Precise coupling of the thalamic head-direction system to hippocampal ripples

The anterior thalamus is a key relay of neuronal signals within the limbic system. During sleep, the occurrence of hippocampal sharp wave-ripples (SWRs), believed to mediate consolidation of explicit memories, is modulated by thalamocortical network activity, yet how information is routed around SWRs and how this communication depends on neuronal dynamics remains unclear. Here, by simultaneously recording ensembles of neurons in the anterior thalamus and local field potentials in the CA1 area of the hippocampus, we show that the head-direction (HD) cells of the anterodorsal nucleus are set in stable directions immediately before SWRs. This response contrasts with other thalamic cells that exhibit diverse couplings to the hippocampus related to their intrinsic dynamics but independent of their anatomical location. Thus, our data suggest a specific and homogeneous contribution of the HD signal to hippocampal activity and a diverse and cell-specific coupling of non-HD neurons. Thalamic head direction (HD) cells are necessary to establish spatial maps in the hippocampus. Here, the authors show that HD cells tuned to a particular direction are coupled to individual hippocampal ripple events during sleep, suggesting an influence of the replay of specific trajectories during sleep memory consolidation.

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