Calcium-mediated paired pulse depression in juvenile rat dorsal striatum

Abstract

As the major division of the basal ganglia, neostriatum forms mutual connections with multiple brain areas and is critically involved in motor control and learning/memory. Long-term synaptic plasticity has been widely studied in different species recently. However, there are rare reports about the short-term synaptic plasticity in neostratium. In the present study, using field excitatory postsynaptic potentials recording, we reported one form of short-term synaptic plasticity that is paired pulse depression in juvenile rat dorsal striatum slices induced by stimuli of the white matter. The field excitatory postsynaptic potentials could be abolished by α-amino-3-hydroxy-5-methylizoxazole-4-propionic acid receptor antagonist, 6-cyano-7-nitroquinoxaline-2,3-dione, but not by gamma-aminobutyric acid type A receptor antagonist bicuculline or dopamine D1 receptor antagonist SKF-81297. The paired pulse depression in the corticostratial pathway was different from paired pulse facilitation in the hippocampal CA1 synapse. In addition, the paired pulse depression was not affected by bath application of gamma-aminobutyric acid type A receptor antagonist or dopamine D1 receptor antagonist. However, low calcium and high magnesium could attenuate the paired pulse depression. These findings suggest a more complicated plasticity form in the dorsal striatum of juvenile rats that is different from that in the hippocampus, which is related with extracellular calcium.

Keywords: calcium; dorsal striatum; juvenile rats; paired pulses depression.

Figure 1

Effect of bicuculline (gamma-aminobutyric acid type A receptor antagonist) and CNQX (α-amino-3-hydroxy-5-methylizoxazole-4-propionic acid receptor antagonist) on striatal population spike. CNQX: 6-cyano-7-nitroquinoxaline-2,3-dione. (A) Representative trace of paired pulse induced population spike in rat corticostriatal slice, and the insert is the magnified P1. (B) Averaged paired pulse ratio pre- and post-bicuculline administration; the insert is averaged P1 amplitude before and after bath application of bicuculline. Measurement data are expressed as mean ± SE. (C) Representative trace of paired pulse induced population spike after bath application of bicuculline. (D) Representative trace of recording from corticostriatal slice pre- and post-CNQX administration.

Figure 2

Effect of bicuculline on hippocampal field excitatory postsynaptic potentials (fEPSP) (A–C) and difference of paired pulse ratio between the hippocampus and striatum (D). (A) Representative trace of paired pulse facilitation in rat hippocampal slices before application of gamma-aminobutyric acid type A receptor antagonist bicuculline (20 μM). (B) Representative trace of paired pulse facilitation in rat hippocampal slices after bath application of gamma-aminobutyric acid type A receptor antagonist bicuculline (20 μM); the insert is averaged P1 amplitude before and after bath application of bicuculline. (C) Trace of paired pulse facilitation after washout of bicuculline. (D) Averaged paired pulse ratio from rat hippocampal and corticostriatal slices. Measurement data are expressed as mean ± SE. ^aP = 0.001, 0.001 2, 0.03, vs. at the hippocampus 20, 40 and 80 interstimulus interval, respectively.

Figure 3

Succinylcholine chloride (muscarinic receptor antagonist) (20 μM) had no effect on the paired pulse depression of population spike/field excitatory postsynaptic potentials. Representative trace of paired pulse depression in rat hippocampal slices before (A) and after (B) application of succinylcholine chloride. (C) Averaged paired pulse ratio pre- and post-succinylcholine chloride administration. Measurement data are expressed as mean ± SE.

Figure 4

SKF-81297(dopamine D1 receptor antagonist) (20 μM) had no effect on the paired pulse depression of population spike/field excitatory postsynaptic potentials. Representative trace of paired pulse depression in rat hippocampal slices before (A) and after (B) application of succinylcholine chloride. (C) Averaged paired pulse ratio pre- and post-SKF-81297 administration. Measurement data are expressed as mean ± SE.

Figure 5

Lowing extracellular calcium partially reduced the striatal paired pulse depression of population spike/field excitatory postsynaptic potential. Representative trace of paired pulse depression of population spike/field excitatory postsynaptic potential in rat striatal slices by application of 2.6 mM Ca²⁺, 1.3 mM Mg²⁺ (A) or 0.5 mM Ca²⁺, 1.3 mM Mg²⁺ (B). (C) Averaged paired pulse ratio via 0.5 mM Ca²⁺ administration. Measurement data are expressed as mean ± SE.

Figure 6

Schematic diagram of the field potential recording from the dorsal striatum (A) and hippocampus (B). Sti: Stimulator; rec, recording electrode; DG: dentate gyrus.