Distinct and Dynamic ON and OFF Neural Ensembles in the Prefrontal Cortex Code Social Exploration

Bo Liang; Lifeng Zhang; Giovanni Barbera; Wenting Fang; Jing Zhang; Xiaochun Chen; Rong Chen; Yun Li; Da-Ting Lin

doi:10.1016/j.neuron.2018.08.043

Distinct and Dynamic ON and OFF Neural Ensembles in the Prefrontal Cortex Code Social Exploration

Neuron. 2018 Nov 7;100(3):700-714.e9. doi: 10.1016/j.neuron.2018.08.043. Epub 2018 Sep 27.

Authors

Bo Liang¹, Lifeng Zhang¹, Giovanni Barbera¹, Wenting Fang², Jing Zhang³, Xiaochun Chen⁴, Rong Chen⁵, Yun Li⁶, Da-Ting Lin⁷

Affiliations

¹ Intramural Research Program, National Institute on Drug Abuse, NIH, 333 Cassell Drive, Baltimore, MD 21224, USA.
² Intramural Research Program, National Institute on Drug Abuse, NIH, 333 Cassell Drive, Baltimore, MD 21224, USA; Department of Neurology, Union Hospital, and Fujian Key Laboratory of Molecular Neurology, Fujian Medical University, Fuzhou, Fujian 350001, China.
³ Intramural Research Program, National Institute on Drug Abuse, NIH, 333 Cassell Drive, Baltimore, MD 21224, USA; Fujian Institute of Geriatrics, Union Hospital, and Fujian Key Laboratory of Molecular Neurology, Fujian Medical University, Fuzhou, Fujian 350001, China.
⁴ Department of Neurology, Union Hospital, and Fujian Key Laboratory of Molecular Neurology, Fujian Medical University, Fuzhou, Fujian 350001, China.
⁵ Department of Diagnostic Radiology and Nuclear Medicine, University of Maryland School of Medicine, 100 N. Greene Street, Baltimore, MD 21205, USA.
⁶ Intramural Research Program, National Institute on Drug Abuse, NIH, 333 Cassell Drive, Baltimore, MD 21224, USA; Department of Zoology and Physiology, University of Wyoming, 1000 E. University Avenue, Laramie, WY 82071, USA. Electronic address: yli30@uwyo.edu.
⁷ Intramural Research Program, National Institute on Drug Abuse, NIH, 333 Cassell Drive, Baltimore, MD 21224, USA; The Solomon H. Snyder Department of Neuroscience, Johns Hopkins University School of Medicine, 725 N. Wolfe Street, Baltimore, MD 21205, USA. Electronic address: da-ting.lin@nih.gov.

Abstract

The medial prefrontal cortex (mPFC) is important for social behavior, but the mechanisms by which mPFC neurons code real-time social exploration remain largely unknown. Here we utilized miniScopes to record calcium activities from hundreds of excitatory neurons in the mPFC while mice freely explored restrained social targets in the absence or presence of the psychedelic drug phencyclidine (PCP). We identified distinct and dynamic ON and OFF neural ensembles that displayed opposing activities to code real-time behavioral information. We further illustrated that ON and OFF ensembles tuned to social exploration carried information of salience and novelty for social targets. Finally, we showed that dysfunctions in these ensembles were associated with abnormal social exploration elicited by PCP. Our findings underscore the importance of mPFC ON and OFF neural ensembles for proper exploratory behavior, including social exploration, and pave the way for future studies elucidating neural circuit dysfunctions in psychiatric disorders.

Keywords: decoding; freely behaving; in vivo calcium imaging; miniature fluorescence microscope; mouse model; preference for social novelty; schizophrenia; sociability.

Publication types

Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't

MeSH terms

Action Potentials / drug effects
Action Potentials / physiology*
Animals
Excitatory Amino Acid Antagonists / pharmacology
Exploratory Behavior / drug effects
Exploratory Behavior / physiology*
Mice
Mice, Inbred C57BL
Nerve Net / chemistry
Nerve Net / drug effects
Nerve Net / physiology*
Optogenetics / methods
Phencyclidine / pharmacology
Prefrontal Cortex / chemistry
Prefrontal Cortex / drug effects
Prefrontal Cortex / physiology*
Social Behavior*

Substances

Excitatory Amino Acid Antagonists
Phencyclidine

Abstract

Publication types

MeSH terms

Substances

Grants and funding