Unlike the sensory thalamus, studies on the functional organization of the midline and intralaminar nuclei are scarce, and this has hindered the establishment of conceptual models of the function of this brain region. We investigated the functional organization of the paraventricular nucleus of the thalamus (PVT), a midline thalamic structure that is increasingly being recognized as a critical node in the control of diverse processes such as arousal, stress, emotional memory and motivation, in mice. We identify two major classes of PVT neurons-termed type I and type II-that differ in terms of gene expression, anatomy and function. In addition, we demonstrate that type II neurons belong to a previously neglected class of PVT neurons that convey arousal-related information to corticothalamic neurons of the infralimbic cortex. Our results uncover the existence of an arousal-modulated thalamo-corticothalamic loop that links the PVT and the ventromedial prefrontal cortex.