Skip to main content

Synaptic transmission and plasticity in the amygdala

An emerging physiology of fear conditioning circuits

Molecular Neurobiology volume 13, pages 1–22 (1996)Cite this article

Abstract

Numerous studies in both rats and humans indicate the importance of the amygdala in the acquisition and expression of learned fear. The identification of the amygdala as an essential neural substrate for fear conditioning has permitted neurophysiological examinations of synaptic processes in the amygdala that may mediate fear conditioning. One candidate cellular mechanism for fear conditioning is long-term potentiation (LTP), an enduring increase in synaptic transmission induced by high-frequency stimulation of excitatory afferents. At present, the mechanisms underlying the induction and expression of amygdaloid LTP are only beginning to be understood, and probably involve both theN-methyl-d-aspartate (NMDA) and α-amino-3-hydroxy-5-methyl-4-isoxazolepropionate (AMPA) subclasses of glutamate receptors. This article will examine recent studies of synaptic transmission and plasticity in the amygdala in an effort to understand the relationships of these processes to aversive learning and memory.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

43,34 €

Price includes VAT (Finland)
Tax calculation will be finalised during checkout.

References

  • Abe K., Nakata A., Mizutani A., and Saito H. (1994) Facilitatory but nonessential role of the muscarinic cholinergic system in the generation of long-term potentiation of population spikes in the dentate gyrus in vivo.Neuropharmacology 33, 847–852.

    PubMed  CAS  Google Scholar 

  • Applegate C. D., Frysinger R. C., Kapp B. S., and Gallagher M. (1982) Multiple unit activity recorded from amygdala central nucleus during Pavlovian heart rate conditioning in rabbit.Brain Res. 238, 457–462.

    PubMed  CAS  Google Scholar 

  • Asprodini E. K., Rainnie D. G., and Shinnick-Gallagher P. (1992) Epileptogenesis reduces the sensitivity of presynaptic GABAB receptors on glutamatergic afferents in the amygdala.J. Pharmacol. Exp. Ther. 262, 1011–1021.

    PubMed  CAS  Google Scholar 

  • Barrionuevo G. and Brown T. H. (1983) Associative long-term potentiation in hippocampal slices.Proc. Natl. Acad. Sci. USA 80, 7347–7351.

    PubMed  CAS  Google Scholar 

  • Bechara A., Tranel D., Damasio H., Adolphs R., Rockland C., and Damasio A. R. (1995) Double dissociation of conditioning and declarative knowledge relative to the amygdala and hippocampus in humans.Science 269, 1115–1118.

    PubMed  CAS  Google Scholar 

  • Bernard J.-F., Alden M., and Besson J.-M. (1993) The organization of the efferent projections from the pontine parabrachial area to the amygdaloid complex: aPhaseolus vulgaris leucoagglutinin (PHA-L) study in the rat.J. Comp. Neurol. 329, 201–229.

    PubMed  CAS  Google Scholar 

  • Bernard J. F. and Besson J. M. (1990) The spino (trigemino)pontoamygdaloid pathway: electrophysiological evidence for an involvement in pain processes.J. Neurophysiol. 63, 473–490.

    PubMed  CAS  Google Scholar 

  • Blanchard D. C. and Blanchard R. J. (1972) Innate and conditioned reactions to threat in rats with amygdaloid lesions.J. Comp. Physiol. Psychol. 81, 281–290.

    PubMed  CAS  Google Scholar 

  • Bliss T. V. and Collingridge G. L. (1993) A synaptic model of memory: long-term potentiation in the hippocampus.Nature (Lond.) 361, 31–39.

    CAS  Google Scholar 

  • Brady J. V., Schreiner L., Geller I., and Kling A. (1954) Subcortical mechanisms in emotional behavior: the effect of rhinencephalic injury upon the acquisition and retention of a conditioned avoidance response in cats.J. Comp. Physiol. Psychol. 47, 179–186.

    PubMed  CAS  Google Scholar 

  • Brodal A. (1947) The amygdaloid nucleus in the rat.J. Comp. Neurol. 87, 1–16.

    Google Scholar 

  • Brothers L. A. and Finch D. M. (1985) Physiological evidence for an excitatory pathway from entorhinal cortex to amygdala in the rat.Brain Res. 359, 10–20.

    PubMed  CAS  Google Scholar 

  • Brown T. H., Chapman P. F., Kairiss E. W., and Keenan C. L. (1988) Long-term synaptic potentiation.Science 242, 724–728.

