Lesions of the mammillary body region alter hippocampal movement signals and theta frequency: implications for path integration models

Cells throughout the hippocampal formation are involved in processing spatial information. These same cells also show an influence of locomotor activity, and these movement signals are thought to be critical for the path integration abilities of these cells. Nuclei in the mammillary region provide ascending influences to the hippocampal formation and have been implicated in influencing both hippocampal spatial and theta signals. Here, we report the effects of mammillary lesions on movement-related signals in several hippocampal subregions. We find first, as predicted by earlier work, these lesions cause an approximately 1 Hz reduction in the frequency of theta modulation of cell firing. According to recent theoretical work, this might, in turn, be expected to influence the size of hippocampal place fields. Our data do not confirm this prediction for any of the hippocampal regions examined. Second, we report lesion effects on the relationship between firing rate and running speed for the hippocampal cells. These lesions caused a reduction in both the slope and intercept of rate-by-speed functions for cells in the hippocampus and postsubiculum. Surprisingly, cells in subiculum showed an opposite effect, so that the excitatory influence of locomotion was enhanced. Path integration theories predict that the speed at which path integration occurs is related to the strength of this movement signal. In remarkable accordance with this prediction, we report that the timing of the place cell signals is slowed following mammillary lesions for hippocampal and postsubicular cells, but, in contrast, is speeded up for subicular cells. In fact, the timing for place signals across lesion condition and brain region is predicted by a single linear function which relates timing to the strength of the running speed signal. Thus, these data provide remarkable support for some aspects of current path integration theory, while posing a challenge for other aspects of these same theories.