Aversive stimulus-tuned responses in the CA1 of the dorsal hippocampus

Throughout life animals inevitably encounter unforeseen threatening events. Activity of principal cells in the hippocampus is tuned for locations and for salient stimuli in the animals’ environment thus forming a map known to be pivotal for guiding behavior. Here, we explored if a code of threatening stimuli exists in the CA1 region of the dorsal hippocampus of mice by recording neuronal response to aversive stimuli delivered at changing locations. We have discovered a rapidly emerging, location independent response to innoxious aversive stimuli composed of the coordinated activation of subgroups of pyramidal cells and connected interneurons. Activated pyramidal cells had higher basal firing rate, more probably participated in ripples, targeted more interneurons than place cells and many of them lacked place fields. We also detected aversive stimulus-coupled assemblies dominated by the activated neurons. Notably, these assemblies could be observed even before the delivery of the first aversive event. Finally, we uncovered the systematic shift of the spatial code from the aversive to, surprisingly, the reward location during the fearful stimulus. Our results uncovered components of the dorsal CA1 circuit possibly key for re-sculpting the spatial map in response to abrupt aversive events.