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Determinants of functional synaptic connectivity among amygdala-projecting prefrontal cortical neurons in male mice

Author

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  • Yoav Printz

    (Weizmann Institute of Science)

  • Pritish Patil

    (Weizmann Institute of Science)

  • Mathias Mahn

    (Weizmann Institute of Science)

  • Asaf Benjamin

    (Weizmann Institute of Science)

  • Anna Litvin

    (Weizmann Institute of Science)

  • Rivka Levy

    (Weizmann Institute of Science)

  • Max Bringmann

    (Weizmann Institute of Science)

  • Ofer Yizhar

    (Weizmann Institute of Science)

Abstract

The medial prefrontal cortex (mPFC) mediates a variety of complex cognitive functions via its vast and diverse connections with cortical and subcortical structures. Understanding the patterns of synaptic connectivity that comprise the mPFC local network is crucial for deciphering how this circuit processes information and relays it to downstream structures. To elucidate the synaptic organization of the mPFC, we developed a high-throughput optogenetic method for mapping large-scale functional synaptic connectivity in acute brain slices. We show that in male mice, mPFC neurons that project to the basolateral amygdala (BLA) display unique spatial patterns of local-circuit synaptic connectivity, which distinguish them from the general mPFC cell population. When considering synaptic connections between pairs of mPFC neurons, the intrinsic properties of the postsynaptic cell and the anatomical positions of both cells jointly account for ~7.5% of the variation in the probability of connection. Moreover, anatomical distance and laminar position explain most of this fraction in variation. Our findings reveal the factors determining connectivity in the mPFC and delineate the architecture of synaptic connections in the BLA-projecting subnetwork.

Suggested Citation

  • Yoav Printz & Pritish Patil & Mathias Mahn & Asaf Benjamin & Anna Litvin & Rivka Levy & Max Bringmann & Ofer Yizhar, 2023. "Determinants of functional synaptic connectivity among amygdala-projecting prefrontal cortical neurons in male mice," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-37318-x
    DOI: 10.1038/s41467-023-37318-x
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    as
    1. Yong-Chun Yu & Ronald S. Bultje & Xiaoqun Wang & Song-Hai Shi, 2009. "Specific synapses develop preferentially among sister excitatory neurons in the neocortex," Nature, Nature, vol. 458(7237), pages 501-504, March.
    2. Lee Cossell & Maria Florencia Iacaruso & Dylan R. Muir & Rachael Houlton & Elie N. Sader & Ho Ko & Sonja B. Hofer & Thomas D. Mrsic-Flogel, 2015. "Functional organization of excitatory synaptic strength in primary visual cortex," Nature, Nature, vol. 518(7539), pages 399-403, February.
    3. Yong-Chun Yu & Shuijin He & She Chen & Yinghui Fu & Keith N. Brown & Xing-Hua Yao & Jian Ma & Kate P. Gao & Gina E. Sosinsky & Kun Huang & Song-Hai Shi, 2012. "Preferential electrical coupling regulates neocortical lineage-dependent microcircuit assembly," Nature, Nature, vol. 486(7401), pages 113-117, June.
    4. James M. Otis & Vijay M. K. Namboodiri & Ana M. Matan & Elisa S. Voets & Emily P. Mohorn & Oksana Kosyk & Jenna A. McHenry & J. Elliott Robinson & Shanna L. Resendez & Mark A. Rossi & Garret D. Stuber, 2017. "Prefrontal cortex output circuits guide reward seeking through divergent cue encoding," Nature, Nature, vol. 543(7643), pages 103-107, March.
    5. Xin-Jun Zhang & Zhizhong Li & Zhi Han & Khadeejah T. Sultan & Kun Huang & Song-Hai Shi, 2017. "Precise inhibitory microcircuit assembly of developmentally related neocortical interneurons in clusters," Nature Communications, Nature, vol. 8(1), pages 1-16, December.
    6. Yumiko Yoshimura & Jami L. M. Dantzker & Edward M. Callaway, 2005. "Excitatory cortical neurons form fine-scale functional networks," Nature, Nature, vol. 433(7028), pages 868-873, February.
    7. Timothy Spellman & Mattia Rigotti & Susanne E. Ahmari & Stefano Fusi & Joseph A. Gogos & Joshua A. Gordon, 2015. "Hippocampal–prefrontal input supports spatial encoding in working memory," Nature, Nature, vol. 522(7556), pages 309-314, June.
    8. Houri Hintiryan & Ian Bowman & David L. Johnson & Laura Korobkova & Muye Zhu & Neda Khanjani & Lin Gou & Lei Gao & Seita Yamashita & Michael S. Bienkowski & Luis Garcia & Nicholas N. Foster & Nora L. , 2021. "Connectivity characterization of the mouse basolateral amygdalar complex," Nature Communications, Nature, vol. 12(1), pages 1-25, December.
    9. Cyril Herry & Stephane Ciocchi & Verena Senn & Lynda Demmou & Christian Müller & Andreas Lüthi, 2008. "Switching on and off fear by distinct neuronal circuits," Nature, Nature, vol. 454(7204), pages 600-606, July.
    10. Wei-Chung Allen Lee & Vincent Bonin & Michael Reed & Brett J. Graham & Greg Hood & Katie Glattfelder & R. Clay Reid, 2016. "Anatomy and function of an excitatory network in the visual cortex," Nature, Nature, vol. 532(7599), pages 370-374, April.
    11. Jean-Sébastien Jouhanneau & Jens Kremkow & James F. A. Poulet, 2018. "Single synaptic inputs drive high-precision action potentials in parvalbumin expressing GABA-ergic cortical neurons in vivo," Nature Communications, Nature, vol. 9(1), pages 1-11, December.
    12. Leopoldo Petreanu & Tianyi Mao & Scott M. Sternson & Karel Svoboda, 2009. "The subcellular organization of neocortical excitatory connections," Nature, Nature, vol. 457(7233), pages 1142-1145, February.
    13. Julien Courtin & Fabrice Chaudun & Robert R. Rozeske & Nikolaos Karalis & Cecilia Gonzalez-Campo & Hélène Wurtz & Azzedine Abdi & Jerome Baufreton & Thomas C. M. Bienvenu & Cyril Herry, 2014. "Prefrontal parvalbumin interneurons shape neuronal activity to drive fear expression," Nature, Nature, vol. 505(7481), pages 92-96, January.
    14. Fabricio H. Do-Monte & Kelvin Quiñones-Laracuente & Gregory J. Quirk, 2015. "A temporal shift in the circuits mediating retrieval of fear memory," Nature, Nature, vol. 519(7544), pages 460-463, March.
    15. Kenneth D. Harris & Thomas D. Mrsic-Flogel, 2013. "Cortical connectivity and sensory coding," Nature, Nature, vol. 503(7474), pages 51-58, November.
    16. Ho Ko & Lee Cossell & Chiara Baragli & Jan Antolik & Claudia Clopath & Sonja B. Hofer & Thomas D. Mrsic-Flogel, 2013. "The emergence of functional microcircuits in visual cortex," Nature, Nature, vol. 496(7443), pages 96-100, April.
    17. Cyril Dejean & Julien Courtin & Nikolaos Karalis & Fabrice Chaudun & Hélène Wurtz & Thomas C. M. Bienvenu & Cyril Herry, 2016. "Prefrontal neuronal assemblies temporally control fear behaviour," Nature, Nature, vol. 535(7612), pages 420-424, July.
    18. Solange P. Brown & Shaul Hestrin, 2009. "Intracortical circuits of pyramidal neurons reflect their long-range axonal targets," Nature, Nature, vol. 457(7233), pages 1133-1136, February.
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