    PubMed  CAS  Google Scholar 

  • Brown T. H., Kairiss E. W., and Keenan C. L. (1990) Hebbian synapses: biophysical mechanisms and algorithms.Ann. Rev. Neurosci. 13, 475–511.

    PubMed  CAS  Google Scholar 

  • Campeau S. and Davis M. (1995) Involvement of the central nucleus and basolateral complex of the amygdala in fear conditioning measured with fear-potentiated startle in rats trained concurrently with auditory and visual conditioned stimuli.J. Neurosci. 15, 2301–2311.

    PubMed  CAS  Google Scholar 

  • Campeau S., Miserendino M. J., and Davis M. (1992) Intra-amygdala infusion of theN-methyl-d-aspartate receptor antagonist AP5 blocks acquisition but not expression of fear-potentiated startle to an auditory conditioned stimulus.Behav. Neurosci. 106, 569–574.

    PubMed  CAS  Google Scholar 

  • 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. 324, 180–194.

    PubMed  CAS  Google Scholar 

  • Cassell M. D. and Gray T. S. (1989) Morphology of peptide-immunoreactive neurons in the rat central nucleus of the amygdala.J. Comp. Neurol. 281, 320–333.

    PubMed  CAS  Google Scholar 

  • Cassell M. D., Gray T. S., and Kiss J. Z. (1986) Neuronal architecture in the rat central nucleus of the amygdala: a cytological, hodological, and immunocytochemical study.J. Comp. Neurol. 246, 478–499.

    PubMed  CAS  Google Scholar 

  • Chapman P. F. and Bellavance L. L. (1992) Induction of long-term potentiation in the basolateral amygdala does not depend on NMDA receptor activation.Synapse 11, 310–318.

    PubMed  CAS  Google Scholar 

  • Chapman P. F., Kairiss E. W., Keenan C. L., and Brown T. H. (1990) Long-term synaptic potentiation in the amygdala.Synapse 6, 271–278.

    PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • Clugnet M. C., LeDoux J. E., and Morrison S. F. (1990) Unit responses evoked in the amygdala and striatum by electrical stimulation of the medial geniculate body.J. Neurosci. 10, 1055–1061.

    PubMed  CAS  Google Scholar 

  • Davis M. (1992) The role of the amygdala in fear and anxiety.Ann. Rev. Neurosci. 15, 353–375.

    PubMed  CAS  Google Scholar 

  • Davis M., Rainnie D., and Cassell M. (1994) Neurotransmission in the rat amygdala related to fear and anxiety.Trends Neurosci. 17, 208–214.

    PubMed  CAS  Google Scholar 

  • Diamond D. M. and Rose G. M. (1994) Does associative LTP underlie classical conditioning?Psychobiol. 22, 263–269.

    Google Scholar 

  • Fanselow M. S. (1993) Associations and memories: the role of NMDA receptors and long-term potentiation.Curr. Dir. Psychol. Sci.,2, 152–156.

    Google Scholar 

  • Fanselow M. S. and Kim J. J. (1994) Acquisition of contextual Pavlovian fear conditioning is blocked by application of an NMDA receptor antagonistd,l-2-amino-5-phosphonovaleric acid to the basolateral amygdala.Behav. Neurosci. 108, 210–212.

    PubMed  CAS  Google Scholar 

  • Farb C. R., Aoki C., and 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.

    PubMed  CAS  Google Scholar 

  • Fuster J. M. and Uyeda A. A. (1971) Reactivity of limbic neurons of the monkey to appetitive and aversive signals.Electroencephalo. Clin. Neurophysiol. 30, 281–293.

    CAS  Google Scholar 

  • Gallistel C. R. (1995) Is long-term potentiation a plausible basis for memory?, inBrain and Memory: Modulation and Mediation of Neuroplasticity (McGaugh J. L., Weinberger N. M., and Lynch G., eds.), Oxford University Press, New York, pp. 328–337.

    Google Scholar 

  • Gean P.-W. and Chang F.-C. (1992) Pharmacological characterization of excitatory synaptic potentials in rat basolateral amygdaloid neurons.Synapse 11, 1–9.

    PubMed  CAS  Google Scholar 

  • Gean P.-W., Huang C.-C., Lin J.-H., and Tsai J.-J. (1992) Sustained enhancement of NMDA receptor-mediated synaptic potential by isoproterenol in rat amygdalar slices.Brain Res. 594, 331–334.

    PubMed  CAS  Google Scholar 

  • Gean P. W., Chang, F. C., Huang C. C., Lin J. H., and Way L. J. (1993a) Long-term enhancement of EPSP and NMDA receptor-mediated synaptic transmission in the amygdala.Brain Res. Bull. 31, 7–11.

