Relating storage of specific information to a particular neuromorphological change is difficult because behavioral performance factors are not readily disambiguated from underlying cognitive processes. This issue is addressed here by demonstrating robust reorganization of the hippocampal mossy fiber terminal field (MFTF) when adult rats learn the location of a hidden platform but not when rats learn to locate a visible platform. Because the latter task requires essentially the same behavioral performance as the former, the observed MFTF growth is seen as the consequence of specific input-dependent hippocampal activity patterns selectively generated by processing of extramaze but not intramaze cues. Successful performance on the hidden platform task requires formation of spatial memory. Increased MFTFs in hidden platform-trained rats are observed 7 d but not 2 d after training nor in swim controls. These results suggest that structural plasticity of the mossy fiber: CA3 circuit may contribute to the maintenance of long-lasting memory but not to the initial storage of the spatial context.