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Research ArticleResearch Article: New Research, Development

Circuit-Specific Dendritic Development in the Piriform Cortex

Laura Moreno-Velasquez, Hung Lo, Stephen Lenzi, Malte Kaehne, Jörg Breustedt, Dietmar Schmitz, Sten Rüdiger and Friedrich W. Johenning
eNeuro 26 May 2020, 7 (3) ENEURO.0083-20.2020; DOI: https://doi.org/10.1523/ENEURO.0083-20.2020
Laura Moreno-Velasquez
1Neuroscience Research Center, Charité-Universitätsmedizin Berlin, Corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, 10117 Berlin, Germany
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Hung Lo
1Neuroscience Research Center, Charité-Universitätsmedizin Berlin, Corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, 10117 Berlin, Germany
5Einstein Center for Neurosciences Berlin, 10117 Berlin, Germany
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Stephen Lenzi
3Sainsbury Wellcome Centre, University College London, London W1T 4JG, UK
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Malte Kaehne
2Institute of Physics, Humboldt Universität Berlin, 12489 Berlin, Germany
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Jörg Breustedt
1Neuroscience Research Center, Charité-Universitätsmedizin Berlin, Corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, 10117 Berlin, Germany
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Dietmar Schmitz
1Neuroscience Research Center, Charité-Universitätsmedizin Berlin, Corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, 10117 Berlin, Germany
4NeuroCure Cluster of Excellence, 10117 Berlin, Germany
5Einstein Center for Neurosciences Berlin, 10117 Berlin, Germany
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Sten Rüdiger
3Sainsbury Wellcome Centre, University College London, London W1T 4JG, UK
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Friedrich W. Johenning
1Neuroscience Research Center, Charité-Universitätsmedizin Berlin, Corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, 10117 Berlin, Germany
5Einstein Center for Neurosciences Berlin, 10117 Berlin, Germany
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Abstract

Dendritic geometry is largely determined during postnatal development and has a substantial impact on neural function. In sensory processing, postnatal development of the dendritic tree is affected by two dominant circuit motifs, ascending sensory feedforward inputs and descending and local recurrent connections. In the three-layered anterior piriform cortex (aPCx), neurons in the sublayers 2a and 2b display vertical segregation of these two circuit motifs. Here, we combined electrophysiology, detailed morphometry, and Ca2+ imaging in acute mouse brain slices and modeling to study circuit-specific aspects of dendritic development. We observed that determination of branching complexity, dendritic length increases, and pruning occurred in distinct developmental phases. Layer 2a and layer 2b neurons displayed developmental phase-specific differences between their apical and basal dendritic trees related to differences in circuit incorporation. We further identified functional candidate mechanisms for circuit-specific differences in postnatal dendritic growth in sublayers 2a and 2b at the mesoscale and microscale levels. Already in the first postnatal week, functional connectivity of layer 2a and layer 2b neurons during early spontaneous network activity scales with differences in basal dendritic growth. During the early critical period of sensory plasticity in the piriform cortex, our data are consistent with a model that proposes a role for dendritic NMDA-spikes in selecting branches for survival during developmental pruning in apical dendrites. The different stages of the morphologic and functional developmental pattern differences between layer 2a and layer 2b neurons demonstrate the complex interplay between dendritic development and circuit specificity.

  • dendritic development
  • NMDA-spike
  • piriform cortex

Footnotes

  • The authors declare no competing financial interests.

  • This work was supported by the Deutsche Forschungsgemeinschaft (German Research Foundation) Grants SFB 1315 Project-ID 327654276, Exc 2049, and SPP 1665 (to D.S.); JO 1079/3-1 (to F.W.J.); and RU1660/5-1 (to S.R.); the Bundesministerium für Bildung und Forschung (Federal Ministry of Education and Research) Grant 01GQ1420B (to D.S.); and the ERC BrainPlay-Synergy Grant (D.S.).

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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Circuit-Specific Dendritic Development in the Piriform Cortex
Laura Moreno-Velasquez, Hung Lo, Stephen Lenzi, Malte Kaehne, Jörg Breustedt, Dietmar Schmitz, Sten Rüdiger, Friedrich W. Johenning
eNeuro 26 May 2020, 7 (3) ENEURO.0083-20.2020; DOI: 10.1523/ENEURO.0083-20.2020

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Circuit-Specific Dendritic Development in the Piriform Cortex
Laura Moreno-Velasquez, Hung Lo, Stephen Lenzi, Malte Kaehne, Jörg Breustedt, Dietmar Schmitz, Sten Rüdiger, Friedrich W. Johenning
eNeuro 26 May 2020, 7 (3) ENEURO.0083-20.2020; DOI: 10.1523/ENEURO.0083-20.2020
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Keywords

  • dendritic development
  • NMDA-spike
  • piriform cortex

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