    PubMed  CAS  Google Scholar 

  • Gean P. W., Chang F. C., and Hung C. R. (1993b) Use-dependent modification of a slow NMDA receptor-mediated synaptic potential in rat amygdalar slices.J. Neurosci. 34, 635–641.

    CAS  Google Scholar 

  • Gean P. W. and Shinnick-Gallagher P. (1987) Picrotoxin induced epileptiform activity in amygdaloid neurons.Neurosci. Lett. 73, 149–154.

    PubMed  CAS  Google Scholar 

  • Groenewegen H. J. and Berendse H. W. (1994) The specificity of the “nonspecific” midline and intralaminar thalamic nuclei.Trends Neurosci. 17, 52–57.

    PubMed  CAS  Google Scholar 

  • Heth D. C. and Rescorla R. A. (1973) Simultaneous and backward fear conditioning in the rat.J. Comp. Physiol. Psychol. 82, 434–443.

    Google Scholar 

  • Hitchcock J. and Davis M. (1986) Lesions of the amygdala, but not of the cerebellum or red nucleus, block conditioned fear as measured with the potentiated startle paradigm.Behav. Neurosci. 100, 11–22.

    PubMed  CAS  Google Scholar 

  • Huang C.-C. and Gean P.-W. (1994) Paired-pulse depression of theN-methyl-d-aspartate receptor-mediated synaptic potentials in the amygdala.Br. J. Pharmacol. 113, 1029–1035.

    PubMed  CAS  Google Scholar 

  • Huang C.-C., Hsu K.-S., and Gean P.-W. (1996) Isoproterenol potentiates synaptic transmission primarily by enhancing presynaptic calcium influx via P- and/or Q-type calcium channels in the rat amygdala.J. Neurosci. 16, 1026–1033.

    PubMed  CAS  Google Scholar 

  • Huang C.-C., Tsai J.-J., and Gean P.-W. (1994) Actions of isoproterenol on amygdalar neuronsin vitro.Clin. J. Physiol. 37, 73–78.

    CAS  Google Scholar 

  • Iwata J., Chida K., and LeDoux J. E. (1987) Cardiovascular responses elicited by stimulation of the neurons in the central amygdaloid nucleus in the awake but not anesthetized rats resemble conditioned emotional responses.Brain Res. 418, 183–188.

    PubMed  CAS  Google Scholar 

  • Iwata J., LeDoux J. E., Meeley M. P., Arneric S., and Reis D. J. (1986) Intrinsic neurons in the amygdaloid field projected to by the medial geniculate body mediate emotional responses conditioned to acoustic stimuli.Brain Res. 383, 195–214.

    PubMed  CAS  Google Scholar 

  • Jerusalinsky D., Ferreira M. B., Walz R., Da Silva R. C., Bianchin M., Ruschel A. C., Zanatta M. S., Medina J. H., and Izquierdo I. (1992) Amnesia by post-training infusion of glutamate receptor antagonists into the amygdala, hippocampus, and entorhinal cortex.Behav. Neural Biol. 58, 76–80.

    PubMed  CAS  Google Scholar 

  • Kapp B. S., Gallagher M., Underwood M. D., McNall C. L., and Whitehorn D. (1982) Cardiovascular responses elicited by electrical stimulation of the amygdala central nucleus in the rabbit.Brain Res. 234, 251–262.

    PubMed  CAS  Google Scholar 

  • Kapp B. S., Whalen P. J., Supple W. F., and Pascoe J. P. (1992) Amygdaloid contributions to conditioned arousal and sensory information processing, inThe Amygdala: Neurobiological Aspects of Emotion, Memory, and Mental Dysfunction (Aggleton J. P., ed.), Wiley-Liss, New York, pp. 229–254.

    Google Scholar 

  • Kelley A. E., Domesick V. B., and Nauta J. H. (1982) The amygdalostriatal projection in the rat: an anatomical study by anterograde and retrograde tracing methods.Neuroscience 7, 615–630.

    PubMed  CAS  Google Scholar 

  • Kellicutt M. H. and Schwartzbaum J. S. (1963) Formation of a conditioned emotional response (CER) following lesions of the amygdaloid complex in rats.Psychol. Rep. 12, 351–358.

    Google Scholar 

  • Kelso S. R., Ganong A. H., and Brown T. H. (1986) Hebbian synapses in hippocampus.Proc. Natl. Acad. Sci. USA 83, 5326–5330.

