During sleep, spontaneous neuronal activity in the spatial navigation system recapitulates previous wake experiences, and this phenomenon is instrumental for learning and memory. Specifically, in the hippocampus, place cell ensembles are spontaneously replayed in sequences corresponding to trajectories of the animal in previously visited environments1. In parallel, head-direction cells of the anterodorsal thalamic nucleus which fire for a specific direction of the animal’s head, remain coordinated during sleep. The HD signal is crucial for spatial navigation and the anterior thalamus is necessary for spatial memory, yet whether thalamic HD cells and hippocampal activity are coordinated during sleep and how much this coordination depends on learning remain unknown. To address this question, we recorded neuronal ensembles of HD cells and hippocampal place cells in freely moving mice performing a spatial memory task. Animals were trained on a forced alternation task on a Y-maze, during which they had only one path to take on each trial. On the day of the recording, after the forced choice task, the animal performed a free alternation task in which it was free to choose either one the two arms and spontaneously alternated between them. Sleep was recorded before and after each task. HD cells fired systematically 50-100 ms before hippocampal neurons. We observed mild reactivation in the hippocampus in the two sleep sessions following the tasks, as expected in a highly familiar environment. HD cells showed no reactivation after the forced alternation but interestingly, showed strong reactivation after the free alternation task. Furthermore, HD and hippocampal ensembles reactivated together after the free alternation task. Hence, during sleep following exposure to a familiar context, the hippocampus potentially reactivates independently of other structures, and spatial learning recruits large scale thalamocortical networks upstream of the hippocampus. These findings shed a new light on the mechanisms of sleep-dependent learning.