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The Journal of Neuroscience, March 1, 1998, 18(5):1662-1670

Bidirectional Synaptic Plasticity in the Rat Basolateral Amygdala: Characterization of an Activity-Dependent Switch Sensitive to the Presynaptic Metabotropic Glutamate Receptor Antagonist 2S--Ethylglutamic Acid

He Li¹, Susan R. B. Weiss², De-Maw Chuang², Robert M. Post², and Michael A. Rogawski¹

¹ Epilepsy Research Branch, National Institute of Neurological Disorders and Stroke, and ² Biological Psychiatry Branch, National Institute of Mental Health, National Institutes of Health, Bethesda, Maryland 20892

This study examines forms of activity-dependent synaptic plasticity in the basolateral amygdala in vitro and demonstrates that a brief high frequency stimulus (HFS) train can induce a switch in the direction of the enduring change in synaptic strength induced by subsequent low-frequency stimulation (LFS). LFS (1 Hz, 15 min) of the external capsule (EC) induced a persistent 1.7-fold enhancement in the amplitude of synaptic potentials recorded intracellularly in basolateral amygdala neurons. The enhancement occurred gradually during the stimulation and was maintained for >30 min after termination of the stimulus train. LFS-induced enduring synaptic facilitation was not affected by the NMDA receptor antagonist D()-2-amino-5-phosphonopentanoate (APV; 100 µM). Brief high-frequency EC stimulation (HFS; 100 Hz, 1 sec) induced APV-sensitive short-term potentiation (2.5-fold) that generally decayed within 10 min. When LFS was applied after recovery from the short-term potentiating effect of HFS (HFS/LFS), there was an initial transient (<10 min) enhancement of the synaptic response followed by persistent synaptic depression (synaptic potential amplitude reduced by 22% at 30 min). This represents the first demonstration of stimulus-dependent long-lasting synaptic depression in the amygdala. Application of the presynaptic (group II) metabotropic glutamate receptor antagonist 2S--ethylglutamic acid (EGLU; 50 µM) prevented the HFS-dependent switch from synaptic facilitation to depression. Thus, LFS in the in vitro amygdala slice can induce either enduring synaptic potentiation or depression, depending on whether a priming HFS train has been applied. This experience-dependent switch, a novel form of metaplasticity, is not dependent on NMDA receptors but may require group II metabotropic glutamate receptors. In the amygdala, experiential modification of activity-dependent long-term synaptic plasticity adds flexibility to the ways in which synaptic strength can be modified and could play a role in diverse amygdala-dependent processes, including the formation, storage, and extinction of emotional memory and the regulation of epileptogenesis.

Key words: basolateral amygdala; synaptic plasticity; long-term potentiation; long-term depression; NMDA receptor; metabotropic glutamate receptor; 2S--ethylglutamic acid

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Copyright © 1998 Society for Neuroscience  0270-6474/98/1851662-09$05.00/0

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