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Cover ArticleResearch Articles, Systems/Circuits

Adolescent Parvalbumin Expression in the Left Orbitofrontal Cortex Shapes Sociability in Female Mice

Yi-Seon Jeon, Daun Jeong, Hanseul Kweon, Jae-Hyun Kim, Choong Yeon Kim, Youngbin Oh, Young-Ho Lee, Chan Hyuk Kim, Sang-Gyu Kim, Jae-Woong Jeong, Eunjoon Kim and Seung-Hee Lee
Journal of Neuroscience 1 March 2023, 43 (9) 1555-1571; DOI: https://doi.org/10.1523/JNEUROSCI.0918-22.2023
Yi-Seon Jeon
1Department of Biological Sciences, KAIST, Daejeon 34141, Korea
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Daun Jeong
1Department of Biological Sciences, KAIST, Daejeon 34141, Korea
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Hanseul Kweon
1Department of Biological Sciences, KAIST, Daejeon 34141, Korea
2Center for Synaptic Brain Dysfunctions, Institute for Basic Science, KAIST, Daejeon 34141, Korea
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Jae-Hyun Kim
1Department of Biological Sciences, KAIST, Daejeon 34141, Korea
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Choong Yeon Kim
3School of Electrical Engineering, KAIST, Daejeon 34141, Korea
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Youngbin Oh
1Department of Biological Sciences, KAIST, Daejeon 34141, Korea
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Young-Ho Lee
1Department of Biological Sciences, KAIST, Daejeon 34141, Korea
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Chan Hyuk Kim
1Department of Biological Sciences, KAIST, Daejeon 34141, Korea
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Sang-Gyu Kim
1Department of Biological Sciences, KAIST, Daejeon 34141, Korea
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Jae-Woong Jeong
3School of Electrical Engineering, KAIST, Daejeon 34141, Korea
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Eunjoon Kim
1Department of Biological Sciences, KAIST, Daejeon 34141, Korea
2Center for Synaptic Brain Dysfunctions, Institute for Basic Science, KAIST, Daejeon 34141, Korea
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Seung-Hee Lee
1Department of Biological Sciences, KAIST, Daejeon 34141, Korea
2Center for Synaptic Brain Dysfunctions, Institute for Basic Science, KAIST, Daejeon 34141, Korea
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Abstract

The adolescent social experience is essential for the maturation of the prefrontal cortex in mammalian species. However, it still needs to be determined which cortical circuits mature with such experience and how it shapes adult social behaviors in a sex-specific manner. Here, we examined social-approaching behaviors in male and female mice after postweaning social isolation (PWSI), which deprives social experience during adolescence. We found that the PWSI, particularly isolation during late adolescence, caused an abnormal increase in social approaches (hypersociability) only in female mice. We further found that the PWSI female mice showed reduced parvalbumin (PV) expression in the left orbitofrontal cortex (OFCL). When we measured neural activity in the female OFCL, a substantial number of neurons showed higher activity when mice sniffed other mice (social sniffing) than when they sniffed an object (object sniffing). Interestingly, the PWSI significantly reduced both the number of activated neurons and the activity level during social sniffing in female mice. Similarly, the CRISPR/Cas9-mediated knockdown of PV in the OFCL during late adolescence enhanced sociability and reduced the social sniffing-induced activity in adult female mice via decreased excitability of PV+ neurons and reduced synaptic inhibition in the OFCL. Moreover, optogenetic activation of excitatory neurons or optogenetic inhibition of PV+ neurons in the OFCL enhanced sociability in female mice. Our data demonstrate that the adolescent social experience is critical for the maturation of PV+ inhibitory circuits in the OFCL; this maturation shapes female social behavior via enhancing social representation in the OFCL.

SIGNIFICANCE STATEMENT Adolescent social isolation often changes adult social behaviors in mammals. Yet, we do not fully understand the sex-specific effects of social isolation and the brain areas and circuits that mediate such changes. Here, we found that adolescent social isolation causes three abnormal phenotypes in female but not male mice: hypersociability, decreased PV+ neurons in the left orbitofrontal cortex (OFCL), and decreased socially evoked activity in the OFCL. Moreover, parvalbumin (PV) deletion in the OFCL in vivo caused the same phenotypes in female mice by increasing excitation compared with inhibition within the OFCL. Our data suggest that adolescent social experience is required for PV maturation in the OFCL, which is critical for evoking OFCL activity that shapes social behaviors in female mice.

  • adolescent social isolation
  • female
  • inhibition
  • maturation
  • orbitofrontal cortex
  • parvalbumin

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The Journal of Neuroscience: 43 (9)
Journal of Neuroscience
Vol. 43, Issue 9
1 Mar 2023
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Adolescent Parvalbumin Expression in the Left Orbitofrontal Cortex Shapes Sociability in Female Mice
Yi-Seon Jeon, Daun Jeong, Hanseul Kweon, Jae-Hyun Kim, Choong Yeon Kim, Youngbin Oh, Young-Ho Lee, Chan Hyuk Kim, Sang-Gyu Kim, Jae-Woong Jeong, Eunjoon Kim, Seung-Hee Lee
Journal of Neuroscience 1 March 2023, 43 (9) 1555-1571; DOI: 10.1523/JNEUROSCI.0918-22.2023

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Adolescent Parvalbumin Expression in the Left Orbitofrontal Cortex Shapes Sociability in Female Mice
Yi-Seon Jeon, Daun Jeong, Hanseul Kweon, Jae-Hyun Kim, Choong Yeon Kim, Youngbin Oh, Young-Ho Lee, Chan Hyuk Kim, Sang-Gyu Kim, Jae-Woong Jeong, Eunjoon Kim, Seung-Hee Lee
Journal of Neuroscience 1 March 2023, 43 (9) 1555-1571; DOI: 10.1523/JNEUROSCI.0918-22.2023
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Keywords

  • adolescent social isolation
  • female
  • inhibition
  • maturation
  • orbitofrontal cortex
  • parvalbumin

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