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Hippocampal cellular and network activity in freely moving echolocating bats

Abstract

The hippocampus is crucial for episodic and spatial memory. In freely moving rodents, hippocampal pyramidal neurons show spatially selective firing when the animal passes through a neuron's 'place-field', and theta-band oscillation is continuously present during locomotion. Here we report the first hippocampal recordings from echolocating bats, mammals phylogenetically distant from rodents, which showed place cells very similar to those of rodents. High-frequency 'ripple' oscillations were also rodent-like. Theta oscillation, however, differed from rodents in two important ways: (i) theta occurred when bats explored the environment without locomoting, using distal sensing through echolocation, and (ii) theta was not continuous, but occurred in short intermittent bouts. The intermittence of theta suggests that models of hippocampal function that rely on continuous theta may not apply to bats. Our data support the hypothesis that theta oscillation in the mammalian hippocampus is involved in sequence learning and hence, theta power should increase with sensory-input rate—which explains why theta power correlates with running speed in rodents and with echolocation call rate in bats.

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Figure 1: Experimental methods.
Figure 2: Place cells in bat hippocampal area CA1.
Figure 3: High-frequency ripple oscillations in bat hippocampus.
Figure 4: Behavior-dependent theta oscillation in the hippocampus of echolocating bats.
Figure 5: Properties of theta oscillation in bat hippocampus.
Figure 6: Theta phase modulation of pyramidal cell firing.

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Acknowledgements

We thank K.D. Harris, M. Lengyel, A. Sirota, J. Siegel, S. Cowan, M. Aytekin, K. Ghose and J. Fritz for critically reading the manuscript, G. Sutherland and B. McNaughton for invaluable technical advice during N.U.'s visit to the Arizona Research Laboratories, J. Lisman, N. Kopell, A.D. Redish, W. Hodos, G. Wilkinson, K. Macleod, S. Sinha, C. Stengel, R. Harlan, T. Barnes and A. Graybiel for helpful discussions and technical advice, B. Falk for help with experiments, E. Covey for a preprint of the bat brain atlas, E. Sanovich for histology and C. Carr for use of the Neurolucida system. This research was supported by US National Institutes of Health grant R01 MH56366 to C.F.M. and by the Center for Neuroscience at the University of Maryland.

Author information

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N.U. designed the study, conducted the experiments, analyzed the data and wrote the manuscript. C.F.M. supervised the project.

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Correspondence to Nachum Ulanovsky.

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The authors declare no competing financial interests.

Supplementary information

Supplementary Fig. 1

Spatial maps (spatial distributions) of the two behavioral modes. (PDF 36 kb)

Supplementary Fig. 2

Histograms of theta-to-delta ratio. (PDF 24 kb)

Supplementary Fig. 3

Depth profile of the percentage of time occupied by theta bouts. (PDF 14 kb)

Supplementary Fig. 4

Average firing rates of individual recorded cells. (PDF 16 kb)

Supplementary Discussion (PDF 21 kb)

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Ulanovsky, N., Moss, C. Hippocampal cellular and network activity in freely moving echolocating bats. Nat Neurosci 10, 224–233 (2007). https://doi.org/10.1038/nn1829

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