Sharp waves of the head-direction system

The head-direction (HD) system is an essential component of the spatial navigation system and is believed to provide key signals during sleep to support memory formation in the downstream parahippocampal regions. The HD signal is processed by a mammillary-thalamic-subicular loop within the Papez circuits. Specifically, the lateral mammillary nucleus (LMN) receives an angular velocity signal from the brainstem and is believed to form an attractor network supporting the generation of the HD signal. By recording from ensembles of LMN neurons in freely moving mice during wakefulness and sleep, we reveal the existence of a brief sharp wave (<20ms) generated in the LMN. These “HD-waves” occurred mainly, but not only, during sleep at an average occurrence rate of about 1Hz. It recruited strong firing within the LMN and activated neurons in the thalamic and subicular stages of the HD system. During non-Rapid Eye Movement sleep, it was negatively coupled with hippocampal sharp waves-ripples (SWRs), suggesting that HD-waves and SWRs are orchestrated by antagonist neuromodulatory systems. Overall, like SWRs that emerge from recurrent connectivity within the CA3 area of the hippocampus, HD-waves provide further evidence for the existence of an attractor network in the LMN. These findings also suggest that the HD circuit generates strong population bursts with potential implication for sleep-dependent memory formation.