Hippocampal CA1 pyramidal cells form functionally distinct sublayers

Hippocampal CA1 pyramidal neurons have frequently been regarded as a homogeneous cell population in biophysical, pharmacological and modeling studies. Here we report robust differences between pyramidal neurons residing in the deep and superficial CA1 sublayers in the rat. Compared to 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, yet during Rapid eye movement (REM) sleep, deep pyramidal cells shifted their preferred phase of firing to the peak of theta. Furthermore, whereas in waking, the majority of REM theta phase-shifting cells fired at the ascending phase of gamma oscillations, non-shifting cells preferred the trough. Thus, CA1 pyramidal cells in adjacent sublayers can address their targets jointly or differentially, depending on brain states.