The striatum constitutes the main input structure of the basal ganglia and is mainly composed of GABAergic medium spiny neurons (MSNs) giving rise to the direct and indirect pathways. An additional compartmentalization of the striatum, consisting in the striosomes and the matrix was described decades ago. The respective network organization and functions of these compartments are much less understood along with the differences in their MSNs intrinsic properties. Our aim is to assess the intrinsic properties of the striosomal and matrix neurons and to characterize their functional connectivity. Using a BAC-Cre transgenic mouse combined with stereotactic injections of Cre-dependent virus and patch clamp experiments, we measured the electrical membrane properties of the striosomal and matrix neurons. Using optogenetics, we obtained light-induced post-synaptic responses in the external globus pallidus (GPe), substantia nigra pars reticulata (SNr) and pars compacta (SNc). Striosomal neurons displayed increased spiking and a substantial shift in membrane resistance, tau and rheobase when compared to the matrix. Light stimulation induced short-term synaptic depression of striosomal and matrix MSNs to GPe and to SNr synapses which was more pronounced in striosomo-pallidal and matrix-nigral synapses. These results indicate a greater excitability of striosome MSNs compared with matrix MSNs. Previous developmental studies of striatopallidal and striatonigral synapses without specific identification of striosome and matrix MSNs have reported short term facilitation as a signature of these synapses. Our results suggest the existence of differences in the synaptic dynamic when stimulating exclusively striosomal or matrix MSNs to GPe and SNr synapses during adulthood.