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