Differential spatiotemporal development of Purkinje cell populations and cerebellum-dependent sensorimotor behaviors

Gerrit Cornelis Beekhof; Catarina Osório; Joshua J. White; Scott Van Zoomeren; Hannah van der Stok; Bilian Xiong; Ingo H.M.S. Nettersheim; Willem Ashwin Mak; Marit Runge; Francesca Romana Fiocchi; Henk Jan Boele; Freek E. Hoebeek; Martijn Schonewille

doi:10.7554/eLife.63668

Differential spatiotemporal development of Purkinje cell populations and cerebellum-dependent sensorimotor behaviors

Gerrit Cornelis Beekhof, Catarina Osório, Joshua J. White, Scott Van Zoomeren, Hannah van der Stok, Bilian Xiong, Ingo H.M.S. Nettersheim, Willem Ashwin Mak, Marit Runge, Francesca Romana Fiocchi, Henk Jan Boele, Freek E. Hoebeek, Martijn Schonewille^*

^*Corresponding author for this work

Neurosciences

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

16 Citations (Scopus)

15 Downloads (Pure)

Abstract

Distinct populations of Purkinje cells (PCs) with unique molecular and connectivity features are at the core of the modular organization of the cerebellum. Previously, we showed that firing activity of PCs differs between ZebrinII-positive and ZebrinII-negative cerebellar modules (Zhou et al., 2014; Wu et al., 2019). Here, we investigate the timing and extent of PC differentiation during development in mice. We found that several features of PCs, including activity levels, dendritic arborization, axonal shape and climbing fiber input, develop differentially between nodular and anterior PC populations. Although all PCs show a particularly rapid development in the second postnatal week, anterior PCs typically have a prolonged physiological and dendritic maturation. In line herewith, younger mice exhibit attenuated anterior-dependent eyeblink conditioning, but faster nodular-dependent compensatory eye movement adaptation. Our results indicate that specific cerebellar regions have unique developmental timelines which match with their related, specific forms of cerebellum-dependent behaviors.

Original language	English
Article number	e63668
Journal	eLife
Volume	10
DOIs	https://doi.org/10.7554/eLife.63668
Publication status	Published - 11 Jun 2021

Bibliographical note

Funding Information:
The authors kindly thank Laura Post, Sander Kruithof and Erika Sabel-Goedknegt for excellent technical assistance; Dick Jaarsma and Lynette Lim for discussions and comments on the manuscript. This work was supported by an ERC starter grant (ERC-Stg #680235; MS), Dutch Organization for Life Sciences (Off-Road fellowship; ZonMW-451001027; CO), VENI fellowship (NWO-ENW; JJW), VIDI grant (NWO-ENW; #016.121.346, FEH) and Medical Sciences (TOP-GO #91210067, FEH) and the CJ Vaillant Fund (FEH).

Funding Information:
H2020 European Research Council ERC-Stg #680235 Martijn Schonewille ZonMw ZonMW-451001027 Catarina Os?rio Nederlandse Organisatie voor Wetenschappelijk Onderzoek #016.121.346 Freek E Hoebeek ZonMw #91210067 Freek E Hoebeek Nederlandse Organisatie voor Wetenschappelijk Onderzoek 016.Veni.192.270 Joshua J White.

Publisher Copyright:
© Beekhof et al.

Access to Document

10.7554/eLife.63668Licence: CC BY

elife-63668-v2Final published version, 8.14 MBLicence: CC BY

Cite this

Beekhof, G. C., Osório, C., White, J. J., Van Zoomeren, S., van der Stok, H., Xiong, B., Nettersheim, I. H. M. S., Mak, W. A., Runge, M., Fiocchi, F. R., Boele, H. J., Hoebeek, F. E., & Schonewille, M. (2021). Differential spatiotemporal development of Purkinje cell populations and cerebellum-dependent sensorimotor behaviors. eLife, 10, Article e63668. https://doi.org/10.7554/eLife.63668

@article{5a741ac63d964d678fa9673e8ae3dbdf,

title = "Differential spatiotemporal development of Purkinje cell populations and cerebellum-dependent sensorimotor behaviors",

abstract = "Distinct populations of Purkinje cells (PCs) with unique molecular and connectivity features are at the core of the modular organization of the cerebellum. Previously, we showed that firing activity of PCs differs between ZebrinII-positive and ZebrinII-negative cerebellar modules (Zhou et al., 2014; Wu et al., 2019). Here, we investigate the timing and extent of PC differentiation during development in mice. We found that several features of PCs, including activity levels, dendritic arborization, axonal shape and climbing fiber input, develop differentially between nodular and anterior PC populations. Although all PCs show a particularly rapid development in the second postnatal week, anterior PCs typically have a prolonged physiological and dendritic maturation. In line herewith, younger mice exhibit attenuated anterior-dependent eyeblink conditioning, but faster nodular-dependent compensatory eye movement adaptation. Our results indicate that specific cerebellar regions have unique developmental timelines which match with their related, specific forms of cerebellum-dependent behaviors.",

author = "Beekhof, {Gerrit Cornelis} and Catarina Os{\'o}rio and White, {Joshua J.} and {Van Zoomeren}, Scott and {van der Stok}, Hannah and Bilian Xiong and Nettersheim, {Ingo H.M.S.} and Mak, {Willem Ashwin} and Marit Runge and Fiocchi, {Francesca Romana} and Boele, {Henk Jan} and Hoebeek, {Freek E.} and Martijn Schonewille",

