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Hippocampal CA1 pyramidal cells form functionally distinct sublayers

Abstract

Hippocampal CA1 pyramidal neurons have frequently been regarded as a homogeneous cell population in biophysical, pharmacological and modeling studies. We found robust differences between pyramidal neurons residing in the deep and superficial CA1 sublayers in rats. Compared with their superficial peers, deep pyramidal cells fired at higher rates, burst more frequently, were more likely to have place fields and were more strongly modulated by slow oscillations of sleep. Both deep and superficial pyramidal cells fired preferentially at the trough of theta oscillations during maze exploration, whereas deep pyramidal cells shifted their preferred phase of firing to the peak of theta during rapid eye movement (REM) sleep. Furthermore, although the majority of REM theta phase-shifting cells fired at the ascending phase of gamma oscillations during waking, nonshifting cells preferred the trough. Thus, CA1 pyramidal cells in adjacent sublayers can address their targets jointly or differentially, depending on brain states.

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Figure 1: Spatial localization of neuronal somata in the CA1 pyramidal layer.
Figure 2: Preferred theta phase of spikes during REM sleep depends on the position of the soma in the CA1 pyramidal layer.
Figure 3: Phase-locking of CA1 pyramidal cell spikes by slow oscillations is location dependent.
Figure 4: Firing rates and bursting properties of CA1 pyramidal cells.
Figure 5: ISI-theta phase relationship of CA1 pyramidal cells.
Figure 6: Larger fraction of place cells in deep layer neurons and REM-shifting group.
Figure 7: Relationship between theta and gamma phase preferences of CA1 pyramidal cells.
Figure 8: The theta phase of spikes during REM is not affected by novel experience.

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Acknowledgements

We thank E. Cela, S. Fujisawa, P.M. Hiche, S. Ozen, A. Sirota, E. Stark and Y. Wang for comments on the manuscript, and D. Sullivan for valuable suggestions. This work was supported by the US National Institutes of Health (NS034994, MH54671), the National Science Foundation, the J.D. McDonnell Foundation, the Uehara Memorial Foundation, the Astellas Foundation for Research on Metabolic Disorders, the Japan Society of Promotion for Sciences, and the Robert Leet and Clara Guthrie Patterson Trust.

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K.M. and G.B. designed the experiments. K.M., K.D. and E.P. collected data. K.M. analyzed the data. K.M. and G.B. wrote the manuscript.

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Correspondence to György Buzsáki.

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Mizuseki, K., Diba, K., Pastalkova, E. et al. Hippocampal CA1 pyramidal cells form functionally distinct sublayers. Nat Neurosci 14, 1174–1181 (2011). https://doi.org/10.1038/nn.2894

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