Mesodiencephalic junction GABAergic inputs are processed separately from motor cortical inputs in the basilar pons

Ayoub J. Khalil; Huibert D. Mansvelder; Laurens Witter

doi:10.1016/j.isci.2022.104641

Mesodiencephalic junction GABAergic inputs are processed separately from motor cortical inputs in the basilar pons

Ayoub J. Khalil, Huibert D. Mansvelder, Laurens Witter^*

^*Corresponding author for this work

Research output: Contribution to Journal › Article › Academic › peer-review

Abstract

The basilar pontine nuclei (bPN) are known to receive excitatory input from the entire neocortex and constitute the main source of mossy fibers to the cerebellum. Various potential inhibitory afferents have been described, but their origin, synaptic plasticity, and network function have remained elusive. Here we identify the mesodiencephalic junction (MDJ) as a prominent source of monosynaptic GABAergic inputs to the bPN. We found no evidence that these inputs converge with motor cortex (M1) inputs at the single neuron or at the local network level. Tracing the inputs to GABAergic MDJ neurons revealed inputs to these neurons from neocortical areas. Additionally, we observed little short-term synaptic facilitation or depression in afferents from the MDJ, enabling MDJ inputs to carry sign-inversed neocortical inputs. Thus, our results show a prominent source of GABAergic inhibition to the bPN that could enrich input to the cerebellar granule cell layer.

Original language	English
Article number	104641
Pages (from-to)	1-16
Number of pages	17
Journal	iScience
Volume	25
Issue number	7
Early online date	18 Jun 2022
DOIs	https://doi.org/10.1016/j.isci.2022.104641
Publication status	Published - 15 Jul 2022

Bibliographical note

Funding Information:
This work was supported by an NWO vernieuwingsimpuls VENI grant 016.Veni.171.056. The authors thank J.C. Lodder, A.J. Timmerman, T.S. Heistek, and J. Wortel for their excellent technical assistance. The authors also thank S. Sheikh Abdirashid, V Zucconi Galli Fonseca, and J.K.W. de Vries for help with experiments and F.J. Meye and R.A.H. Adan for help with designing the rabies virus experiment. EnvA-complemented rabies virus (SAD-dG-tdTomato) was a generous gift from K.K. Conzelmann (DFG project-ID 118803580-SFB 870). pAAV-Syn-Chronos-GFP and pAAV-syn-ChrimsonR-tdT were a generous gift from E. Boyden. L.W. designed the study. A.K. performed and analyzed electrophysiological experiments. L.W. performed and analyzed anatomical experiments. All authors checked the data analysis. A.K. and L.W. wrote the article. All authors critically revised the article. The authors declare no competing interests.

Funding Information:
This work was supported by an NWO vernieuwingsimpuls VENI grant 016.Veni.171.056 . The authors thank J.C. Lodder, A.J. Timmerman, T.S. Heistek, and J. Wortel for their excellent technical assistance. The authors also thank S. Sheikh Abdirashid, V Zucconi Galli Fonseca, and J.K.W. de Vries for help with experiments and F.J. Meye and R.A.H. Adan for help with designing the rabies virus experiment. EnvA-complemented rabies virus (SAD-dG-tdTomato) was a generous gift from K.K. Conzelmann (DFG project-ID 118803580-SFB 870). pAAV-Syn-Chronos-GFP and pAAV-syn-ChrimsonR-tdT were a generous gift from E. Boyden.

Publisher Copyright:
© 2022 The Author(s)

Keywords

Cell biology
Neuroscience
Physiology

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title = "Mesodiencephalic junction GABAergic inputs are processed separately from motor cortical inputs in the basilar pons",

abstract = "The basilar pontine nuclei (bPN) are known to receive excitatory input from the entire neocortex and constitute the main source of mossy fibers to the cerebellum. Various potential inhibitory afferents have been described, but their origin, synaptic plasticity, and network function have remained elusive. Here we identify the mesodiencephalic junction (MDJ) as a prominent source of monosynaptic GABAergic inputs to the bPN. We found no evidence that these inputs converge with motor cortex (M1) inputs at the single neuron or at the local network level. Tracing the inputs to GABAergic MDJ neurons revealed inputs to these neurons from neocortical areas. Additionally, we observed little short-term synaptic facilitation or depression in afferents from the MDJ, enabling MDJ inputs to carry sign-inversed neocortical inputs. Thus, our results show a prominent source of GABAergic inhibition to the bPN that could enrich input to the cerebellar granule cell layer.",

