Molecular Neurobiology

, Volume 30, Issue 2, pp 127–141 | Cite as

The physiological role of kainate receptors in the amygdala

  • Maria F. M. Braga
  • Vassiliki Aroniadou-Anderjaska
  • He Li


The kainate subtype of glutamate receptors has received considerable attention in recent years, and a wealth of knowledge has been obtained regarding the function of these receptors. Kainate receptors have been shown to mediate synaptic transmission in some brain regions, modulate presynaptic release of glutamate and γ-aminobutyric acid (GABA), and mediate synaptic plasticity or the development of seizure activity. This article focuses on the function of kainate receptors in the amygdala, a brain region that plays a central role in emotional behavior and certain psychiatric illnesses. Evidence is reviewed indicating that postsynaptic kainate receptors containing the glutamate receptor 5 kainate receptor (GLUk5) subunit are present on interneurons and pyramidal cells in the basolateral amygdala and mediate a component of the synaptic responses of these neurons to glutamatergic input. In addition, GLUk5-containing kainate receptors are present on presynaptic terminals of GABAergic neurons, where they modulate the release of GABA in an agonist concentration-dependent, bidirectional manner. GLUk5-containing kainate receptors also mediate a longlasting synaptic facilitation induced by low-frequency stimulation in the external capsule to the basolateral nucleus pathway, and they appear to be party responsible for the susceptibility of the amygdala to epileptogenesis. Taken together, these findings have suggested a prominent role of GLUk5-containing kainate receptors in the regulation of neuronal excitability in the amygdala.

Index Entries

Kainate receptors GLUk5 amygdala excitatory synaptic transmission inhibitory synaptic transmission synaptic plasticity long-term potentiation epilepsy emotional memory mood disorders 


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  1. 1.
    Huettner J. E. (2003). Kainate receptors and synaptic transmission. Prog. Neurobiol. 70, 387–407.PubMedCrossRefGoogle Scholar
  2. 2.
    Lerma J. (2003). Roles and rules of kainate receptors in synaptic transmission. Nat. Rev. Neurosci. 4, 481–495.PubMedCrossRefGoogle Scholar
  3. 3.
    Bettler B., Boulter J., Hermans-Borgmeyer I., et al. (1990). Cloning of a novel glutamate receptor subunit, GluR5: expression in the nervous system during development. Neuron 5, 583–595.PubMedCrossRefGoogle Scholar
  4. 4.
    Sommer B., Burnashev N., Verdoorn T. A., Keinanen K., Sakmann B., Seeburg P. H. (1992). A glutamate receptor channel with high affinity for domoate and kainate. EMBO J. 11, 1651–1656.PubMedGoogle Scholar
  5. 5.
    Egebjerg J., Heinemann S. F. (1993). Ca2+ permeability of unedited and edited versions of the kainate selective glutamate receptor GluR6. Proc. Natl. Acad. Sci. USA 90, 755–759.PubMedCrossRefGoogle Scholar
  6. 6.
    Schiffer H. H., Swanson G. T., Heinemann S. F. (1997). Rat GluR7 and a carboxy-terminal splice variant, GluR7b, are functional kainate receptor subunits with a low sensitivity to glutamate. Neuron 19, 1141–1146.PubMedCrossRefGoogle Scholar
  7. 7.
    Cui C., Mayer M. L. (1999). Heteromeric kainate receptors formed by the coassembly of GluR5, GluR6, and GluR7. J. Neurosci. 19, 8281–8291.PubMedGoogle Scholar
  8. 8.
    Paternain A. V., Herrera M. T., Nieto M. A., Lerma J. (2000). GluR5 and GluR6 kainate receptor subunits coexist in hippocampal neurons and coassemble to form functional receptors. J. Neurosci. 20, 196–205.PubMedGoogle Scholar
  9. 9.
    Herb A., Burnashev N., Werner P., Sakmann B., Wisden W., Seeburg P. H. (1992). The KA-2 subunit of excitatory amino acid receptors shows widespread expression in brain and forms ion channels with distantly related subunits. Neuron 8, 775–785.PubMedCrossRefGoogle Scholar
  10. 10.
