The Morris water maze has been extensively used in the study of spatial learning and memory, and a number of hippocampal, parahippocampal and neocortical brain regions have been identified as necessary for successful performance in this task. Immediate Early Genes (IEGs) have been implicated in learning and memory processes, and are used as markers of neural activity in a brain region in response to learning tasks. The use of adequate control conditions in these tasks has been identified as important, and we devised a novel control condition in an attempt to address these concerns. We examined the expression of IEGs over the course of spatial learning, finding that Zif268 expression was upregulated in a number of regions during early learning, and that c-Fos was upregulated during late learning. We investigated the role of IEGs in cellular consolidation at different time-points in the hours following learning, but we did not find support for multiple waves of IEG expression as previously reported in the literature. We also examined the course of systems consolidation by analysing IEG expression during recent and remote memory probe trials. The hippocampus was equivalently or increasingly activated over the course of time reflecting its continued involvement, while widespread increases in cortical activity were observed at remote time-points, consistent with systems consolidation theories. In addition, we showed that IEG expression was associated with error correction during learning and with superior performance during retention.