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Journal of Neuroscience, Vol 12, 4224-4233, Copyright © 1992 by Society for Neuroscience
Long-term synaptic depression in the striatum: physiological and pharmacological characterization
P Calabresi, R Maj, A Pisani, NB Mercuri and G Bernardi
Clinica Neurologica, Dip. Sanita, II Universita di Roma, Italy.
The effect of tetanic activation of corticostriatal glutamatergic fibers
was studied in striatal slices by utilizing extracellular and intracellular
recording techniques. Tetanic stimulation produced a long- term synaptic
depression (LTD) (> 2 h) of both extracellularly recorded field
potentials and intracellularly recorded EPSPs. LTD was not coupled with
changes of intrinsic membrane properties of the recorded neurons. In some
neurons, repetitive cortical activation produced a short-term posttetanic
potentiation (1-3 min). Subthreshold tetanic stimulation, which under
control condition did not cause LTD, induced LTD when associated with
membrane depolarization. Moreover, LTD was not expressed in cells in which
the conditioning tetanus was coupled with hyperpolarization of the
membrane. Bath application of aminophosphonovalerate (30-50 microM), an
antagonist of NMDA receptors, did not affect the amplitude of the synaptic
potentials and the expression of LTD. Striatal LTD was significantly
reduced by the pretreatment of the slices with 30 microM
2-amino-3-phosphonopropionic acid, an antagonist of glutamate metabotropic
receptors. LTD was not blocked by bicuculline (30 microM), a GABA(A)
receptor antagonist. Scopolamine (3 microM), an antagonist of muscarinic
receptors, induced a slight, but significant, increase of the amplitude of
LTD. Both SCH 23390 (3 microM), an antagonist of D1 dopamine (DA)
receptors, and I- sulpiride (1 microM), an antagonist of D2 DA receptors,
blocked LTD. LTD was also absent in slices obtained from rats in which the
nigrostriatal DA system was lesioned by unilateral nigral injection of
6-hydroxydopamine. In DA-depleted slices, LTD could be restored by applying
exogenous DA (30 microM) before the conditioning tetanus. In DA-depleted
slices, LTD could also be restored by coadministration of SKF 38393 (3-10
microM), a D1 receptor agonist, and of LY 171555 (1-3 microM), a D2
receptor agonist. Application of a single class of DA receptor agonists
failed to restore LTD. These data show that striatal LTD requires three
main physiological and pharmacological conditions: (1) membrane
depolarization and action potential discharge of the postsynaptic cell
during the conditioning tetanus, (2) activation of glutamate metabotropic
receptors, and (3) coactivation of D1 and D2 DA receptors. Striatal LTD may
alter the output signals from the striatum to the other structures of the
basal ganglia. This form of synaptic plasticity can influence the striatal
control of motor activity.
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