Theta-phase locking of single neurons during human spatial memory

bioRxiv (Cold Spring Harbor Laboratory)

Abstract

The precise timing of single-neuron activity in relation to local field potentials may support various cognitive functions. Extensive research in rodents, along with some evidence in humans, suggests that single-neuron activity at specific phases of theta oscillations plays a crucial role in memory processes. Our fundamental understanding of such theta-phase locking in humans and its dependency on basic electrophysiological properties of the local field potential is still limited, however. Here, using single-neuron recordings in epilepsy patients performing a spatial memory task, we thus aimed at improving our understanding of factors modulating theta-phase locking in the human brain. Combining a generalized-phase approach for frequency-adaptive theta-phase estimation with time-resolved spectral parameterization, our results show that theta-phase locking is a strong and prevalent phenomenon across human medial temporal lobe regions, both during spatial memory encoding and retrieval. Neuronal theta-phase locking increased during periods of elevated theta power, when clear theta oscillations were present, and when aperiodic activity exhibited steeper slopes. Theta-phase locking was similarly strong during successful and unsuccessful memory, and most neurons activated at similar theta phases between encoding and retrieval. Some neurons changed their preferred theta phases between encoding and retrieval, in line with the idea that different memory processes are separated within the theta cycle. Together, these results help disentangle how different properties of local field potentials and memory states influence theta-phase locking of human single neurons. This contributes to a better understanding of how interactions between single neurons and local field potentials may support human spatial memory.

Authors 6

1. Tim A Guth corresponding

   University of Freiburg · University Hospital Bonn · University Medical Center Freiburg

   Affiliation as printed

   Department of Epileptology, University Hospital Bonn, Bonn, Germany

   Epilepsy Center, Medical Center - University of Freiburg, Faculty of Medicine, University of Freiburg, Freiburg, Germany

2. Armin Brandt

   University of Freiburg · University Medical Center Freiburg

   Affiliation as printed

   Epilepsy Center, Medical Center - University of Freiburg, Faculty of Medicine, University of Freiburg, Freiburg, Germany

3. Peter Christoph Reinacher Aachen Fraunhofer Institute for Laser Technology (ILT)

   University of Freiburg · University Medical Center Freiburg · Fraunhofer Institute for Laser Technology

   Affiliation as printed

   Department of Stereotactic and Functional Neurosurgery, Medical Center - University of Freiburg, Faculty of Medicine, University of Freiburg, Freiburg, Germany

   Fraunhofer Institute for Laser Technology, Aachen, Germany

4. Andreas Schulze‐Bonhage

   University of Freiburg · University Medical Center Freiburg

   Affiliation as printed

   Epilepsy Center, Medical Center - University of Freiburg, Faculty of Medicine, University of Freiburg, Freiburg, Germany

5. Joshua Jacobs

   Columbia University Irving Medical Center · Columbia University

   Affiliation as printed

   Department of Biomedical Engineering, Columbia University, New York, NY, USA

   Department of Neurological Surgery, Columbia University Medical Center, New York, NY, USA

6. Lukas Kunz

   University Hospital Bonn

   Affiliation as printed

   Department of Epileptology, University Hospital Bonn, Bonn, Germany