    PubMed  CAS  Google Scholar 

  • Kim M., Campeau S., Falls W. A., and Davis M. (1993) Infusion of the non-NMDA receptor antagonist CNQX into the amygdala blocks the expression of fear-potentiated startle.Behav. Neural Biol. 59, 5–8.

    PubMed  CAS  Google Scholar 

  • Kim M. and McGaugh J. L. (1992) Effects of intraamygdala injections of NMDA receptor antagonists on acquisition and retention of inhibitory avoidance.Brain Res. 585, 35–48.

    PubMed  CAS  Google Scholar 

  • Krettek J. E. and Price J. L. (1974) A direct input from the amygdala to the thalamus and cerebral cortex.Brain Res. 67, 169–174.

    PubMed  CAS  Google Scholar 

  • Krettek J. E. and Price J. L. (1977) Projections from the amygdaloid complex to the cerebral cortex and thalamus in rat and cat.J. Comp. Neurol. 172, 687–722.

    PubMed  CAS  Google Scholar 

  • Krettek J. E. and Price J. L. (1978a) Amygdaloid projections to subcortical structures within the basal forebrain and brainstem in the rat and cat.J. Comp. Neurol. 178, 225–254.

    PubMed  CAS  Google Scholar 

  • Krettek J. E. and Price J. L. (1978b) A description of the amygdaloid complex in the rat and cat with observations on intra-amygdaloid axonal connections.J. Comp. Neurol. 178, 255–279.

    PubMed  CAS  Google Scholar 

  • Le Gal La Salle G. and Ben-Ari Y. (1981) Unit activity in the amygdaloid complex: a review, inThe Amygdaloid Complex (Ben-Ari Y., ed.), Elsevier/ North Holland, Amsterdam, pp. 227–237.

    Google Scholar 

  • LeDoux J. E. (1995) Emotion: clues from the brain.Ann. Rev. Psych. 46, 209–235.

    CAS  Google Scholar 

  • LeDoux J. E., Cicchetti P., Xagoraris A., and Romanski L. M. (1990a) The lateral amygdaloid nucleus: sensory interface of the amygdala in fear conditioning.J. Neurosci. 10, 1062–1069.

    PubMed  CAS  Google Scholar 

  • LeDoux, J. E., Farb C., and Ruggiero D. A. (1990b) Topographic organization of neurons in the acoustic thalamus that project to the amygdala.J. Neurosci. 10, 1043–1054.

    PubMed  CAS  Google Scholar 

  • LeDoux J. E. and Farb C. R. (1991) Neurons of the acoustic thalamus that project to the amygdala contain glutamate.Neurosci. Lett. 134, 145–149.

    PubMed  CAS  Google Scholar 

  • LeDoux J. E., Farb C. R., and Romanski L. M. (1991) Overlapping projections to the amygdala and striatum from auditory processing ares of the thalamus and cortex.Neurosci. Lett. 134, 139–144.

    PubMed  CAS  Google Scholar 

  • LeDoux J. E., Iwata J., Cicchetti P., and Reis D. J. (1988) Different projections of the central amygdaloid nucleus mediate autonomic and behavioral correlates of conditioned fear.J. Neurosci. 8, 2517–2529.

    PubMed  CAS  Google Scholar 

  • Li X. F., Phillips R., and 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.

    PubMed  CAS  Google Scholar 

  • Liang K. C., Hon W., and Davis M. (1994) Pre- and posttraining infusion ofN-methyl-d-aspartate receptor antagonists into the amygdala impair memory in an inhibitory avoidance task.Behav. Neurosci. 108, 241–253.

    PubMed  CAS  Google Scholar 

  • Liao D., Hessler N. A., and Malinow R. (1995) Activation of postsynaptically silent synapses during pairing-induced LTP in CA1 region of hippocampal sliceNature (Lond.) 375, 400–404.

    CAS  Google Scholar 

  • Maren S., Aharonov G., and Fanselow M. S. (1996) Retrograde abolition of conditional fear after excitotoxic lesions in the basolateral amygdala in rats: absence of a temporal gradient.Behav. Neurosci., in press.

  • Maren S., Aharonov G., Stote D. L., and Fanselow M. S. (1997) N-methyl-d-aspartate receptors in the basolateral amygdala are required for both acquisition and expression of conditional fear in rats.Behav. Neurosci., in press.

  • Maren S. and Baudry M. (1995) Properties and mechanisms of long-term synaptic plasticity in the mammalian brain: relationships to learning and memory.Neurobiol. Learn. Mem. 63, 1–18.