keywords = "Cell biology, Neuroscience, Physiology",

author = "Khalil, {Ayoub J.} and Mansvelder, {Huibert D.} and Laurens Witter",

note = "Funding Information: This work was supported by an NWO vernieuwingsimpuls VENI grant 016.Veni.171.056. The authors thank J.C. Lodder, A.J. Timmerman, T.S. Heistek, and J. Wortel for their excellent technical assistance. The authors also thank S. Sheikh Abdirashid, V Zucconi Galli Fonseca, and J.K.W. de Vries for help with experiments and F.J. Meye and R.A.H. Adan for help with designing the rabies virus experiment. EnvA-complemented rabies virus (SAD-dG-tdTomato) was a generous gift from K.K. Conzelmann (DFG project-ID 118803580-SFB 870). pAAV-Syn-Chronos-GFP and pAAV-syn-ChrimsonR-tdT were a generous gift from E. Boyden. L.W. designed the study. A.K. performed and analyzed electrophysiological experiments. L.W. performed and analyzed anatomical experiments. All authors checked the data analysis. A.K. and L.W. wrote the article. All authors critically revised the article. The authors declare no competing interests. Funding Information: This work was supported by an NWO vernieuwingsimpuls VENI grant 016.Veni.171.056 . The authors thank J.C. Lodder, A.J. Timmerman, T.S. Heistek, and J. Wortel for their excellent technical assistance. The authors also thank S. Sheikh Abdirashid, V Zucconi Galli Fonseca, and J.K.W. de Vries for help with experiments and F.J. Meye and R.A.H. Adan for help with designing the rabies virus experiment. EnvA-complemented rabies virus (SAD-dG-tdTomato) was a generous gift from K.K. Conzelmann (DFG project-ID 118803580-SFB 870). pAAV-Syn-Chronos-GFP and pAAV-syn-ChrimsonR-tdT were a generous gift from E. Boyden. Publisher Copyright: {\textcopyright} 2022 The Author(s)",

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AU - Khalil, Ayoub J.

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N1 - Funding Information: This work was supported by an NWO vernieuwingsimpuls VENI grant 016.Veni.171.056. The authors thank J.C. Lodder, A.J. Timmerman, T.S. Heistek, and J. Wortel for their excellent technical assistance. The authors also thank S. Sheikh Abdirashid, V Zucconi Galli Fonseca, and J.K.W. de Vries for help with experiments and F.J. Meye and R.A.H. Adan for help with designing the rabies virus experiment. EnvA-complemented rabies virus (SAD-dG-tdTomato) was a generous gift from K.K. Conzelmann (DFG project-ID 118803580-SFB 870). pAAV-Syn-Chronos-GFP and pAAV-syn-ChrimsonR-tdT were a generous gift from E. Boyden. L.W. designed the study. A.K. performed and analyzed electrophysiological experiments. L.W. performed and analyzed anatomical experiments. All authors checked the data analysis. A.K. and L.W. wrote the article. All authors critically revised the article. The authors declare no competing interests. Funding Information: This work was supported by an NWO vernieuwingsimpuls VENI grant 016.Veni.171.056 . The authors thank J.C. Lodder, A.J. Timmerman, T.S. Heistek, and J. Wortel for their excellent technical assistance. The authors also thank S. Sheikh Abdirashid, V Zucconi Galli Fonseca, and J.K.W. de Vries for help with experiments and F.J. Meye and R.A.H. Adan for help with designing the rabies virus experiment. EnvA-complemented rabies virus (SAD-dG-tdTomato) was a generous gift from K.K. Conzelmann (DFG project-ID 118803580-SFB 870). pAAV-Syn-Chronos-GFP and pAAV-syn-ChrimsonR-tdT were a generous gift from E. Boyden. Publisher Copyright: © 2022 The Author(s)

PY - 2022/7/15

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N2 - The basilar pontine nuclei (bPN) are known to receive excitatory input from the entire neocortex and constitute the main source of mossy fibers to the cerebellum. Various potential inhibitory afferents have been described, but their origin, synaptic plasticity, and network function have remained elusive. Here we identify the mesodiencephalic junction (MDJ) as a prominent source of monosynaptic GABAergic inputs to the bPN. We found no evidence that these inputs converge with motor cortex (M1) inputs at the single neuron or at the local network level. Tracing the inputs to GABAergic MDJ neurons revealed inputs to these neurons from neocortical areas. Additionally, we observed little short-term synaptic facilitation or depression in afferents from the MDJ, enabling MDJ inputs to carry sign-inversed neocortical inputs. Thus, our results show a prominent source of GABAergic inhibition to the bPN that could enrich input to the cerebellar granule cell layer.

AB - The basilar pontine nuclei (bPN) are known to receive excitatory input from the entire neocortex and constitute the main source of mossy fibers to the cerebellum. Various potential inhibitory afferents have been described, but their origin, synaptic plasticity, and network function have remained elusive. Here we identify the mesodiencephalic junction (MDJ) as a prominent source of monosynaptic GABAergic inputs to the bPN. We found no evidence that these inputs converge with motor cortex (M1) inputs at the single neuron or at the local network level. Tracing the inputs to GABAergic MDJ neurons revealed inputs to these neurons from neocortical areas. Additionally, we observed little short-term synaptic facilitation or depression in afferents from the MDJ, enabling MDJ inputs to carry sign-inversed neocortical inputs. Thus, our results show a prominent source of GABAergic inhibition to the bPN that could enrich input to the cerebellar granule cell layer.

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KW - Neuroscience

KW - Physiology

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ER -

Mesodiencephalic junction GABAergic inputs are processed separately from motor cortical inputs in the basilar pons

Abstract

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