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The Journal of Neurophysiology Vol. 84 No. 2 August 2000, pp. 759-770
Copyright ©2000 by the American Physiological Society
Department of Pharmacology and Toxicology, The University of Texas Medical Branch, Galveston, Texas 77555-1031
Neugebauer, Volker,
Fatiha Zinebi,
Rex Russell,
Joel P. Gallagher, and
Patricia Shinnick-Gallagher.
Cocaine and Kindling Alter the Sensitivity of Group II and III
Metabotropic Glutamate Receptors in the Central Amygdala. J. Neurophysiol. 84: 759-770, 2000. G-protein-coupled metabotropic glutamate receptors (mGluRs) are being
implicated in various forms of neuroplasticity and CNS disorders. This
study examined whether the sensitivities of mGluR agonists are
modulated in a distinct fashion in different models of synaptic
plasticity, specifically, kindling and chronic cocaine treatment. The
influence of kindling and chronic cocaine exposure in vivo was examined
in vitro on the modulation of synaptic transmission by group II and III
metabotropic glutamate receptors using whole cell voltage-clamp
recordings of central amygdala (CeA) neurons. Synaptic transmission was
evoked by electrical stimulation of the basolateral amygdala (BLA) and
ventral amygdaloid pathway (VAP) afferents in brain slices from control
rats and from rats treated with cocaine or exposed to three to five
stage-five kindled seizures. This study shows that after chemical
stimulation with chronic cocaine exposure or after electrical
stimulation with kindling the receptor sensitivities for mGluR agonists
are altered in opposite ways. In slices from control rats, group II
agonists, (2S,1'S,2'S)-2-(carboxycyclopropyl)glycine (LCCG1) and
(+)-2-aminobicyclo[3.1.0]hexane-2,6-dicarboxylic acid (LY354740),
depressed neurotransmission more potently at the BLA-CeA than at the
VAP-CeA synapse while group III agonist, L(+)-2-amino-4-phosphonobutyrate (LAP4), depressed neurotransmission more potently at the VAP-CeA synapse than at the BLA-CeA. These agonist
actions were not seen (were absent) in amygdala neurons from chronic
cocaine-treated animals. In contrast, after kindling, concentration
response relationships for LCCG1 and LAP4 were shifted to the left,
suggesting that sensitivity to these agonists is increased. Except at
high concentrations, LCCG1, LY354740, and LAP4 neither induced membrane
currents nor changed current-voltage relationships. Loss of mGluR
inhibition with chronic cocaine treatment may contribute to
counter-adaptive changes including anxiety and depression in cocaine
withdrawal. Drugs that restore the inhibitory effects of group II and
III mGluRs may be novel tools in the treatment of cocaine dependence.
The enhanced sensitivity to group II and III mGluR agonists in kindling
is similar to that recorded at the lateral to BLA synapse in the
amygdala where they reduce epileptiform bursting. These findings
suggest that drugs modifying mGluRs may prove useful in the treatment
of cocaine withdrawal or epilepsy.
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