Multiscale representation of very large environments in the hippocampus of flying bats.

Hippocampal place cells encode the animal's location. Place cells were traditionally studied in small environments, and nothing is known about large ethologically relevant spatial scales. We wirelessly recorded from hippocampal dorsal CA1 neurons of wild-born bats flying in a long tunnel (200 meters). The size of place fields ranged from 0.6 to 32 meters. Individual place cells exhibited multiple fields and a multiscale representation: Place fields of the same neuron differed up to 20-fold in size. This multiscale coding was observed from the first day of exposure to the environment, and also in laboratory-born bats that never experienced large environments. Theoretical decoding analysis showed that the multiscale code allows representation of very large environments with much higher precision than that of other codes. Together, by increasing the spatial scale, we discovered a neural code that is radically different from classical place codes.

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.