To characterize the organization and plasticity of the trigeminal reflex blink circuit, we interacted blink-evoking supraorbital (SO) and infraorbital (IO) nerve stimuli in alert rats. Stimulation of either trigeminal branch produced a short-lasting inhibition followed by a longer-lasting facilitation of blinks evoked by stimulating the other nerve. When IO stimulation evoked a smaller blink than SO stimulation (IO < SO), SO stimulation facilitated subsequent IO-evoked blinks more than IO stimulation facilitated SO-evoked blinks. When IO > SO, IO and SO stimulation exerted equivalent facilitation of subsequent reflex blinks. To investigate whether the blink circuit obeyed rules analogous to those governing the associative and spike timing-dependent plasticity exhibited by individual synapses, we compared the effects of 3600 simultaneous IO and SO pairings, asynchronous IO and SO pairings, or synchronous IO and SO pairings separated by 20 ms on temporal interactions between IO and SO inputs to the blink circuit. Simultaneous pairing of a weak IO and a strong SO strengthened the IO input to the blink circuit, whereas asynchronous pairing weakened the stronger input. When the pairing pattern made an afferent input arrive after blink circuit activity, it weakened that afferent input. Analogous to synaptic modifiability, the results revealed that blink-evoking stimuli acted as a "presynaptic input" and blink circuit activity acted as a "postsynaptic spike." These mechanisms may create the maladaptive reorganization of trigeminal inputs in diseases such as hemifacial spasm.