibitory avoidance learning after posttraining amygdala lesions. Behav. Neurosci. 109, 803–807.PubMedCrossRefGoogle Scholar
  76. 76.
    Clugnet M. C. and LeDoux J. E. (1990) Synaptic plasticity in fear conditioning circuits: induction of LTP in the lateral nucleus of the amygdala by stimulation of the medial geniculate body. J. Neurosci. 10, 2818–2824.PubMedGoogle Scholar
  77. 77.
    Maren S. and Fanselow M. S. (1995) Synaptic plasticity in the basolateral amygdala induced by hippocampal stimulation in vivo. J. Neurosci. 15, 7584–7564.Google Scholar
  78. 78.
    Yaniv D. and Richter-Levin G. (2000) LTP in the rat basal amygdala induced by perirhinal cortex stimulation in vivo. Neuroreport 28, 525–530.CrossRefGoogle Scholar
  79. 79.
    Rogan M. T. and LeDoux J. E. (1996) Emotion: systems, cells, synaptic plasticity. Cell 17, 469–75.Google Scholar
  80. 80.
    McKernan M. G. and Shinnick-Gallagher P. (1997) Fear conditioning induces a lasting potentiation of synaptic currents in vitro. Nature 390, 607–611.PubMedCrossRefGoogle Scholar
  81. 81.
    Rogan M. T., Staubli U. V., and LeDoux J. E. (1997) Fear conditioning induces associative long-term potentiation in the amygdala. Nature 1, 604–607.CrossRefGoogle Scholar
  82. 82.
    Akirav I., Sandi C., and Richter-Levin G. (2001). Hippocampus and amygdala involvement in spatial learning as a function of stress. Submitted.Google Scholar
  83. 83.
    Canteras N. S. and Swanson L. W. (1992) Projections of the ventral subiculum to the amygdala, septum, and hypothalamus: a PHAL anterograde tract-tracing study in the rat. J. Comp. Neurol. 8, 180–194.CrossRefGoogle Scholar
  84. 84.
    Ottersen O. P. (1982) Connections of the amygdala of the rat. IV: Corticoamygdaloid and intraamygdaloid connections as studied with axonal transport of horseradish peroxidase. J. Comp. Neurol. 10, 30–48.CrossRefGoogle Scholar
  85. 85.
    Swanson L. W. and Kohler C. (1986) Anatomical evidence for direct projections from the entorhinal area to the entire cortical mantle in the rat. J. Neurosci. 6, 3010–3023.PubMedGoogle Scholar
  86. 86.
    Wyss J. M. (1981) An autoradiographic study of the efferent connections of the entorhinal cortex in the rat. J. Comp. Neurol. 199, 495–512.PubMedCrossRefGoogle Scholar
  87. 87.
    Mello L. E., Tan A. M., and Finch D. M. (1992a) GABAergic synaptic transmission in projections from the basal forebrain and hippocampal formation to the amygdala: an in vivo iontophoretic study. Brain Res. 31, 41–48.CrossRefGoogle Scholar
  88. 88.
    Mello L. E., Tan A. M., and Finch D. M. (1992b) Convergence of projections from the rat hippocampal formation, medial geniculate and basal forebrain onto single amygdaloid neurons: an in vivo extra- and intracellular electrophysiological study. Brain Res. 31, 24–40.CrossRefGoogle Scholar
  89. 89.
    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.PubMedCrossRefGoogle Scholar
  90. 90.
    Morgan M. A. and LeDoux J. E. (1995) Differential contribution of dorsal and ventral medial prefrontal cortex to the acquisition and extinction of conditioned fear in rats. Behav. Neurosci. 109, 681–688.PubMedCrossRefGoogle Scholar
  91. 91.
    Morgan M. A. and LeDoux J. E. (1999) Contribution of ventrolateral prefrontal cortex to the acquisition and extinction of conditioned fear in rats. Neurobiol. Learn. Mem. 72, 244–251.PubMedCrossRefGoogle Scholar
  92. 92.
    Doyere V., Burette F., Negro C. R., and Laroche S. (1993) Long-term potentiation of hippocampal afferents and efferents to prefrontal cortex: implications for associative learning. Neuropsychologia 31, 1031–1053.PubMedCrossRefGoogle Scholar
  93. 93.
    Jay T. M., Burette F., and Laroche S. (1995) NMDA receptor-dependent long-term potentiation in the hippocampal afferent fiber system to the prefrontal cortex in the rat. Eur. J. Neurosci. 1, 247–250.CrossRefGoogle Scholar
  94. 94.
    Jay T. M., Burette F., and Laroche S. (1996) Plasticity of the hippocampal-prefrontal cortex synapses. J. Physiol. Paris 90, 361–366.CrossRefGoogle Scholar
  95. 95.
    Laroche S., Jay T. M., and Thierry A. M. (1990) Long-term potentiation in the prefrontal cortex following stimulation of the hippocampal CA1/subicular region. Neurosci. Lett. 3, 184–190.CrossRefGoogle Scholar

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© Humana Press Inc 2001

Authors and Affiliations

  1. 1.Department of Psychology, Laboratory of Behavioral NeuroscienceHaifa UniversityHaifaIsrael

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