    Sakimura K., Morita T., Kushiya E., Mishina M. (1992). Primary structure and expression of the gamma 2 subunit of the glutamate receptor channel selective for kainate. Neuron 8, 267–274.PubMedCrossRefGoogle Scholar
  11. 11.
    Hollmann M., Heinemann S. (1994). Cloned glutamate receptors. Annu. Rev. Neurosci. 17, 31–108.PubMedCrossRefGoogle Scholar
  12. 12.
    Gregor P., O’Hara B. F., Yang X., Uhl G. R. (1993). Expression and novel subunit isoforms of glutamate receptor genes GluR5 and GluR6. Neuroreport 4, 1343–1346.PubMedCrossRefGoogle Scholar
  13. 13.
    Herb A., Higuchi M., Sprengel R., Seeburg P. H. (1996). Q/R site editing in kainate receptor GluR5 and GluR6 pre-mRNAs requires distant intronic sequences. Proc. Natl. Acad. Sci. USA 93, 1875–1880.PubMedCrossRefGoogle Scholar
  14. 14.
    Sommer B., Kohler M., Sprengel R., Seeburg P. H. (1991). RNA editing in brain controls a determinant of ion flow in glutamate-gated channels. Cell 67, 11–19.PubMedCrossRefGoogle Scholar
  15. 15.
    Burnashev N., Zhou Z., Neher E., Sakmann B. (1995). Fractional calcium currents through recombinant GluR channels of the NMDA, AMPA and kainate receptor subtypes. J. Physiol. 485(pt 2), 403–418.PubMedGoogle Scholar
  16. 16.
    Bowie D., Mayer M. L. (1995). Inward rectification of both AMPA and kainate subtype glutamate receptors generated by polyamine-mediated ion channel block. Neuron 15, 453–462.PubMedCrossRefGoogle Scholar
  17. 17.
    Kamboj S. K., Swanson G. T., Cull-Candy S. G. (1995). Intracellular spermine confers rectification on rat calcium-permeable AMPA and kainate receptors. J. Physiol. 486(pt 2), 297–303.PubMedGoogle Scholar
  18. 18.
    Donevan S. D., Rogawski M. A. (1995). Intracellular polyamines mediate inward rectification of Ca(2+)-permeable alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid receptors. Proc. Natl. Acad. Sci. USA 92, 9298–9302.PubMedCrossRefGoogle Scholar
  19. 19.
    Koh D. S., Burnashev N., Jonas P. (1995). Block of native Ca(2+)-permeable AMPA receptors in rat brain by intracellular polyamines generates double rectification. J. Physiol. 486(pt 2), 305–312.PubMedGoogle Scholar
  20. 20.
    Bahring R., Bowie D., Benveniste M., Mayer M. L. (1997). Permeation and block of rat GluR6 glutamate receptor channels by internal and external polyamines. J. Physiol. 502(pt 3), 575–589.PubMedCrossRefGoogle Scholar
  21. 21.
    Kohler M., Burnashev N., Sakmann B., Seeburg P. H. (1993). Determinants of Ca2+ permeability in both TM1 and TM2 of high affinity kainate receptor channels: diversity by RNA editing. Neuron 10, 491–500.PubMedCrossRefGoogle Scholar
  22. 22.
    Castillo P. E., Malenka R. C., Nicoll R. A. (1997). Kainate receptors mediate a slow post-synaptic current in hippocampal CA3 neurons. Nature 388, 182–186.PubMedCrossRefGoogle Scholar
  23. 23.
    Vignes M., Bleakman D., Lodge D., Collingridge G. L. (1997). The synaptic activation of the GluR5 subtype of kainate receptor in area CA3 of the rat hippocampus. Neuropharmacology 36, 1477–1481.PubMedCrossRefGoogle Scholar
  24. 24.
    Cossart R., Esclapez M., Hirsch J. C., Bernard C., Ben Ari Y. (1998). GluR5 kainate receptor activation in interneurons increases tonic inhibition of pyramidal cells. Nat. Neurosci. 1, 470–478.PubMedCrossRefGoogle Scholar
  25. 25.
    Li H., Rogawski M. A. (1998). GluR5 kainate receptor mediated synaptic transmission in rat basolateral amygdala in vitro. Neuropharmacology 37, 1279–1286.PubMedCrossRefGoogle Scholar
  26. 26.
