Head Direction Cell Representations Maintain Internal Coherence during Conflicting Proximal and Distal Cue Rotations: Comparison with Hippocampal Place Cells

Place cells of the hippocampal formation encode a spatial representation of the environment, and the orientation of this representation is apparently governed by the head direction cell system. The representation of a well explored environment by CA1 place cells can be split when there is conflicting information from salient proximal and distal cues, because some place fields rotate to follow the distal cues, whereas others rotate to follow the proximal cues (Knierim, 2002a). In contrast, the CA3 representation is more coherent than CA1, because the place fields in CA3 tend to rotate in the same direction (Lee et al., 2004). The present study tests whether the head direction cell network produces a split representation or remains coherent under these conditions by simultaneously recording both CA1 place cells and head direction cells from the thalamus. In agreement with previous studies, split representations of the environment were observed in ensembles of CA1 place cells in approximately 75% of the mismatch sessions, in which some fields followed the counterclockwise rotation of proximal cues and other fields followed the clockwise rotation of distal cues. However, of 225 recording sessions, there was not a single instance of the head direction cell ensembles revealing a split representation of head direction. Instead, in most of the mismatch sessions, the head direction cell tuning curves rotated as an ensemble clockwise (94%) and in a few sessions rotated counterclockwise (6%). The findings support the notion that the head direction cells may be part of an attractor network bound more strongly to distal landmarks than proximal landmarks, even under conditions in which the CA1 place representation loses its coherence.