The function and the origin of replay of motor activity during sleep are currently unknown. Spontaneous activity patterns in the nucleus robustus of the arcopallium (RA) and in HVC (a letter-based name) of the sleeping songbird resemble premotor patterns in these areas observed during singing. We test the hypothesis that the nucleus interface of the nidopallium (NIf) has an important role for initiating and shaping these sleep-related activity patterns. In head-fixed, sleeping zebra finches we find that injections of the GABAA-agonist muscimol into NIf lead to transient abolishment of premotor-like bursting activity in HVC neurons. Using antidromic activation of NIf neurons by electrical stimulation in HVC, we are able to distinguish a class of HVC-projecting NIf neurons from a second class of NIf neurons. Paired extracellular recordings in NIf and HVC show that NIf neurons provide a strong bursting drive to HVC. In contrast to HVC neurons, whose bursting activity waxes and wanes in burst epochs, individual NIf projection neurons are nearly continuously bursting and tend to burst only once on the time scale of song syllables. Two types of HVC projection neurons, premotor and striatal projecting, respond differently to the NIf drive, in agreement with notions of HVC relaying premotor signals to RA and an anticipatory copy thereof to areas of a basal ganglia pathway.