    Kidd F. L., Isaac J. T. (1999). Developmental and activity-dependent regulation of kainate receptors at thalamocortical synapses. Nature 400, 569–573.PubMedCrossRefGoogle Scholar
  27. 27.
    Frerking M., Nicoll R. A. (2000). Synaptic kainate receptors. Curr. Opin. Neurobiol. 10, 342–351.PubMedCrossRefGoogle Scholar
  28. 28.
    Kullmann D. M. (2001). Presynaptic kainate receptors in the hippocampus: slowly emerging from obscurity. Neuron 32, 561–564.PubMedCrossRefGoogle Scholar
  29. 29.
    Kullmann D. M. (2001). Presynaptic kainate receptors in the hippocampus. Slowly emerging from obscurity. Neuron 32, 561–564.PubMedCrossRefGoogle Scholar
  30. 30.
    Wisden W., Seeburg P. H. (1993). A complex mosaic of high-affinity kainate receptors in rat brain. J. Neurosci. 13, 3582–3598.PubMedGoogle Scholar
  31. 31.
    LeDoux J. E. (1992). Brain mechanisms of emotion and emotional learning. Curr. Opin. Neurobiol. 2, 191–197.PubMedCrossRefGoogle Scholar
  32. 32.
    Davis M. (1994). The role of the amygdala in emotional learning. Int. Rev. Neurobiol. 36, 225–266.PubMedCrossRefGoogle Scholar
  33. 33.
    Schneider F., Grodd W., Weiss U., et al. (1997). Functional MRI reveals left amygdala activation during emotion. Psychiatry Res. 76, 75–82.PubMedCrossRefGoogle Scholar
  34. 34.
    Davidson R. J., Abercrombie H., Nitschke J. B., Putnam K. (1999). Regional brain function, emotion and disorders of emotion. Curr. Opin. Neurobiol. 9, 228–234.PubMedCrossRefGoogle Scholar
  35. 35.
    Goldstein L. E., Rasmusson A. M., Bunney B. S., Roth R. H. (1996). Role of the amygdala in the coordination of behavioral, neuroendocrine, and prefrontal cortical monoamine responses to psychological stress in the rat. J. Neurosci. 16, 4787–4798.PubMedGoogle Scholar
  36. 36.
    Habib K. E., Gold P. W., Chrousos G. P. (2001). Neuroendocrinology of stress. Endocrinol. Metab. Clin. N. Am. 30, 695–728.CrossRefGoogle Scholar
  37. 37.
    Davis M. (1992). The role of the amygdala in fear and anxiety. Annu. Rev. Neurosci. 15, 353–375.PubMedCrossRefGoogle Scholar
  38. 38.
    Abercrombie H. C., Schaefer S. M., Larson C. L., et al. (1998). Metabolic rate in the right amygdala predicts negative affect in depressed patients. Neuroreport 9, 3301–3307.PubMedCrossRefGoogle Scholar
  39. 39.
    Drevets W. C. (1999). Prefrontal cortical-amygdalar metabolism in major depression. Ann. NY Acad. Sci. 877, 614–637.PubMedCrossRefGoogle Scholar
  40. 40.
    Davidson R. J., Slagter H. A. (2000). Probing emotion in the developing brain, functional neuroimaging in the assessment of the neural substrates of emotion in normal and disordered children and adolescents. Ment. Retard. Dev. Disabil. Res. Rev. 6, 166–170.PubMedCrossRefGoogle Scholar
  41. 41.
    Rauch S. L., Whalen P. J., Shin L. M., et al. (2000). Exaggerated amygdala response to masked facial stimuli in posttraumatic stress disorder, a functional MRI study. Biol. Psychiatry 47, 769–776.PubMedCrossRefGoogle Scholar
  42. 42.
    Rauch S. L., Shin L. M., Wright C. I. (2003). Neuroimaging studies of amygdala function in anxiety disorders. Ann. NY Acad. Sci. 985, 389–410.PubMedGoogle Scholar
  43. 43.
