Sparse, spatially selective activity in neuronal populations is believed to be reflective of an “indexing” system that stores the patterns of activity corresponding to memories. Such activity has been observed in neurons in the hippocampus (HPC) and across many regions of the neocortex, particularly in the superficial layers. Generally, this kind of place-cell like activity in the neocortex (NC) seems to be dependent on the hippocampus, as hippocampal lesions greatly reduce the spatial selectivity of superficial neocortical neurons. Questions about these spatially selective neocortical neurons remain outstanding though, including the extent to their distributions across layers and how their activity is modulated by stimuli in different sensory domains. To better understand what shapes spatial selectivity in neocortical neurons, neuronal ensembles in the secondary motor (M2) and retrosplenial (RSC) cortices of head-fixed mice with hippocampal or sham lesions were recorded using linear electrode arrays. Mice ran through a visual virtual reality environment for reward during the recording. Behavioral results showed that sham controls slowed down before upcoming rewards, indicating they likely remembered the reward locations. Hippocampus lesioned mice did not. This is consistent with many previous accounts of deficits in spatial memory following hippocampal lesion. Physiological results showed that in M2 neurons, in both sham and lesioned mice, there was a significant increase in activity around reward areas. In sham mice, there was greater M2 activity ramping up before the reward, whereas in lesioned mice, the increase in M2 activity occurred after reward administration. While many neurons responded around the reward sites in both a new and old VR environment, their firing rates at those rewards often changed. Firing rate differences between VR environments were observed, which may be analogous to the ‘rate remapping’ seen in the hippocampus when a rodent’s spatial environment changes without a corresponding change in its path integration system. Neurons in lesioned mice showed greater firing rate differences, indicating that this phenomenon may be driven more by changing visual inputs when the hippocampus is lesioned. This study is the first to examine neocortical responses to different contexts (real or virtual) in hippocampal lesioned animals.