The dorsal midline thalamus (dMT) is a group of non-sensory thalamic nuclei that has been implicated in arousal and in the homeostatic maintenance of sleep choreography. Neocortical slow oscillations and hippocampal sharp wave ripples (SPW-R) are the hallmarks of non-rapid eye-movement (NREM) sleep and reflect synchronous activation of neocortical and hippocampal neuronal ensembles, respectively. The dMT is reciprocally connected both with the neocortex and with the hippocampal system, however, little is known about their interaction during sleep. We performed large-scale unit recordings from dMT neurons during unrestrained sleep-wake behavior, while simultaneously recorded population activity from the prelimbic cortex and ventral subiculum, the main output of the hippocampus. We found that neurons are differentially coupled to cortical DOWN states and hippocampal SPW-Rs in the posterior and anterior segments of dMT, and they show different firing characteristics during sleep-wake behavior.Surprisingly, we found that a fraction of dMT neurons are selectively active during cortical DOWN states and their activity is either negatively or not correlated with hippocampal SPW-Rs. When the activity of these DOWN state active neurons (DSA) are compared with the rest of the population, we found that DSA neurons showed higher correlation with each other than with non-DSA neurons in both in NREM sleep and during wakefulness, suggesting the presence of two antagonistic subnetworks within the dMT. These findings demonstrate how neocortical and hippocampal/subicular regions can influence this “limbic” thalamic nucleus. In the reverse direction, dMT may coordinate activity across wide cortical and subcortical areas.