    Rogawski M. A., Gryder D., Castaneda D., Yonekawa W., Banks M. K., Li H. (2003). GluR5 kainate receptors, seizures, and the amygdala. Ann. NY Acad. Sci. 985, 150–162.PubMedGoogle Scholar
  44. 44.
    McDonald A. J. (2003). Is there an amygdala and how far does it extend? An anatomical perspective. Ann. NY Acad. Sci. 985, 1–21.PubMedGoogle Scholar
  45. 45.
    Sah P., Faber E. S., Lopez D. A., Power J. (2003). The amygdaloid complex, anatomy and physiology. Physiol. Rev. 83, 803–834.PubMedGoogle Scholar
  46. 46.
    Rainnie D. G., Asprodini E. K., Shinnick-Gallagher P. (1992). Kindling-induced long-lasting changes in synaptic transmission in the basolateral amygdala. J. Neurophysiol. 67, 443–454.PubMedGoogle Scholar
  47. 47.
    Gean P. W., Chang F. C. (1992). Pharmacological characterization of excitatory synaptic potentials in rat basolateral amygdaloid neurons. Synapse 11, 1–9.PubMedCrossRefGoogle Scholar
  48. 48.
    Farb C. R., Aoki C., LeDoux J. E. (1995). Differential localization of NMDA and AMPA receptor subunits in the lateral and basal nuclei of the amygdala, a light and electron microscopic study. J. Comp. Neurol. 362, 86–108.PubMedCrossRefGoogle Scholar
  49. 49.
    Li X. F., Phillips R., LeDoux J. E. (1995). NMDA and non-NMDA receptors contribute to synaptic transmission between the medial geniculate body and the lateral nucleus of the amygdala. Exp. Brain Res. 105, 87–100.PubMedCrossRefGoogle Scholar
  50. 50.
    Neugebauer V., Keele N. B., Shinnick-Gallagher P. (1997). Epileptogenesis in vivo enhances the sensitivity of inhibitory presynaptic metabotropic glutamate receptors in basolateral amygdala neurons in vitro. J. Neurosci. 17, 983–995.PubMedGoogle Scholar
  51. 51.
    Li H., Weiss S. R., Chuang D. M., Post R. M., Rogawski M. A. (1998). Bidirectional synaptic plasticity in the rat basolateral amygdala: characterization of an activity-dependent switch sensitive to the presynaptic metabotropic glutamate receptor antagonist 2S-alpha-ethylglutamic acid. J. Neurosci. 18, 1662–1670.PubMedGoogle Scholar
  52. 52.
    Li H., Chen A., Xing G., Wei M. L., Rogawski M. A. (2001). Kainate receptor-mediated heterosynaptic facilitation in the amygdala. Nat. Neurosci. 4, 612–620.PubMedCrossRefGoogle Scholar
  53. 53.
    Braga M. F., Aroniadou-Anderjaska V., Xie J., Li H. (2003). Bidirectional modulation of GABA release by presynaptic glutamate receptor 5 kainate receptors in the basolateral amygdala. J. Neurosci. 23, 442–452.PubMedGoogle Scholar
  54. 54.
    Vignes M., Collingridge G. L. (1997). The synaptic activation of kainate receptors. Nature 388, 179–182.PubMedCrossRefGoogle Scholar
  55. 55.
    Wilding T. J., Huettner J. E. (1995). Differential antagonism of alpha-amino-3-hydroxy-5-methyl-4- isoxazolepropionic acid-preferring and kainate-preferring receptors by 2,3-benzodiazepines. Mol. Pharmacol. 47, 582–587.PubMedGoogle Scholar
  56. 56.
    Paternain A. V., Morales M., Lerma J. (1995). Selective antagonism of AMPA receptors unmasks kainate receptor-mediated responses in hippocampal neurons. Neuron 14, 185–189.PubMedCrossRefGoogle Scholar
  57. 57.
    Bleakman R., Schoepp D. D., Ballyk B., et al. (1996). Pharmacological discrimination of GluR5 and GluR6 kainate receptor subtypes by (3S,4a R, 6R, 8a R)-6-[2-(1 (2) H-tetrazole-5-yl)ethyl]decahyd roisdoquinoline-3 carboxylicacid. Mol. Pharmacol. 49, 581–585.PubMedGoogle Scholar
  58. 58.
