The retrosplenial cortex (RSC) and hippocampus support the encoding, storage, and retrieval of different aspects of associative experience. In the hippocampus, learning and updating information about the content details of space triggers long-term depression (LTD) (doi: 10.3389/fnbeh.2022.806356) . Here we used fluorescence in situ hybridization (FISH) explore to what extent this kind of spatial content learning triggers somatic immediate early gene (IEG i.e. Homer1a) expression in the cornus ammonis and RSC, as an indication of active storage of learned experience. Adult rats explored novel spatial constellations of small items concealed in holeboard holes either with, or without, electrophysiological stimulation of Schaffer collateral-CA1 synapses. We found that the CA1 region that is near to the subiculum (distal CA1) and the CA3 region that is near to CA1 (proximal-CA3), as well as the entire RSC, exhibited significant elevations of somatic IEG expression following the learning event. Responses were similar when weak afferent SC stimulation was coupled with item constellation learning that resulted in SC-LTD. By contrast, induction of LTD by strong afferent stimulation in the absence of learning resulted in an homogenous elevation of nuclear Homer1a expression across the entire proximodistal CA-axis following LTD induction solely by means of afferent stimulation and weaker RSC IEG expression than that elicited by learning. Our results indicate that the hippocampal CA regions and the RSC both engage in encoding of spatial content in a process that is likely to be interrelated.Supported by a grant from the German Research Foundation (DFG) to D.M.-V. (SFB874/B1, Projectnr: 122679504).