Differential Synaptic Input to External Globus Pallidus Neuronal Subpopulations In Vivo

The rodent external globus pallidus (GPe) contains two main neuronal subpopulations, prototypic and arkypallidal cells, which differ in their cellular properties. Their functional synaptic connectivity is largely unknown. Here we studied the membrane properties, synaptic inputs, and sensory responses of these subpopulations in the mouse GPe. We performed in vivo whole-cell recordings in GPe neurons and used optogenetic stimulation to dissect their afferent inputs from the striatum and subthalamic nucleus (STN). Both GPe subpopulations received barrages of excitatory and inhibitory inputs during slow wave activity and responded to sensory stimulation with distinct multiphasic patterns. Prototypic cells synaptically inhibited arkypallidal and prototypic cells. Both GPe subpopulations received synaptic input from STN and striatal medium spiny neurons (MSNs). Although STN and indirect pathway MSNs strongly targeted prototypic cells, direct pathway MSNs selectively inhibited arkypallidal cells. We show that GPe subtypes have distinct connectivity patterns that underlie their respective functional roles.