    PubMed  CAS  Google Scholar 

  • Maren S. and Fanselow M. S. (1995) Synaptic plasticity in the basolateral amygdala induced by hippocampal formation stimulationin vivo.J. Neurosci. 15, 7548–7564.

    PubMed  CAS  Google Scholar 

  • Maren S. and Fanselow M. S. (1996) The amygdala and fear conditioning: Has the nut been cracked?Neuron 16, 237–240.

    PubMed  CAS  Google Scholar 

  • Maren S., Poremba A., and Gabriel M. (1991) Basolateral amygdaloid multi-unit neuronal cor-relates of discriminative avoidance learning in rabbits.Brain Res. 549, 311–316.

    PubMed  CAS  Google Scholar 

  • Maren S., Tocco G., Standley S., Baudry M., and Thompson R. F. (1993) Postsynaptic factors in the expression of long-term potentiation (LTP): increased glutamate receptor binding following LTP inductionin vivo.Proc. Natl. Acad. Sci. USA 90, 9554–9658.

    Google Scholar 

  • McDonald A. J. (1984) Neuronal organization of the lateral and basolateral amygdaloid nuclei in the rat.J. Comp. Neurol. 222, 589–606.

    PubMed  CAS  Google Scholar 

  • McDonald A. J. (1985a) Immunohistochemical identification of GABA-containing neurons in the rat basolateral amygdala.Neurosci. Lett. 53, 203–207.

    PubMed  CAS  Google Scholar 

  • McDonald A. J. (1985b) Morphology of peptide-containing neurons in the rat basolateral amygdaloid nucleus.Brain Res. 338, 186–191.

    PubMed  CAS  Google Scholar 

  • McDonald A. J. (1989) Coexistence of somatostatin with neuropeptide Y, but not with cholecystokinin or vasoactive intestinal peptide, in neurons of the rat amygdala.Brain Res. 500 37–45.

    PubMed  CAS  Google Scholar 

  • McDonald A. J. (1994) Neuronal localization of glutamate receptor subunits in the basolateral amygdala.Neuroreport 6, 13–16.

    PubMed  CAS  Google Scholar 

  • McDonald A. J. and Pearson J. C. (1989) Coexistence of GABA and peptide immunoreactivity in non-pyramidal neurons of the basolateral amygdala.Neurosci. Lett. 100, 53–58.

    PubMed  CAS  Google Scholar 

  • McGaugh J. L. (1989) Involvement of hormonal and neuromodulatory systems in the regulation of memory storage.Ann. Rev. Neurosci. 12, 255–287.

    PubMed  CAS  Google Scholar 

  • Mello L. E., Tan A. M., and Finch D. M. (1992a) Convergence of projections from the rat hippocampal formation, medial geniculate and basal forebrain onto single amygdaloid neurons: anin vivo extra- and intracellular electrophysiological study.Brain Res. 587, 24–40.

    PubMed  CAS  Google Scholar 

  • Mello L. E., Tan A. M., and Finch D. M. (1992b) GABAergic synaptic transmission in projections from the basal forebrain and hippocampal formation to the amygdala: anin vivo iontophoretic study.Brain Res. 587, 41–48.

    PubMed  CAS  Google Scholar 

  • Miserendino M. J., Sananes C. B., Melia K. R., and Davis M. (1990) Blocking of acquisition but not expression of conditioned fear-potentiated startle by NMDA antagonists in the amygdala.Nature (Lond.) 345, 716–718.

    CAS  Google Scholar 

  • Morrison F. and Poletti C. E. (1980) Hippocampal influences on amygdala unit activity in awake squirrel monkeys.Brain Res. 192, 353–369.

    PubMed  CAS  Google Scholar 

  • Muramoto K., Ono T., Nishijo H., and Fukuda M. (1993) Rat amygdaloid neuron responses during auditory discrimination.Neuroscience 52, 621–636.

    PubMed  CAS  Google Scholar 

  • Nicoll R. A. and Malenka R. C. (1995) Contrasting properties of two forms of long-term potentiation in the hippocampus.Nature (Lond.) 377, 115–118.

    CAS  Google Scholar 

  • Norgren R. (1976) Taste pathways to hypothalamus and amygdala.J. Comp. Neurol. 166, 17–30.

    PubMed  CAS  Google Scholar 

  • Nose I., Higashi H., Inokuchi H., and Nishi S. (1991) Synaptic responses of guinea pig and rat central amygdala neuronsin vitro.J. Neurophysiol. 65, 1227–1241.