    Bureau I., Dieudonne S., Coussen F., Mulle C. (2000). Kainate receptor-mediated synaptic currents in cerebellar Golgi cells are not shaped by diffusion of glutamate. Proc. Natl. Acad. Sci. USA 97, 6838–6843.PubMedCrossRefGoogle Scholar
  59. 59.
    Li P., Wilding T. J., Kim S. J., Calejesan A. A., Huettner J. E., Zhuo M. (1999). Kainate-receptor-mediated sensory synaptic transmission in mammalian spinal cord. Nature 397, 161–164.PubMedCrossRefGoogle Scholar
  60. 60.
    Gryder D. S., Rogawski M. A. (2003). Selective antagonism of GluR5 kainate-receptor-mediated synaptic currents by topiramate in rat basolateral amygdala neurons. J. Neurosci. 23, 7069–7074.PubMedGoogle Scholar
  61. 61.
    Liu Q. S., Patrylo P. R., Gao X. B., van den Pol A. N. (1999). Kainate acts at presynaptic receptors to increase GABA release from hypothalamic neurons. J. Neurophysiol. 82, 1059–1062.PubMedGoogle Scholar
  62. 62.
    Cossart R., Tyzio R., Dinocourt C., et al. (2001). Presynaptic kainate receptors that enhance the release of GABA on CA1 hippocampal interneurons. Neuron 29, 497–508.PubMedCrossRefGoogle Scholar
  63. 63.
    Contractor A., Swanson G., Heinemann S. F. (2001). Kainate receptors are involved in short-and long-term plasticity at mossy fiber synapses in the hippocampus. Neuron 29, 209–216.PubMedCrossRefGoogle Scholar
  64. 64.
    Schmitz D., Mellor J., Frerking M., Nicoll R. A. (2001). Presynaptic kainate receptors at hippocampal mossy fiber synapses. Proc. Natl. Acad. Sci. USA 98, 11,003–11,008.CrossRefGoogle Scholar
  65. 65.
    Chittajallu R., Braithwaite S. P., Clarke V. R., Henley J. M. (1999). Kainate receptors, subunits, synaptic localization and function. Trends Pharmacol. Sci. 20, 26–35.PubMedCrossRefGoogle Scholar
  66. 66.
    Mulle C., Sailer A., Swanson G. T., et al. (2000). Subunit composition of kainate receptors in hippocampal interneurons. Neuron 28, 475–484.PubMedCrossRefGoogle Scholar
  67. 67.
    Semyanov A., Kullmann D. M. (2001). Kainate receptor-dependent axonal depolarization and action potential initiation in interneurons. Nat. Neurosci. 4, 718–723.PubMedCrossRefGoogle Scholar
  68. 68.
    Cunha R. A., Malva J. O., Ribeiro J. A. (2000). Pertussis toxin prevents presynaptic inhibition by kainate receptors of rat hippocampal [(3)H]GABA release. FEBS Lett. 469, 159–162.PubMedCrossRefGoogle Scholar
  69. 69.
    Rodriguez-Moreno A., Lerma J. (1998). Kainate receptor modulation of GABA release involves a metabotropic function. Neuron 20, 1211–1218.PubMedCrossRefGoogle Scholar
  70. 70.
    Fanselow M. S., Gale G. D. (2003). The amygdala, fear, and memory. Ann. NY Acad. Sci. 985, 125–134.PubMedGoogle Scholar
  71. 71.
    Teyler T. J., DiScenna P. (1987). Long-term potentiation. Annu. Rev. Neurosci. 10, 131–161.PubMedCrossRefGoogle Scholar
  72. 72.
    Gustafsson B., Wigstrom H. (1988). Physiological mechanisms underlying long-term potentiation. Trends Neurosci. 11, 156–162.PubMedCrossRefGoogle Scholar
  73. 73.
    Nicoll R. A., Kauer J. A., Malenka R. C. (1988). The current excitement in long-term potentiation. Neuron 1, 97–103.PubMedCrossRefGoogle Scholar
  74. 74.
    Madison D. V., Malenka R. C., Nicoll R. A. (1991). Mechanisms underlying long-term potentiation of synaptic transmission. Annu. Rev. Neurosci. 14, 379–397.PubMedCrossRefGoogle Scholar
  75. 75.