note = "Funding Information: The authors kindly thank Laura Post, Sander Kruithof and Erika Sabel-Goedknegt for excellent technical assistance; Dick Jaarsma and Lynette Lim for discussions and comments on the manuscript. This work was supported by an ERC starter grant (ERC-Stg #680235; MS), Dutch Organization for Life Sciences (Off-Road fellowship; ZonMW-451001027; CO), VENI fellowship (NWO-ENW; JJW), VIDI grant (NWO-ENW; #016.121.346, FEH) and Medical Sciences (TOP-GO #91210067, FEH) and the CJ Vaillant Fund (FEH). Funding Information: H2020 European Research Council ERC-Stg #680235 Martijn Schonewille ZonMw ZonMW-451001027 Catarina Os?rio Nederlandse Organisatie voor Wetenschappelijk Onderzoek #016.121.346 Freek E Hoebeek ZonMw #91210067 Freek E Hoebeek Nederlandse Organisatie voor Wetenschappelijk Onderzoek 016.Veni.192.270 Joshua J White. Publisher Copyright: {\textcopyright} Beekhof et al.",

year = "2021",

month = jun,

day = "11",

doi = "10.7554/eLife.63668",

language = "English",

volume = "10",

journal = "eLife",

issn = "2050-084X",

publisher = "eLife Sciences Publications",

}

TY - JOUR

T1 - Differential spatiotemporal development of Purkinje cell populations and cerebellum-dependent sensorimotor behaviors

AU - Beekhof, Gerrit Cornelis

AU - Osório, Catarina

AU - White, Joshua J.

AU - Van Zoomeren, Scott

AU - van der Stok, Hannah

AU - Xiong, Bilian

AU - Nettersheim, Ingo H.M.S.

AU - Mak, Willem Ashwin

AU - Runge, Marit

AU - Fiocchi, Francesca Romana

AU - Boele, Henk Jan

AU - Hoebeek, Freek E.

AU - Schonewille, Martijn

N1 - Funding Information: The authors kindly thank Laura Post, Sander Kruithof and Erika Sabel-Goedknegt for excellent technical assistance; Dick Jaarsma and Lynette Lim for discussions and comments on the manuscript. This work was supported by an ERC starter grant (ERC-Stg #680235; MS), Dutch Organization for Life Sciences (Off-Road fellowship; ZonMW-451001027; CO), VENI fellowship (NWO-ENW; JJW), VIDI grant (NWO-ENW; #016.121.346, FEH) and Medical Sciences (TOP-GO #91210067, FEH) and the CJ Vaillant Fund (FEH). Funding Information: H2020 European Research Council ERC-Stg #680235 Martijn Schonewille ZonMw ZonMW-451001027 Catarina Os?rio Nederlandse Organisatie voor Wetenschappelijk Onderzoek #016.121.346 Freek E Hoebeek ZonMw #91210067 Freek E Hoebeek Nederlandse Organisatie voor Wetenschappelijk Onderzoek 016.Veni.192.270 Joshua J White. Publisher Copyright: © Beekhof et al.

PY - 2021/6/11

Y1 - 2021/6/11

N2 - Distinct populations of Purkinje cells (PCs) with unique molecular and connectivity features are at the core of the modular organization of the cerebellum. Previously, we showed that firing activity of PCs differs between ZebrinII-positive and ZebrinII-negative cerebellar modules (Zhou et al., 2014; Wu et al., 2019). Here, we investigate the timing and extent of PC differentiation during development in mice. We found that several features of PCs, including activity levels, dendritic arborization, axonal shape and climbing fiber input, develop differentially between nodular and anterior PC populations. Although all PCs show a particularly rapid development in the second postnatal week, anterior PCs typically have a prolonged physiological and dendritic maturation. In line herewith, younger mice exhibit attenuated anterior-dependent eyeblink conditioning, but faster nodular-dependent compensatory eye movement adaptation. Our results indicate that specific cerebellar regions have unique developmental timelines which match with their related, specific forms of cerebellum-dependent behaviors.

AB - Distinct populations of Purkinje cells (PCs) with unique molecular and connectivity features are at the core of the modular organization of the cerebellum. Previously, we showed that firing activity of PCs differs between ZebrinII-positive and ZebrinII-negative cerebellar modules (Zhou et al., 2014; Wu et al., 2019). Here, we investigate the timing and extent of PC differentiation during development in mice. We found that several features of PCs, including activity levels, dendritic arborization, axonal shape and climbing fiber input, develop differentially between nodular and anterior PC populations. Although all PCs show a particularly rapid development in the second postnatal week, anterior PCs typically have a prolonged physiological and dendritic maturation. In line herewith, younger mice exhibit attenuated anterior-dependent eyeblink conditioning, but faster nodular-dependent compensatory eye movement adaptation. Our results indicate that specific cerebellar regions have unique developmental timelines which match with their related, specific forms of cerebellum-dependent behaviors.

UR - http://www.scopus.com/inward/record.url?scp=85108304079&partnerID=8YFLogxK

U2 - 10.7554/eLife.63668

DO - 10.7554/eLife.63668

M3 - Article

C2 - 33973524

AN - SCOPUS:85108304079

SN - 2050-084X

VL - 10

JO - eLife

JF - eLife

M1 - e63668

ER -

Differential spatiotemporal development of Purkinje cell populations and cerebellum-dependent sensorimotor behaviors

Abstract

Bibliographical note

Access to Document

Other files and links

Fingerprint

Cite this