    PubMed  CAS  Google Scholar 

  • Ono T., Nishijo H., and Uwano T. (1995) Amygdala role in conditioned associative learning.Prog. Neurobiol. 46, 401–422.

    PubMed  CAS  Google Scholar 

  • Ottersen O. P. (1980) Afferent connections of the amygdaloid complex of the rat and cat: II. afferents from the hypothalamus and the basal telencephalon.J. Comp. Neurol. 194, 267–298.

    PubMed  CAS  Google Scholar 

  • Ottersen O. P. (1981) Afferent connections of the amygdaloid complex of the rat with some observations in the cat: III. afferents from the lower brain stem.J. Comp. Neurol. 202, 335–356.

    PubMed  CAS  Google Scholar 

  • Ottersen O. P. (1982) Connections of the amygdala of the rat. IV: corticoamygdaloid and intra-amygdaloid connections as studied with axonal transport of horseradish peroxidase.J. Comp. Neurol. 205, 30–48.

    PubMed  CAS  Google Scholar 

  • Ottersen P. P. and Ben-Ari Y. (1979) Afferent connections to the amygdaloid complex of the rat and cat.J. Comp. Neurol. 187, 401–424.

    PubMed  CAS  Google Scholar 

  • Pare D., Smith Y., and Pare J.-F. (1995) Intra-amygdaloid projections of the basolateral and basomedial nuclei in the cat:Phaseolus vulgaris-leucoagglutinin anterograde tracing at the light and electron microscopic level.Neurosci. 69, 567–583.

    CAS  Google Scholar 

  • Pascoe J. P. and Kapp B. S. (1985) Electrophysiological characteristics of amygdaloid central nucleus neurons during Pavlovian fear conditioning in the rabbit.Behav. Brain Res. 16, 117–133.

    PubMed  CAS  Google Scholar 

  • Prelevic S., Burnham W. M., and Gloor P. (1976) A microelectrode study of amygdaloid afferents: temporal neocortex inputs.Brain Res. 105, 437–457.

    PubMed  CAS  Google Scholar 

  • Quirk G. J., Repa J. C., and LeDoux J. E. (1995) Fear conditioning enhances short-latency auditory responses of lateral amygdala neurons: parallel recordings in the freely behaving rat.Neuron 15, 1029–1039.

    PubMed  CAS  Google Scholar 

  • Racine R. J. and Milgram N. W. (1983) Short-term potentiation phenomena in the rat limbic forebrain.Brain Res. 260, 201–216.

    PubMed  CAS  Google Scholar 

  • Racine R. J., Milgram N. W., and Hafner S. (1983) Long-term potentiation phenomena in the rat limbic forebrain.Brain Res. 260, 217–31.

    PubMed  CAS  Google Scholar 

  • Rainnie D. G., Asprodini E. K., and Shinnick-Gallagher P. (1991a) Excitatory transmission in the basolateral amygdala.J. Neurophysiol. 66, 986–998.

    PubMed  CAS  Google Scholar 

  • Rainnie D. G., Asprodini E. K., and Shinnick-Gallagher P. (1991b) Inhibitory transmission in the basolateral amygdala.J. Neurophysiol. 66, 999–1009.

    PubMed  CAS  Google Scholar 

  • Rainnie D. G., Asprodini E. K., and Shinnick-Gallagher P. (1993) Intracellular recordings from morphologically identified neurons of the basolateral amygdala.J. Neurophysiol. 69, 1350–1362.

    PubMed  CAS  Google Scholar 

  • Rainnie D. G., Fernhout B. J. H., and Shinnick-Gallagher P. (1992) Differential actions of corticotropin releasing factor on basolateral and central amygdaloid neurones,in vitro.J. Pharmacol. Exp. Ther. 263, 846–858.

    PubMed  CAS  Google Scholar 

  • Rainnie D. G., Holmes K. H., and Shinnick-Gallagher P. (1994) Activation of postsynaptic metabotropic glutamate receptors bytrans-ACPD hyperpolarizes neurons of the basolateral amygdala.J. Neurosci. 14, 7208–7220.

    PubMed  CAS  Google Scholar 

  • Rainnie D. G. and Shinnick-Gallagher P. (1992)trans-ACPD andl-APB presynaptically inhibit excitatory glutamatergic transmission in the basolateral amygdala (BLA)Neurosci. Lett. 139, 87–91.

    PubMed  CAS  Google Scholar 

  • Rizvi T. A., Ennis M., Behbehani M. M., and Shipley M. T. (1991) Connections between the central nucleus of the amygdala and the midbrain periaqueductal gray: topography and reciprocity.J. Comp. Neurol. 303, 121–131.

