The head direction (HD) system functions as a compass with member neurons robustly increasing their firing rates when the animal’s head points in a specific direction. HD neurons may be driven by peripheral sensors or, as computational models postulate, internally-generated (‘attractor’) mechanisms. We addressed the contributions of stimulus-driven and internally-generated activity by recording ensembles of HD neurons in the antero-dorsal thalamic nucleus and the postsubiculum of mice by comparing their activity in various brain states. The temporal correlation structure of HD neurons is preserved during sleep, characterized by a 60°-wide correlated neuronal firing (‘activity packet’), both within as well as across these two brain structures. During REM, the spontaneous drift of the activity packet was similar to that observed during waking and accelerated tenfold during slow wave sleep. These findings demonstrate that peripheral inputs impinge upon an internally-organized network, which provides amplification and enhanced precision of the head-direction signal.