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Research Report: Regular Manuscript

Induction of BDNF expression in layer II/III and layer V neurons of the motor cortex is essential for motor learning

Thomas Andreska, Stefanie Rauskolb, Nina Scheffler, Patrick Lüningschrör, Manju Sasi, Jeremy Signoret-Genest, Marcus Behringer, Robert Blum, Markus Sauer, Philip Tovote and Michael Sendtner
Journal of Neuroscience 10 July 2020, JN-RM-0288-20; DOI: https://doi.org/10.1523/JNEUROSCI.0288-20.2020
Thomas Andreska
1Institute of Clinical Neurobiology, University Hospital Wuerzburg, 97080 Wuerzburg, Germany
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Stefanie Rauskolb
1Institute of Clinical Neurobiology, University Hospital Wuerzburg, 97080 Wuerzburg, Germany
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Nina Scheffler
1Institute of Clinical Neurobiology, University Hospital Wuerzburg, 97080 Wuerzburg, Germany
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Patrick Lüningschrör
1Institute of Clinical Neurobiology, University Hospital Wuerzburg, 97080 Wuerzburg, Germany
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Manju Sasi
1Institute of Clinical Neurobiology, University Hospital Wuerzburg, 97080 Wuerzburg, Germany
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Jeremy Signoret-Genest
1Institute of Clinical Neurobiology, University Hospital Wuerzburg, 97080 Wuerzburg, Germany
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Marcus Behringer
2Department of Biotechnology and Biophysics, Biocenter, Julius-Maximilians-University Wuerzburg, 97074 Wuerzburg, Germany
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Robert Blum
1Institute of Clinical Neurobiology, University Hospital Wuerzburg, 97080 Wuerzburg, Germany
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Markus Sauer
2Department of Biotechnology and Biophysics, Biocenter, Julius-Maximilians-University Wuerzburg, 97074 Wuerzburg, Germany
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Philip Tovote
1Institute of Clinical Neurobiology, University Hospital Wuerzburg, 97080 Wuerzburg, Germany
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Michael Sendtner
1Institute of Clinical Neurobiology, University Hospital Wuerzburg, 97080 Wuerzburg, Germany
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Abstract

Motor learning depends on synaptic plasticity between corticostriatal projections and striatal medium spiny neurons. Retrograde tracing from the dorsolateral striatum reveals that both layer II/III and layer V neurons in the motor cortex express Brain-derived neurotrophic factor (BDNF) as a potential regulator of plasticity in corticostriatal projections in male and female mice. The number of these BDNF expressing cortical neurons and levels of BDNF protein are highest in juvenile mice when adult motor patterns are shaped, while BDNF levels in the adult are low. When mice are trained by physical exercise in the adult, BDNF expression in motor cortex is re-induced especially in layer II/III projection neurons. Reduced expression of cortical BDNF in 3-month-old mice results in impaired motor learning while space memory is preserved. These findings suggest that activity regulates BDNF expression differentially in layer II/III and V striatal afferents from motor cortex and that cortical BDNF is essential for motor learning.

Impact Statement:

Motor learning in mice depends on corticostriatal BDNF supply, and regulation of BDNF expression during motor learning is highest in corticostriatal projection neurons in cortical layer II/III.

Footnotes

  • The authors have no conflicts of interest or relevant financial relationships to disclose.

  • We thank Drs. Francis Lee, Anders Nykjær and Volkmar Leßmann for critical comments and suggestions. We thank Dr. Tonnis Timmusk for providing the 4C8, 3C11 and 3B2 monoclonal BDNF antibodies. This work was funded by the Deutsche Forschungsgemeinschaft, TRR 58, Project A09, Project SE 697/7-1, a preparatory grant for DFG TRR 295, A05 and the BMBF through the EnergI consortium.

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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Induction of BDNF expression in layer II/III and layer V neurons of the motor cortex is essential for motor learning
Thomas Andreska, Stefanie Rauskolb, Nina Scheffler, Patrick Lüningschrör, Manju Sasi, Jeremy Signoret-Genest, Marcus Behringer, Robert Blum, Markus Sauer, Philip Tovote, Michael Sendtner
Journal of Neuroscience 10 July 2020, JN-RM-0288-20; DOI: 10.1523/JNEUROSCI.0288-20.2020

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Induction of BDNF expression in layer II/III and layer V neurons of the motor cortex is essential for motor learning
Thomas Andreska, Stefanie Rauskolb, Nina Scheffler, Patrick Lüningschrör, Manju Sasi, Jeremy Signoret-Genest, Marcus Behringer, Robert Blum, Markus Sauer, Philip Tovote, Michael Sendtner
Journal of Neuroscience 10 July 2020, JN-RM-0288-20; DOI: 10.1523/JNEUROSCI.0288-20.2020
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