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Distinct VIP interneurons in the cingulate cortex encode anxiogenic and social stimuli

Connor Johnson, Lisa N. Kretsge, William W. Yen, Balaji Sriram, Jessica C. Jimenez, Tushare J. Jinadasa, Alexandra O’Connor, Ruichen Sky Liu, Thanh P. H. Nguyen, Eun Seon Cho, Erelle Fuchs, Eli D. Spevack, Berta Escude Velasco, Frances S. Hausmann, View ORCID ProfileAlberto Cruz-Martín
doi: https://doi.org/10.1101/2020.12.22.424056
Connor Johnson
1Department of Biology, Boston University, Boston, Massachusetts, United States of America
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Lisa N. Kretsge
2The Graduate Program for Neuroscience, Boston University, Boston, Massachusetts, United States of America
3Neurophotonics Center, Boston University, Boston, Massachusetts, United States of America
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William W. Yen
1Department of Biology, Boston University, Boston, Massachusetts, United States of America
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Balaji Sriram
4Research and Early Development, Biogen, Cambridge, Massachusetts, United States of America
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Jessica C. Jimenez
5Department of Neurology, University of California, San Francisco, San Francisco, California, USA
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Tushare J. Jinadasa
1Department of Biology, Boston University, Boston, Massachusetts, United States of America
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Alexandra O’Connor
6Department of Biomedical Engineering, Boston University, Boston, Massachusetts
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Ruichen Sky Liu
7MS in Statistical Practice, Boston University, Boston, Massachusetts, United States of America, United States of America
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Thanh P. H. Nguyen
6Department of Biomedical Engineering, Boston University, Boston, Massachusetts
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Eun Seon Cho
1Department of Biology, Boston University, Boston, Massachusetts, United States of America
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Erelle Fuchs
1Department of Biology, Boston University, Boston, Massachusetts, United States of America
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Eli D. Spevack
1Department of Biology, Boston University, Boston, Massachusetts, United States of America
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Berta Escude Velasco
1Department of Biology, Boston University, Boston, Massachusetts, United States of America
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Frances S. Hausmann
1Department of Biology, Boston University, Boston, Massachusetts, United States of America
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Alberto Cruz-Martín
1Department of Biology, Boston University, Boston, Massachusetts, United States of America
3Neurophotonics Center, Boston University, Boston, Massachusetts, United States of America
9Molecular Biology, Cell Biology and Biochemistry Program, Boston University, Boston, Massachusetts, United States of America
10Department Pharmacology and Experimental Therapeutics, Boston University, Boston, Massachusetts, United States of America
11Center for Systems Neuroscience, Boston University, Boston, Massachusetts, United States of America
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  • ORCID record for Alberto Cruz-Martín
  • For correspondence: acmartin@bu.edu
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ABSTRACT

A hallmark of higher-order cortical regions is their functional heterogeneity, but it is not well understood how these areas encode such diverse information. The anterior cingulate cortex (ACC), for example, is important in both emotional regulation and social cognition. Previous work shows activation of the ACC to anxiety-related and social stimuli, but it is unknown how subpopulations or microcircuits within the ACC simultaneously encode these distinct stimuli. One type of inhibitory interneuron, which is positive for vasoactive intestinal peptide (VIP), is known to alter the activity of many cells in local cortical microcircuits, but it is unknown whether the activity of VIP cells in the ACC (VIPACC) encodes anxiety-related or social information. Using in vivo calcium imaging and miniscopes in freely behaving mice to monitor VIPACC activity, we identified distinct, non-overlapping subpopulations of VIPACC that preferentially activated to either anxiogenic, anxiolytic, social, or non-social stimuli. We determined that stimulus-selective cells encode the animal’s behavioral states and VIP interneuron clusters may co-activate, improving this encoding. Finally, we used trans-synaptic tracing to show that VIPACC receive widespread inputs from regions implicated in emotional regulation and social cognition. These findings demonstrate not only that the ACC is not homogeneous in its function, but also that there is marked functional heterogeneity even within disinhibitory interneuron populations. This work contributes to our understanding of how the cortex encodes information across diverse contexts and provides insight into the complexity of neural processes involved in anxiety and social behavior.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • ↵# Co-first author

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Distinct VIP interneurons in the cingulate cortex encode anxiogenic and social stimuli
Connor Johnson, Lisa N. Kretsge, William W. Yen, Balaji Sriram, Jessica C. Jimenez, Tushare J. Jinadasa, Alexandra O’Connor, Ruichen Sky Liu, Thanh P. H. Nguyen, Eun Seon Cho, Erelle Fuchs, Eli D. Spevack, Berta Escude Velasco, Frances S. Hausmann, Alberto Cruz-Martín
bioRxiv 2020.12.22.424056; doi: https://doi.org/10.1101/2020.12.22.424056
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Distinct VIP interneurons in the cingulate cortex encode anxiogenic and social stimuli
Connor Johnson, Lisa N. Kretsge, William W. Yen, Balaji Sriram, Jessica C. Jimenez, Tushare J. Jinadasa, Alexandra O’Connor, Ruichen Sky Liu, Thanh P. H. Nguyen, Eun Seon Cho, Erelle Fuchs, Eli D. Spevack, Berta Escude Velasco, Frances S. Hausmann, Alberto Cruz-Martín
bioRxiv 2020.12.22.424056; doi: https://doi.org/10.1101/2020.12.22.424056

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