    Bliss T. V., Collingridge G. L. (1993). A synaptic model of memory, long-term potentiation in the hippocampus. Nature 361, 31–39.PubMedCrossRefGoogle Scholar
  76. 76.
    Nicoll R. A., Malenka R. C. (1995). Contrasting properties of two forms of long-term potentiation in the hippocampus. Nature 377, 115–118.PubMedCrossRefGoogle Scholar
  77. 77.
    Lynch G., Larson J., Kelso S., Barrionuevo G., Schottler F. (1983). Intracellular injections of EGTA block induction of hippocampal long-term potentiation. Nature 305, 719–721.PubMedCrossRefGoogle Scholar
  78. 78.
    Mulkey R. M., Malenka R. C. (1992). Mechanisms underlying induction of homosynaptic long-term depression in area CA1 of the hippocampus. Neuron 9, 967–975.PubMedCrossRefGoogle Scholar
  79. 79.
    Teyler T. J., Cavus I., Coussens C., et al. (1994). Multideterminant role of calcium in hippocampal synaptic plasticity. Hippocampus 4, 623–634.PubMedCrossRefGoogle Scholar
  80. 80.
    Chittajallu R., Alford S., Collingridge G. L. (1998). Ca2+ and synaptic plasticity. Cell Calcium 24, 377–385.PubMedCrossRefGoogle Scholar
  81. 81.
    Kemp N., Bashir Z. I. (2001). Long-term depression, a cascade of induction and expression mechanisms. Prog. Neurobiol. 65, 339–365.PubMedCrossRefGoogle Scholar
  82. 82.
    Collingridge G. L., Kehl S. J., McLennan H. (1983). Excitatory amino acids in synaptic transmission in the Schaffer collateral-commissural pathway of the rat hippocampus. J. Physiol 334, 33–46.PubMedGoogle Scholar
  83. 83.
    Muller D., Joly M., Lynch G. (1988). Contributions of quisqualate and NMDA receptors to the induction and expression of LTP. Science 242, 1694–1697.PubMedCrossRefGoogle Scholar
  84. 84.
    Malenka R. C., Nicoll R. A. (1993). NMDA-receptor-dependent synaptic plasticity, multiple forms and mechanisms. Trends Neurosci. 16, 521–527.PubMedCrossRefGoogle Scholar
  85. 85.
    Kullmann D. M., Siegelbaum S. A. (1995). The site of expression of NMDA receptor-dependent LTP: new fuel for an old fire. Neuron 15, 997–1002.PubMedCrossRefGoogle Scholar
  86. 86.
    Malenka R. C., Nicoll R. A. (1999). Long-term potentiation—a decade of progress? Science 285, 1870–1874.PubMedCrossRefGoogle Scholar
  87. 87.
    Kemp N., McQueen J., Faulkes S., Bashir Z. I. (2000). Different forms of LTD in the CA1 region of the hippocampus, role of age and stimulus protocol. Eur. J. Neurosci. 12, 360–366.PubMedCrossRefGoogle Scholar
  88. 88.
    Grover L. M., Teyler T. J. (1990). Two components of long-term potentiation induced by different patterns of afferent activation. Nature 347, 477–479.PubMedCrossRefGoogle Scholar
  89. 89.
    Morgan S. L., Teyler T. J. (1999). VDCCs and NMDARs underlie two forms of LTP in CA1 hippocampus in vivo. J. Neurophysiol. 82, 736–740.PubMedGoogle Scholar
  90. 90.
    Aroniadou V. A., Teyler T. J. (1992). Induction of NMDA receptor-independent long-term potentiation (LTP) in visual cortex of adult rats. Brain Res. 584, 169–173.PubMedCrossRefGoogle Scholar
  91. 91.
    Aroniadou V. A., Maillis A., Stefanis C. C. (1993). Dihydropyridine-sensitive calcium channels are involved in the induction of N-methyl-d-aspartate receptor-independent long-term potentiation in visual cortex of adult rats. Neurosci. Lett. 151, 77–80.PubMedCrossRefGoogle Scholar
  92. 92.
