Influence of Path Integration Versus Environmental Orientation on Place Cell Remapping Between Visually Identical Environments

1 Department of Computer Science, Carnegie Mellon University, Pittsburgh, Pennsylvania; and 2 Division of Neural Systems, Memory, and Aging, University of Arizona, Tucson, Arizona Submitted 7 February 2005; accepted in final form 4 June 2005 To assess the effects of interactions between angular path integration and visual landmarks on the firing of hippocampal neurons, we recorded from CA1 pyramidal cells as rats foraged in two identical boxes with polarizing internal cues. In the same-orientation condition, following an earlier experiment by Skaggs and McNaughton, the boxes were oriented identically and connected by a corridor. In the opposite-orientation condition, the boxes were abutted by rotating them 90° in opposite directions, so that their orientations differed by 180°. After 16–23 days of pretraining on the same-orientation condition, three rats experienced both conditions in counterbalanced order on each of two consecutive days. On the third day they ran two opposite-orientation trials. Although Skaggs and McNaughton observed stable partial "remapping" of place fields, none of the fields in this experiment remapped in the same-orientation condition. In the opposite-orientation condition, place fields in the first box were isomorphic with those in the same-orientation condition, whereas in the second box the rats eventually exhibited completely different fields. The rats differed as to the trial in which this first occurred. Once the second box exhibited different fields, it continued to do so in all subsequent opposite-orientation trials, yet fields remained the same in subsequent same-orientation trials. The results demonstrate that when animals move actively between environments, and are thus potentially able to maintain their inertial angular orientation, discordance between environmental orientation and the rat's idiothetic direction sense can profoundly affect the hippocampal map—either immediately, or as a result of cumulative experience. Address for reprint requests and other correspondence: D. S. Touretzky, Computer Science Department, Carnegie Mellon University, Pittsburgh, PA 15213-3891 (E-mail: dst{at}cs.cmu.edu )