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New Research, Cognition and Behavior

Enhancement of motor cortical gamma oscillations and sniffing activity by medial forebrain bundle stimulation precedes locomotion

Airi Yoshimoto, Yusuke Shibata, Mikuru Kudara, Yuji Ikegaya and Nobuyoshi Matsumoto
eNeuro 14 June 2022, ENEURO.0521-21.2022; DOI: https://doi.org/10.1523/ENEURO.0521-21.2022
Airi Yoshimoto
1Graduate School of Pharmaceutical Sciences, The University of Tokyo, Tokyo 113-0033, Japan
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Yusuke Shibata
1Graduate School of Pharmaceutical Sciences, The University of Tokyo, Tokyo 113-0033, Japan
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Mikuru Kudara
1Graduate School of Pharmaceutical Sciences, The University of Tokyo, Tokyo 113-0033, Japan
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Yuji Ikegaya
1Graduate School of Pharmaceutical Sciences, The University of Tokyo, Tokyo 113-0033, Japan
2Institute for AI and Beyond, The University of Tokyo, Tokyo 113-0033, Japan
3Center for Information and Neural Networks, National Institute of Information and Communications Technology, Suita City, Osaka, 565-0871, Japan
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Nobuyoshi Matsumoto
1Graduate School of Pharmaceutical Sciences, The University of Tokyo, Tokyo 113-0033, Japan
2Institute for AI and Beyond, The University of Tokyo, Tokyo 113-0033, Japan
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Abstract

The medial forebrain bundle (MFB) is a white matter pathway that traverses through mesolimbic structures and includes dopaminergic neural fibers ascending from the ventral tegmental area. Since dopaminergic signals represent hedonic responses, electrical stimulation of the MFB in animals has been used as a neural reward for operant and spatial tasks. MFB stimulation strongly motivates animals to rapidly learn to perform a variety of behavioral tasks to obtain a reward. Although the MFB is known to connect various brain regions and MFB stimulation dynamically modulates animal behavior, how central and peripheral functions are affected by MFB stimulation per se is poorly understood. To address this question, we simultaneously recorded electrocorticograms (ECoGs) in the primary motor cortex (M1), primary somatosensory cortex, and olfactory bulb of behaving rats while electrically stimulating the MFB. We found that MFB stimulation increased the locomotor activity of rats. Spectral analysis confirmed that immediately after MFB stimulation, sniffing activity was facilitated and the power of gamma oscillations in the M1 was increased. After sniffing activity and motor cortical gamma oscillations were facilitated, animals started to move. These results provide insight into the importance of sniffing activity and cortical gamma oscillations for motor execution and learning facilitated by MFB stimulation.

Significance statement

Electrical stimulation of the medial forebrain bundle (MFB) in the brain reward system motivates animals to perform a variety of behavioral tasks. However, how MFB stimulation per se influences neural activity and relevant behavior remains incompletely understood. We recorded neural activity from the olfactory bulb, the primary motor cortex, and the primary somatosensory cortex of freely moving rats and monitored their behavior while regularly stimulating the MFB of the rats. We found that stimulation of the rat MFB facilitated sniffing activity and enhanced gamma oscillations only in the primary motor cortex, and subsequently induced locomotion. Our findings suggest the possible contribution of gamma oscillations to motor execution and learning facilitated by MFB stimulation.

  • gamma
  • locomotion
  • medial forebrain bundle
  • motor cortex
  • olfactory bulb
  • sniffing

Footnotes

  • The authors have no conflicts of interest to disclose with respect to this research.

  • This work was supported by JST ERATO (JPMJER1801), Institute for AI and Beyond of the University of Tokyo, and JSPS Grants-in-Aid for Scientific Research (18H05525 and 20K15926).

This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license, which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.

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Enhancement of motor cortical gamma oscillations and sniffing activity by medial forebrain bundle stimulation precedes locomotion
Airi Yoshimoto, Yusuke Shibata, Mikuru Kudara, Yuji Ikegaya, Nobuyoshi Matsumoto
eNeuro 14 June 2022, ENEURO.0521-21.2022; DOI: 10.1523/ENEURO.0521-21.2022

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Enhancement of motor cortical gamma oscillations and sniffing activity by medial forebrain bundle stimulation precedes locomotion
Airi Yoshimoto, Yusuke Shibata, Mikuru Kudara, Yuji Ikegaya, Nobuyoshi Matsumoto
eNeuro 14 June 2022, ENEURO.0521-21.2022; DOI: 10.1523/ENEURO.0521-21.2022
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Keywords

  • gamma
  • locomotion
  • medial forebrain bundle
  • Motor cortex
  • olfactory bulb
  • sniffing

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