E-Cannula reveals anatomical diversity in sharp-wave ripples as a driver for the recruitment of distinct hippocampal assemblies
Xin Liu,
Satoshi Terada,
Mehrdad Ramezani,
Jeong-Hoon Kim,
Yichen Lu,
Andres Grosmark,
Attila Losonczy,
Duygu Kuzum
Affiliations
Xin Liu
Department of Electrical and Computer Engineering, University of California, San Diego, La Jolla, CA, USA
Satoshi Terada
Department of Neuroscience, Columbia University, New York, NY, USA; Mortimer B. Zuckerman Mind Brain Behavior Institute, Columbia University, New York, NY, USA
Mehrdad Ramezani
Department of Electrical and Computer Engineering, University of California, San Diego, La Jolla, CA, USA
Jeong-Hoon Kim
Department of Electrical and Computer Engineering, University of California, San Diego, La Jolla, CA, USA
Yichen Lu
Department of Electrical and Computer Engineering, University of California, San Diego, La Jolla, CA, USA
Andres Grosmark
Department of Neuroscience, Columbia University, New York, NY, USA; Mortimer B. Zuckerman Mind Brain Behavior Institute, Columbia University, New York, NY, USA; The Kavli Institute for Brain Science, Columbia University, New York, NY, USA
Attila Losonczy
Department of Neuroscience, Columbia University, New York, NY, USA; Mortimer B. Zuckerman Mind Brain Behavior Institute, Columbia University, New York, NY, USA; The Kavli Institute for Brain Science, Columbia University, New York, NY, USA; Corresponding author
Duygu Kuzum
Department of Electrical and Computer Engineering, University of California, San Diego, La Jolla, CA, USA; Halıcıoğlu Data Science Institute, University of California, San Diego, La Jolla, CA, USA; Corresponding author
Summary: The hippocampus plays a critical role in spatial navigation and episodic memory. However, research on in vivo hippocampal activity dynamics mostly relies on single modalities, such as electrical recordings or optical imaging, with respectively limited spatial and temporal resolution. Here, we develop the E-Cannula, integrating fully transparent graphene microelectrodes with imaging cannula, which enables simultaneous electrical recording and two-photon calcium imaging from the exact same neural populations across an anatomically extended region of the mouse hippocampal CA1 stably across several days. The large-scale multimodal recordings show that sharp wave ripples (SWRs) exhibit spatiotemporal wave patterns along multiple axes in two-dimensional (2D) space with different spatial extents and temporal propagation modes. Notably, distinct SWR wave patterns are associated with the selective recruitment of orthogonal CA1 cell assemblies. These results demonstrate the utility of the E-Cannula as a versatile neurotechnology with the potential for future integration with other optical components.
