Nonoscillatory Phase Coding and Synchronization in the Bat Hippocampal Formation

Hippocampal theta oscillations were proposed to be important for multiple functions, including memory and temporal coding of position. However, previous findings from bats have questioned these proposals by reporting absence of theta rhythmicity in bat hippocampal formation. Does this mean that temporal coding is unique to rodent hippocampus and does not generalize to other species? Here, we report that, surprisingly, bat hippocampal neurons do exhibit temporal coding similar to rodents, albeit without any continuous oscillations at the 1–20 Hz range. Bat neurons exhibited very strong locking to the non-rhythmic fluctuations of the field potential, such that neurons were synchronized together despite the absence of oscillations. Further, some neurons exhibited “phase precession” and phase coding of the bat's position—with spike phases shifting earlier as the animal moved through the place field. This demonstrates an unexpected type of neural coding in the mammalian brain—nonoscillatory phase coding—and highlights the importance of synchrony and temporal coding for hippocampal function across species. Measurements in freely moving bats reveal that hippocampal neurons encode the animal's position through temporal coding but in the absence of the oscillations observed in rodents.