    PubMed  CAS  Google Scholar 

  • Rogan M. T. and LeDoux J. E. (1995) LTP is accompanied by commensurate enhancement of auditory-evoked responses in a fear conditioning circuit.Neuron 15, 127–136.

    PubMed  CAS  Google Scholar 

  • Romanski L. M., Clugnet M. C., Bordi, F., and LeDoux J. E. (1993) Somatosensory and auditory convergence in the lateral nucleus of the amygdala.Behav. Neurosci. 107, 444–450.

    PubMed  CAS  Google Scholar 

  • Sananes C. B. and Davis M. (1992)N-methyl-d-aspartate lesions of the lateral and basolateral nuclei of the amygdala block fear-potentiated startle and shock sensitization of startle.Behav. Neurosci. 106, 72–80.

    PubMed  CAS  Google Scholar 

  • Sanghera M. K., Rolls E. T., and Roper-Hall A. (1979) Visual responses of neurons in the dorsolateral amygdala of the alert monkey.Exp. Neurol. 63, 610–626.

    PubMed  CAS  Google Scholar 

  • Sarter M. and Markowitsch H. J. (1985) Involvement of the amygdala in learning and memory: a critical review, with emphasis on anatomical relations.Behav. Neurosci. 99, 342–380.

    PubMed  CAS  Google Scholar 

  • Schiess M. C., Asprodini E. K., Rainnie D. G., and Shinnick-Gallagher P. (1993) The central nucleus of the rat amygdala:in vitro intracellular recordings.Brain Res. 604, 283–297.

    PubMed  CAS  Google Scholar 

  • Shindou T., Watanabe S., Yamamoto, K., and Nakanishi H. (1993) NMDA receptor-dependent formation of long-term potentiation in the rat medial amygdala neuron in anin vitro slice preparation.Brain Res. Bull. 31, 667–672.

    PubMed  CAS  Google Scholar 

  • Smith Y. and Pare D. (1994) Intra-amygdaloid projections of the lateral nucleus in the cat: PHA-L anterograde labeling combined with postembedding GABA and glutamate immunocytochemistry.J. Comp. Neurol. 342, 232–248.

    PubMed  CAS  Google Scholar 

  • Sripanidkulchai K., Sripanidkulchai B., and Wyss J. M. (1984) The cortical projection of the basolateral amygdaloid nucleus in the rat: a retrograde fluorescent dye study.J. Comp. Neurol. 229, 419–431.

    PubMed  CAS  Google Scholar 

  • Stefanacci L., Farb C. R., Pitkanen A., Go G., LeDoux J. E., and Amaral D. G. (1992) Projections from the lateral nucleus to the basal nucleus of the amygdala: a light and electron microscopic PHA-L study in the rat.J. Comp. Neurol. 323, 586–601.

    PubMed  CAS  Google Scholar 

  • Stringer J. L., Greenfield L. J., Hackett J. T., and Guyenet P. G. (1983) Blockade of long-term potentiation by phencyclidine and sigma opiates in the hippocampus in vivo and in vitro.Brain Res. 280, 127–138.

    PubMed  CAS  Google Scholar 

  • Sugita S. and North R. A. (1993) Opioid actions on neurons of rat lateral amygdalain vitro.Brain Res. 612, 151–155.

    PubMed  CAS  Google Scholar 

  • Sugita S., Shen K.-Z., and North R. A. (1992) 5-Hydroxytryptamine is a fast excitatory transmitter at 5-HT3 receptors in rat amygdala.Neuron 8, 199–203.

    PubMed  CAS  Google Scholar 

  • Sugita S., Tanaka E., and North R. A. (1993) Membrane properties and synaptic potentials of three types of neurone in rat lateral amygdala.J. Physiol. (Lond.) 460, 705–718.

    CAS  Google Scholar 

  • Sun N. and Cassell M. D. (1993) Intrinsic GABAergic neurons in the rat central extended amygdala.J. Comp. Neurol. 330, 381–404.

    PubMed  CAS  Google Scholar 

  • Sun N., Yi, H., and Cassell M. D. (1994) Evidence for a GABAergic interface between cortical afferents and brainstem projection neurons in the rat central extended amygdala.J. Comp. Neurol. 340, 43–64.

    PubMed  CAS  Google Scholar 

  • Turner B. H. and Herkenham M. (1991) Thalamoamygdaloid projections in the rat: a test of the amygdala’s role in sensory processing.J. Comp. Neurol. 313, 295–325.

