Head direction cells in rats with hippocampal or overlying neocortical lesions: Evidence for impaired angular path integration

Rodents use two distinct navigation strategies that are based on environmen tal cues (landmark navigation) or internal cues (path integration). Head di rection (HD) cells are neurons that discharge when the animal points its he ad in a particular direction and are responsive to the same cues that suppo rt path integration and landmark navigation. Experiment 1 examined whether HD cells in rats with lesions to the hippocampus plus the overlying neocort ex or to just the overlying neocortex could maintain a stable preferred fir ing direction when the rats locomoted from a familiar to a novel environmen t, a process thought to require path integration. HD cells from both lesion groups were unable to maintain a similar preferred direction between envir onments, with cells from hippocampal rats showing larger shifts than cells from rats sustaining only cortical damage. When the rats first explored the novel environment, the preferred directions of the cells drifted for up to 4 min before establishing a consistent firing orientation. The preferred d irection was usually maintained during subsequent visits to the novel envir onment but not across longer time periods (days to weeks). Experiment 2 dem onstrated that a novel landmark cue was able to establish control over HD c ell preferred directions in rats from both lesion groups, showing that the impairment observed in experiment 1 cannot be attributed to an impairment i n establishing cue control. Experiment 3 showed that the preferred directio n drifted when HD cells in lesioned animals were recorded in the dark. It w as also shown that the anticipatory property of anterodorsal thalamic nucle us HD cells was still present in lesioned animals; thus, this property cann ot be attributed to an intact hippocampus. These findings suggest that the hippocampus and the overlying neocortex are involved in path integration me chanisms, which enable an animal to maintain an accurate representation of its directional heading when exploring a novel environment.