    Bortolotto Z. A., Clarke V. R., Delany C. M., et al. (1999). Kainate receptors are involved in synaptic plasticity. Nature 402, 297–301.PubMedCrossRefGoogle Scholar
  93. 93.
    Aroniadou-Anderjaska V., Post R. M., Rogawski M. A., Li H. (2001). Input-specific LTP and depotentiation in the basolateral amygdala. Neuroreport 12, 635–640.PubMedCrossRefGoogle Scholar
  94. 94.
    Rammes G., Steckler T., Kresse A., Schutz G., Zieglgansberger W., Lutz B. (2000). Synaptic plasticity in the basolateral amygdala in transgenic mice expressing dominant-negative cAMP response element-binding protein (CREB) in forebrain. Eur. J. Neurosci. 12, 2534–2546.PubMedCrossRefGoogle Scholar
  95. 95.
    Rogan M. T., Staubli U. V., LeDoux J. E. (1997). Fear conditioning induces associative long-term potentiation in the amygdala. Nature 390, 604–607.PubMedCrossRefGoogle Scholar
  96. 96.
    Maren S. (1999). Long-term potentiation in the amygdala, a mechanism for emotional learning and memory. Trends Neurosci. 22, 561–567.PubMedCrossRefGoogle Scholar
  97. 97.
    Huang Y. Y., Kandel E. R. (1998). Postsynaptic induction and PKA-dependent expression of LTP in the lateral amygdala. Neuron 21, 169–178.PubMedCrossRefGoogle Scholar
  98. 98.
    Weisskopf M. G., Bauer E. P., LeDoux J. E. (1999). l-type voltage-gated calcium channels mediate NMDA-independent associative long-term potentiation at thalamic input synapses to the amygdala. J. Neurosci. 19, 10,512–10,519.Google Scholar
  99. 99.
    Mahanty N. K., Sah P. (1998). Calcium-permeable AMPA receptors mediate long-term potentiation in interneurons in the amygdala. Nature 394, 683–687.PubMedCrossRefGoogle Scholar
  100. 100.
    Wang S. J., Gean P. W. (1999). Long-term depression of excitatory synaptic transmission in the rat amygdala. J. Neurosci. 19, 10,656–10,663.Google Scholar
  101. 101.
    Jones K. A., Wilding T. J., Huettner J. E., Costa A. M. (1997). Desensitization of kainate receptors by kainate, glutamate and diastereomers of 4-methylglutamate. Neuropharmacology 36, 853–863.PubMedCrossRefGoogle Scholar
  102. 102.
    Chapman P. F. (2001). The diversity of synaptic plasticity. Nat. Neurosci. 4, 556–558.PubMedCrossRefGoogle Scholar
  103. 103.
    Aggleton J. P. (2000). The Amygdala, A Functional Analysis, 2nd ed. Oxford University Press, Oxford.Google Scholar
  104. 104.
    Braga M. F. M., Li H., Rogawski M. A. (2003). Topiramate enhances GABAergic transmission and blocks GluR5 kainate receptors in basolateral amygdala interneurons. Soc. Neurosci. Abs. 33, 582.15.Google Scholar
  105. 105.
    Vieta E., Sanchez-Moreno J., Goikolea J. M., et al. (2003). Adjunctive topiramate in bipolar II disorder. World J. Biol. Psychiatry 4(4), 172–176.PubMedCrossRefGoogle Scholar
  106. 106.
    Sachs G. S. (2003). Decision tree for the treatment of bipolar disorder. J. Clin. Psychiatry 64(Suppl 8), 35–40.PubMedGoogle Scholar
  107. 107.
    Deutsch S. I., Schwartz B. L., Rosse R. B., Mastropaolo J., Marvel C. L., Drapalski A. L. (2003). Adjuvant topiramate administration, a pharmacologic strategy for addressing NMDA receptor hypofunction in schizophrenia. Clin. Neuropharmacol. 26(4), 199–206.PubMedCrossRefGoogle Scholar

Copyright information

© Humana Press Inc 2004

Authors and Affiliations

  • Maria F. M. Braga
    • 1
  • Vassiliki Aroniadou-Anderjaska
    • 1
  • He Li
    • 1
  1. 1.Department of PsychiatryUniformed Services University of the Health SciencesBethesda

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