Integration of single-photon miniature fluorescence microscopy and electrophysiological recording methods for in vivo studying hippocampal neuronal activity

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Abstract

The miniature single-photon fluorescent microscope (miniscope) enables the visualization of calcium activity in vivo in freely moving laboratory animals, providing the capability to track cellular activity during the investigation of memory formation, learning, sleep, and social interactions. However, the use of calcium sensors for in vivo imaging is limited by their relatively slow (millisecond-scale) kinetics, which complicates the recording of high-frequency spike activity. The integration of methods from single-photon miniature fluorescent microscopy with electrophysiological recording, which possesses microsecond resolution, represents a potential solution to this issue. Such a combination of techniques allows for the simultaneous recording of optical and electrophysiological activity in a single animal in vivo. In this study, a flexible polyimide microelectrode was developed and integrated with the gradient lens of the miniscope. The in vivo tests conducted in this research confirmed that the microelectrode combined with the gradient lens facilitates simultaneous single-photon calcium imaging and local field potential recording in the hippocampus of an adult mouse.

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About the authors

А. I. Erofeev

Peter the Great St. Petersburg polytechnic university

Author for correspondence.
Email: alexandr.erofeew@gmail.com

Institute of Biomedical Systems and Biotechnology

Russian Federation, St. Petersburg

E. K. Vinokurov

Peter the Great St. Petersburg polytechnic university

Email: alexandr.erofeew@gmail.com

Institute of Biomedical Systems and Biotechnology

Russian Federation, St. Petersburg

I. E. Antifeev

Institute of Analytical Instrumentation

Email: alexandr.erofeew@gmail.com
Russian Federation, St. Petersburg

О. L. Vlasova

Peter the Great St. Petersburg polytechnic university

Email: alexandr.erofeew@gmail.com

Institute of Biomedical Systems and Biotechnology

Russian Federation, St. Petersburg

I. В. Bezprozvanny

Peter the Great St. Petersburg polytechnic university; University of Texas Southwestern Medical Center at Dallas

Email: alexandr.erofeew@gmail.com

Institute of Biomedical Systems and Biotechnology, Department of Physiology

Russian Federation, St. Petersburg; United States of America, Dallas, TX

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Supplementary files

Supplementary Files
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2. Fig. 1. 12-pin polyimide microelectrode designed for integration with a gradient lens of a miniscope: (a) – Schematic; (b) – Photograph of the microelectrode.

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3. Fig. 2. Transition cable for connecting the microelectrode to the wireless electrophysiological complex: (a) – Diagram; (b) – Photograph of the transition cable.

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4. Fig. 3. The cross-sectional view of the microelectrode and transition cable manufacturing process: (a) – Source material; (b) – Photoresist application; (c) – Photoresist exposure; (d) – Photoresist development; (e) – Copper galvanic deposition; (f) – Metalresist application; (g) – Photoresist removal; (h) – Copper etching; (i) – Metalresist removal; (j) – Polyimide capping layer application; (k) – Gold layer application.

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5. Fig. 4. 12-channel microelectrode. (a) – Forming of a 12-channel microelectrode around a GRIN lens with a diameter of 1.8 mm using a metal ring for subsequent heat treatment; (b) – GRIN-lens-microelectrode complex.

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6. Fig. 5. Schematic representation: (a) – Miniature fluorescence microscope (miniscope); (b) – Wireless electrophysiological module.

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7. Fig. 6. Schematic diagram of the connection of the system for simultaneous intravital calcium visualization and electrophysiological recording. A miniature fluorescence microscope (miniscope) is connected to the data acquisition system (DAQ) using a coaxial cable. In turn, DAQ is connected to a personal computer via a USB3.0 cable, which provides data transfer, power supply, and control of the miniscope. Power from the USB port of the personal computer is transmitted to the DAQ, and then via a coaxial cable goes to the miniscope. Thus, a voltage of 5 V is formed on the capacitor of the printed circuit board (PCB) of the miniscope and then fed to the wireless electrophysiological module. Data is transferred from the module to the personal computer via the Bluetooth Low Energy protocol.

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8. Fig. 7. Components of the system for simultaneous intravital calcium imaging and electrophysiological recording: (a) – External view of the entire system; (b) – Connection of the wireless electrophysiological module to the miniscope. The frame highlighted by the dotted line shows the connection of the power supply of the wireless electrophysiological module to the capacitor on the miniscope board.

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9. Fig. 8. Distribution of impedance of recording contacts of the developed 12-channel microelectrode. When measuring impedance, alternating sinusoidal signals with a voltage amplitude of 5 mV and frequencies from 0.1 to 1000 Hz were used. The dotted dark gray lines indicate the frequency range from 7 to 250 Hz. The solid red line indicates the impedance level of 2 MΩ.

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10. Fig. 9. Simultaneous Ca2+ imaging and local field potential recording in vivo: (a) – Photograph of the system for simultaneous intravital calcium imaging and electrophysiological recording in a laboratory mouse during the experiment; (b) – Image of fluorescent neurons (marked with white triangles) obtained using a single-photon miniature fluorescence microscope; (c) – Example of normalized spontaneous Ca2+ activity for 40 neurons in the CA1 region of the hippocampus identified by the MiniAn program; (d) – Example of an electrophysiological recording obtained using a wireless electrophysiological complex during calcium imaging.

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