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Fear conditioning induces a lasting potentiation of synaptic currents in vitro

Nature volume 390, pages 607–611 (1997)Cite this article

Abstract

The amygdala plays a critical role in the mediation of emotional responses, particularly fear, in both humans and animals1,2,3,4. Fear conditioning, a conditioned learning paradigm, has served as a model for emotional learning in animals, and the neuroanatomical circuitry underlying the auditory fear-conditioning paradigm is well characterized5. Synaptic transmission in the medial geniculate nucleus (MGN) to lateral nucleus of the amygdala (LA) pathway, a key segment of the auditory fear conditioning circuit, is mediated largely through N-methyl-D-aspartate (NMDA) and non-NMDA (such as α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA)) glutamate receptors6; the potential for neural plasticity in this pathway is suggested by its capacity to support long-term potentiation (LTP)7,8. Here we report a long-lasting increase in the synaptic efficacy of the MGN–LA pathway attributable to fear-conditioning itself, rather than an electrically induced model of learning. Fear-conditioned animals show a presynaptic facilitation of AMPA-receptor-mediated transmission, directly measured in vitro with whole-cell recordings in lateral amygdala neurons. These findings represent one of the first in vitro measures of synaptic plasticity resulting from emotional learning by whole animals.

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Figure 1: Fear conditioning results in potentiation of evoked EPSCs.
Figure 2: PPF is decreased in fear-conditioned animals.
Figure 3: The endopyriform–LA pathway is not potentiated in fear-conditioned animals.

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Acknowledgements

We thank J. E. Blankenship, B. Christensen, J. Gallagher, K. Johnson, M. Thomas and V. Neugebauer for critically reading the manuscript, and K. Cunningham for statistical assistance. This work was supported by the John Sealy Memorial Endowment Fund for Biomedical Research (P.S.G.), an NIMH National Research Service Award (M.G.M.) and a PhRMA Medical Student Research Fellowship in Pharm.-Clinical Pharmacology (M.G.M.).

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  1. Department of Pharmacology and Toxicology, The University of Texas Medical Branch, Galveston, 77555-1031, Texas, USA

    M. G. McKernan & P. Shinnick-Gallagher

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Correspondence to P. Shinnick-Gallagher.

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McKernan, M., Shinnick-Gallagher, P. Fear conditioning induces a lasting potentiation of synaptic currents in vitro. Nature 390, 607–611 (1997). https://doi.org/10.1038/37605

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