Two distinct glutamatergic synaptic inputs to striatal medium spiny neurones of neonatal rats and paired-pulse depression.

Excitatory postsynaptic currents (EPSCs) were recorded from the medium spiny neurones of neonatal rat striatal slices using the whole-cell patch clamp method. EPSCs were selectively elicited in the presence of picrotoxin with a glass stimulating pipette placed in the striatum. We found two distinct unitary EPSCs that were evoked by stimulation of single presynaptic fibres. The major type of EPSC, termed 'S-type', failed frequently and had a small mean amplitude (2.05 pA). They probably represented cortical afferents. The other type of unitary EPSC, the 'H-type', seldom failed and was 13 times larger than the S-type. Spontaneous EPSCs with amplitudes similar to those of H-type EPSCs could be induced. H-type EPSCs were mediated by both non-NMDA and NMDA receptors. The two types of EPSCs could be evoked in the same neurons. The intensity of stimulation for H-type EPSCs was higher than that for S-type EPSCs. H-type EPSCs could be polysynaptically activated, suggesting the presence of glutamatergic interneurones in the striatum that generated H-type EPSCs. H-type EPSCs displayed particularly long-lasting paired-pulse depression, while that displayed by the S-type EPSCs was short. The paired-pulse depression of both EPSCs was Ca2+ dependent and involved presynaptic mechanisms. We have demonstrated that the medium spiny neurones of neonatal rats receive two different glutamatergic input systems having different amplitudes, origins and paired-pulse depression, reminiscent of cerebellar Purkinje cells. This suggests that the two types of EPSCs also play distinctive roles in striatal neuronal circuitry.