Hippocampal Motifs

Dorsal Hippocampal neurons provide an allocentric map of space, characterized by three key properties. First, their firing is spatially selective, termed a rate code. Second, as animals traverse through place fields, neurons sustain elevated firing rates for long periods, however this has received little attention. Third the theta-phase of spikes within this sustained activity varies with animal's location, termed phase-precession or a temporal code. The precise relationship between these properties and the mechanisms governing them are not understood, although distal visual cues (DVC) are thought to be sufficient to reliably elicit them. Hence, we measured rat CA1 neurons' activity during random foraging in two-dimensional VR—where only DVC provide consistent allocentric location information— and compared it with their activity in real world (RW). Surprisingly, we found little spatial selectivity in VR. This is in sharp contrast to robust spatial selectivity commonly seen in one-dimensional RW and VR, or two-dimensional RW. Despite this, neurons in VR generated approximately two-second long phase precessing spike sequences, termed “hippocampal motifs”. Motifs, and “Motif-fields”, an aggregation of all motifs of a neuron, had qualitatively similar properties including theta-scale temporal coding in RW and VR, but the motifs were far less spatially localized in VR. These results suggest that intrinsic, network mechanisms generate temporally coded hippocampal motifs, which can be dissociated from their spatial selectivity. Further, DVC alone are insufficient to localize motifs spatially to generate a robust rate code.