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Entorhinal layer 6b subplate neurons govern spatial learning and memory

View ORCID ProfileYoav Ben-Simon, View ORCID ProfileKarola Kaefer, View ORCID ProfilePhilipp Velicky, View ORCID ProfileJozsef Csicsvari, View ORCID ProfileJohann G. Danzl, View ORCID ProfilePeter Jonas
doi: https://doi.org/10.1101/2022.01.26.477814
Yoav Ben-Simon
1Institute of Science and Technology, Klosterneuburg, Austria
2Dept. of Neurophysiology and Pharmacology, Vienna Medical University, Vienna, Austria
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  • For correspondence: yoav.bensimon@meduniwien.ac.at
Karola Kaefer
1Institute of Science and Technology, Klosterneuburg, Austria
3Department of Neuroinformatics, Radboud University, Nijmegen, The Netherlands
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Philipp Velicky
1Institute of Science and Technology, Klosterneuburg, Austria
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Jozsef Csicsvari
1Institute of Science and Technology, Klosterneuburg, Austria
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Johann G. Danzl
1Institute of Science and Technology, Klosterneuburg, Austria
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Peter Jonas
1Institute of Science and Technology, Klosterneuburg, Austria
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Abstract

The mammalian hippocampal formation (HF) plays a key role in several higher brain functions, such as spatial coding, learning and memory. Its simple circuit architecture is often viewed as a “trisynaptic loop”, processing input originating from the superficial layers of the entorhinal cortex (EC) in a linear fashion, and sending it back to its deeper layers. Here, we show that contrary to this canonical view, excitatory neurons in the deepest layer of the mouse EC, exhibiting the unique morphology and molecular profile of layer 6b cortical subplate neurons (SPNs), project to all sub-regions comprising the HF, with a preference towards CA3 pyramidal neurons, and receive input from the CA1, thalamus and claustrum. Furthermore, their output is characterized by unique slow-decaying excitatory post-synaptic currents (EPSCs), capable of driving plateau-like potentials in their target cells. Optogenetic inhibition of the EC-6b pathway markedly affects spatial coding in CA1 pyramidal neurons, while cell ablation impairs not only acquisition of new spatial memories, but also degradation of previously acquired ones. Our results provide the first evidence of a functional role for the cortical layer 6b neurons in the adult brain and elucidate a critical novel element determining cortico-hippocampal activity patterns.

Competing Interest Statement

The authors have declared no competing interest.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted January 27, 2022.
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Entorhinal layer 6b subplate neurons govern spatial learning and memory
Yoav Ben-Simon, Karola Kaefer, Philipp Velicky, Jozsef Csicsvari, Johann G. Danzl, Peter Jonas
bioRxiv 2022.01.26.477814; doi: https://doi.org/10.1101/2022.01.26.477814
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Entorhinal layer 6b subplate neurons govern spatial learning and memory
Yoav Ben-Simon, Karola Kaefer, Philipp Velicky, Jozsef Csicsvari, Johann G. Danzl, Peter Jonas
bioRxiv 2022.01.26.477814; doi: https://doi.org/10.1101/2022.01.26.477814

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