    PubMed  CAS  Google Scholar 

  • Uwano T., Nishijo H., Ono T., and Tamure R. (1995) Neuronal responsiveness to various sensory stimuli, and associative learning in the rat amygdala.Neuroscience 68, 339–361.

    PubMed  CAS  Google Scholar 

  • Van Groen T. and Wyss J. M. (1990) Extrinsic projections from area CA1 of the rat hippocampus: olfactory, cortical, subcortical, and bilateral hippocampal formation projections.J. Comp. Neurol. 302, 515–528.

    PubMed  Google Scholar 

  • Veenig J. G. (1978a) Cortical afferents of the amygdaloid complex in the rat: an HRP study.Neurosci. Lett. 8, 191–195.

    Google Scholar 

  • Veenig J. G. (1978b) Subcortical afferents of the amygdaloid complex in the rat: an HRP study.Neurosci. Lett. 8, 197–202.

    Google Scholar 

  • Wang S.-J., Huang C.-C., and Gean P.-W. (1995) Tetrahydro-9-aminoacridine presynaptically inhibits glutamatergic transmission in the rat amygdala.Brain Res. Bull. 37, 325–327.

    PubMed  CAS  Google Scholar 

  • Washburn M. S. and Moises H. C. (1992a) Electrophysiological and morphological properties of rat basolateral amygdaloid neuronsin vitro.J. Neurosci. 12, 4066–4079.

    PubMed  CAS  Google Scholar 

  • Washburn M. S. and Moises H. C. (1992b) Inhibitory responses of rat basolateral amygdaloid neurons recordedin vitro.Neuroscience 50, 811–830.

    PubMed  CAS  Google Scholar 

  • Watanabe Y., Ikegaya Y., Saito H., and Abe K. (1995a) Roles of GABAA, NMDA and muscarinic receptors in the induction of long-term potentiation in the medial and lateral amygdalain vitro.Neurosci. Res. 21, 317–322.

    PubMed  CAS  Google Scholar 

  • Watanabe Y., Saito H., and Abe K. (1995b) Nitric oxide is involved in long-term potentiation in the medial but not lateral amygdala neuron synapsesin vitro.Brain Res. 688, 233–236.

    PubMed  CAS  Google Scholar 

  • Wigstrom H. and Gustafsson B. (1986) Postsynaptic control of hippocampal long-term potentiation.J. Physiol. (Lond.) 81, 228–236.

    CAS  Google Scholar 

  • Womble M. D. and Moises H. C. (1992). Muscarinic inhibition of M-current and a potassium leak conductance in neurones of the rat basolateral amygdala.J. Physiol. 457, 93–114.

    PubMed  CAS  Google Scholar 

  • Womble M. D. and Moises H. C. (1993a) Hyperpolarization-activated currents in neurons of the rat basolateral amygdala.J. Neurophysiol. 70, 2056–2065.

    PubMed  CAS  Google Scholar 

  • Womble M. D. and Moises H. C. (1993b) Muscarinic modulation of conductances underlying the afterhyperpolarization in neurons of the rat basolateral amygdala.Brain Res. 621, 87–96.

    PubMed  CAS  Google Scholar 

  • Wyss J. M. (1981) An autoradiographic study of the efferent connections of the entorhinal cortex in the rat.J. Comp. Neurol. 199, 495–512.

    PubMed  CAS  Google Scholar 

  • Yu B. and Shinnick-Gallagher P. (1994) Interleukin-1β inhibits synaptic transmission and induces membrane hyperpolarization in amygdala neurons.J. Pharmacol. Exp. Ther. 271, 590–600.

    PubMed  CAS  Google Scholar 

  • Zalutsky R. A. and Nicoll R. A. (1990) Comparison of two forms of long-term potentiation in single hippocampal neurons.Science 248, 1619–1624.

    PubMed  CAS  Google Scholar 

  • Zucker R. S. (1989) Short-term synaptic plasticity.Ann. Rev. Neurosci. 12, 13–31.

    PubMed  CAS  Google Scholar 

Download references

Author information

Affiliations

  1. Department of Psychology, University of Michigan, 525 E. University Avenue, 48109-1109, Ann Arbor, MI

    Stephen Maren

Authors
  1. Stephen Maren
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Maren, S. Synaptic transmission and plasticity in the amygdala. Mol Neurobiol 13, 1–22 (1996). https://doi.org/10.1007/BF02740749

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02740749

Index Entries

  • Amygdala
  • long-term potentiation
  • glutamate receptors
  • learning
  • memory
  • rats