Phase locking of hippocampal CA3 neurons to distal CA1 theta oscillations selectively predicts memory performance
Shih-Pi Ku,
Erika Atucha,
Nico Alavi,
Halla Mulla-Osman,
Rukhshona Kayumova,
Motoharu Yoshida,
Jozsef Csicsvari,
Magdalena M. Sauvage
Affiliations
Shih-Pi Ku
Leibniz Institute for Neurobiology, Functional Architecture of Memory Department, Magdeburg, Germany; Corresponding author
Erika Atucha
Leibniz Institute for Neurobiology, Functional Architecture of Memory Department, Magdeburg, Germany
Nico Alavi
Leibniz Institute for Neurobiology, Functional Architecture of Memory Department, Magdeburg, Germany
Halla Mulla-Osman
Leibniz Institute for Neurobiology, Functional Architecture of Memory Department, Magdeburg, Germany
Rukhshona Kayumova
Leibniz Institute for Neurobiology, Functional Architecture of Memory Department, Magdeburg, Germany
Motoharu Yoshida
Leibniz Institute for Neurobiology, Functional Architecture of Memory Department, Magdeburg, Germany; German Center for Neurodegenerative Diseases (DZNE), Magdeburg, Germany
Jozsef Csicsvari
Institute of Science and Technology (IST), Klosterneuburg, Austria
Magdalena M. Sauvage
Leibniz Institute for Neurobiology, Functional Architecture of Memory Department, Magdeburg, Germany; Otto von Guericke University, Medical Faculty, Functional Neuroplasticity Department, Magdeburg, Germany; Center for Behavioral Brain Sciences (CBBS), Magdeburg, Germany; Corresponding author
Summary: How the coordination of neuronal spiking and brain rhythms between hippocampal subregions supports memory function remains elusive. We studied the interregional coordination of CA3 neuronal spiking with CA1 theta oscillations by recording electrophysiological signals along the proximodistal axis of the hippocampus in rats that were performing a high-memory-demand recognition memory task adapted from humans. We found that CA3 population spiking occurs preferentially at the peak of distal CA1 theta oscillations when memory was tested but only when previously encountered stimuli were presented. In addition, decoding analyses revealed that only population cell firing of proximal CA3 together with that of distal CA1 can predict performance at test in the present non-spatial task. Overall, our work demonstrates an important role for the synchronization of CA3 neuronal activity with CA1 theta oscillations during memory testing.