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Research Articles, Systems/Circuits

Neuropilin 2/Plexin-A3 Receptors Regulate the Functional Connectivity and the Excitability in the Layers 4 and 5 of the Cerebral Cortex

Hussain Y. Khdour, Krishnakanth Kondabolu, Alina Khadka, Maxime Assous, James M. Tepper, Tracy S. Tran and Pierre-Olivier Polack
Journal of Neuroscience 15 June 2022, 42 (24) 4828-4840; DOI: https://doi.org/10.1523/JNEUROSCI.1965-21.2022
Hussain Y. Khdour
1Center for Molecular and Behavioral Neuroscience, Rutgers University–Newark, Newark, New Jersey 07102
3Behavioral and Neural Sciences Graduate Program, Rutgers University–Newark, Newark, New Jersey 07102
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Krishnakanth Kondabolu
1Center for Molecular and Behavioral Neuroscience, Rutgers University–Newark, Newark, New Jersey 07102
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Alina Khadka
1Center for Molecular and Behavioral Neuroscience, Rutgers University–Newark, Newark, New Jersey 07102
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Maxime Assous
1Center for Molecular and Behavioral Neuroscience, Rutgers University–Newark, Newark, New Jersey 07102
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James M. Tepper
1Center for Molecular and Behavioral Neuroscience, Rutgers University–Newark, Newark, New Jersey 07102
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Tracy S. Tran
2Department of Biological Sciences, Rutgers University–Newark, Newark, New Jersey 07102
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Pierre-Olivier Polack
1Center for Molecular and Behavioral Neuroscience, Rutgers University–Newark, Newark, New Jersey 07102
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Abstract

The functions of cortical networks are progressively established during development by series of events shaping the neuronal connectivity. Synaptic elimination, which consists of removing the supernumerary connections generated during the earlier stages of cortical development, is one of the latest stages in neuronal network maturation. The semaphorin 3F coreceptors neuropilin 2 (Nrp2) and plexin-A3 (PlxnA3) may play an important role in the functional maturation of the cerebral cortex by regulating the excess dendritic spines on cortical excitatory neurons. Yet, the identity of the connections eliminated under the control of Nrp2/PlxnA3 signaling is debated, and the importance of this synaptic refinement for cortical functions remains poorly understood. Here, we show that Nrp2/PlxnA3 controls the spine densities in layer 4 (L4) and on the apical dendrite of L5 neurons of the sensory and motor cortices. Using a combination of neuroanatomical, ex vivo electrophysiology, and in vivo functional imaging techniques in Nrp2 and PlxnA3 KO mice of both sexes, we disprove the hypothesis that Nrp2/PlxnA3 signaling is required to maintain the ectopic thalamocortical connections observed during embryonic development. We also show that the absence of Nrp2/PlxnA3 signaling leads to the hyperexcitability and excessive synchronization of the neuronal activity in L5 and L4 neuronal networks, suggesting that this system could participate in the refinement of the recurrent corticocortical connectivity in those layers. Altogether, our results argue for a role of semaphorin–Nrp2/PlxnA3 signaling in the proper maturation and functional connectivity of the cerebral cortex, likely by controlling the refinement of recurrent corticocortical connections.

SIGNIFICANCE STATEMENT The function of a neuronal circuit is mainly determined by the connections that neurons establish with one another during development. Understanding the mechanisms underlying the establishment of the functional connectivity is fundamental to comprehend how network functions are implemented, and to design treatments aiming at restoring damaged neuronal circuits. Here, we show that the cell surface receptors for the family of semaphorin guidance cues neuropilin 2 (Nrp2) and plexin-A3 (PlxnA3) play an important role in shaping the functional connectivity of the cerebral cortex likely by trimming the recurrent connections in layers 4 and 5. By removing the supernumerary inputs generated during early development, Nrp2/PlxnA3 signaling reduces the neuronal excitability and participates in the maturation of the cortical network functions.

  • cortex maturation
  • cortical layers
  • functional connectivity
  • sema 3F signaling
  • synaptic pruning
  • thalamocortical

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The Journal of Neuroscience: 42 (24)
Journal of Neuroscience
Vol. 42, Issue 24
15 Jun 2022
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Neuropilin 2/Plexin-A3 Receptors Regulate the Functional Connectivity and the Excitability in the Layers 4 and 5 of the Cerebral Cortex
Hussain Y. Khdour, Krishnakanth Kondabolu, Alina Khadka, Maxime Assous, James M. Tepper, Tracy S. Tran, Pierre-Olivier Polack
Journal of Neuroscience 15 June 2022, 42 (24) 4828-4840; DOI: 10.1523/JNEUROSCI.1965-21.2022

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Neuropilin 2/Plexin-A3 Receptors Regulate the Functional Connectivity and the Excitability in the Layers 4 and 5 of the Cerebral Cortex
Hussain Y. Khdour, Krishnakanth Kondabolu, Alina Khadka, Maxime Assous, James M. Tepper, Tracy S. Tran, Pierre-Olivier Polack
Journal of Neuroscience 15 June 2022, 42 (24) 4828-4840; DOI: 10.1523/JNEUROSCI.1965-21.2022
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Keywords

  • cortex maturation
  • cortical layers
  • functional connectivity
  • sema 3F signaling
  • synaptic pruning
  • thalamocortical

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