Cerebellar plasticity and associative memories are controlled by perineuronal nets

Daniela Carulli; Robin Broersen; Fred de Winter; Elizabeth M Muir; Maja Mešković; Matthijs de Waal; Sharon de Vries; Henk-Jan Boele; Cathrin B Canto; Chris I De Zeeuw; Joost Verhaagen

doi:10.1073/pnas.1916163117

Cerebellar plasticity and associative memories are controlled by perineuronal nets

Daniela Carulli, Robin Broersen, Fred de Winter, Elizabeth M Muir, Maja Mešković, Matthijs de Waal, Sharon de Vries, Henk-Jan Boele, Cathrin B Canto, Chris I De Zeeuw, Joost Verhaagen

Netherlands Institute for Neuroscience (NIN)

Research output: Contribution to journal/periodical › Article › Scientific › peer-review

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Abstract

Perineuronal nets (PNNs) are assemblies of extracellular matrix molecules, which surround the cell body and dendrites of many types of neuron and regulate neural plasticity. PNNs are prominently expressed around neurons of the deep cerebellar nuclei (DCN), but their role in adult cerebellar plasticity and behavior is far from clear. Here we show that PNNs in the mouse DCN are diminished during eyeblink conditioning (EBC), a form of associative motor learning that depends on DCN plasticity. When memories are fully acquired, PNNs are restored. Enzymatic digestion of PNNs in the DCN improves EBC learning, but intact PNNs are necessary for memory retention. At the structural level, PNN removal induces significant synaptic rearrangements in vivo, resulting in increased inhibition of DCN baseline activity in awake behaving mice. Together, these results demonstrate that PNNs are critical players in the regulation of cerebellar circuitry and function.

Original language	English
Pages (from-to)	6855-6865
Journal	Proceedings of the National Academy of Sciences of the United States of America
Volume	117
DOIs	https://doi.org/10.1073/pnas.1916163117
Publication status	Published - 09 Mar 2020

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Carulli, D., Broersen, R., de Winter, F., Muir, E. M., Mešković, M., de Waal, M., de Vries, S., Boele, H.-J., Canto, C. B., De Zeeuw, C. I., & Verhaagen, J. (2020). Cerebellar plasticity and associative memories are controlled by perineuronal nets. Proceedings of the National Academy of Sciences of the United States of America, 117, 6855-6865. https://doi.org/10.1073/pnas.1916163117

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title = "Cerebellar plasticity and associative memories are controlled by perineuronal nets",

abstract = "Perineuronal nets (PNNs) are assemblies of extracellular matrix molecules, which surround the cell body and dendrites of many types of neuron and regulate neural plasticity. PNNs are prominently expressed around neurons of the deep cerebellar nuclei (DCN), but their role in adult cerebellar plasticity and behavior is far from clear. Here we show that PNNs in the mouse DCN are diminished during eyeblink conditioning (EBC), a form of associative motor learning that depends on DCN plasticity. When memories are fully acquired, PNNs are restored. Enzymatic digestion of PNNs in the DCN improves EBC learning, but intact PNNs are necessary for memory retention. At the structural level, PNN removal induces significant synaptic rearrangements in vivo, resulting in increased inhibition of DCN baseline activity in awake behaving mice. Together, these results demonstrate that PNNs are critical players in the regulation of cerebellar circuitry and function.",

author = "Daniela Carulli and Robin Broersen and {de Winter}, Fred and Muir, {Elizabeth M} and Maja Me{\v s}kovi{\'c} and {de Waal}, Matthijs and {de Vries}, Sharon and Henk-Jan Boele and Canto, {Cathrin B} and {De Zeeuw}, {Chris I} and Joost Verhaagen",

note = "Copyright {\textcopyright} 2020 the Author(s). Published by PNAS.",

year = "2020",

month = mar,

day = "9",

doi = "10.1073/pnas.1916163117",

language = "English",

volume = "117",

pages = "6855--6865",

journal = "Proceedings of the National Academy of Sciences of the United States of America",

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Carulli, D , Broersen, R , de Winter, F, Muir, EM, Mešković, M, de Waal, M, de Vries, S, Boele, H-J, Canto, CB , De Zeeuw, CI & Verhaagen, J 2020, 'Cerebellar plasticity and associative memories are controlled by perineuronal nets', Proceedings of the National Academy of Sciences of the United States of America, vol. 117, pp. 6855-6865. https://doi.org/10.1073/pnas.1916163117

TY - JOUR

T1 - Cerebellar plasticity and associative memories are controlled by perineuronal nets

AU - Carulli, Daniela

AU - Broersen, Robin

AU - de Winter, Fred

AU - Muir, Elizabeth M

AU - Mešković, Maja

AU - de Waal, Matthijs

AU - de Vries, Sharon

AU - Boele, Henk-Jan

AU - Canto, Cathrin B

AU - De Zeeuw, Chris I

AU - Verhaagen, Joost

PY - 2020/3/9

Y1 - 2020/3/9

N2 - Perineuronal nets (PNNs) are assemblies of extracellular matrix molecules, which surround the cell body and dendrites of many types of neuron and regulate neural plasticity. PNNs are prominently expressed around neurons of the deep cerebellar nuclei (DCN), but their role in adult cerebellar plasticity and behavior is far from clear. Here we show that PNNs in the mouse DCN are diminished during eyeblink conditioning (EBC), a form of associative motor learning that depends on DCN plasticity. When memories are fully acquired, PNNs are restored. Enzymatic digestion of PNNs in the DCN improves EBC learning, but intact PNNs are necessary for memory retention. At the structural level, PNN removal induces significant synaptic rearrangements in vivo, resulting in increased inhibition of DCN baseline activity in awake behaving mice. Together, these results demonstrate that PNNs are critical players in the regulation of cerebellar circuitry and function.

AB - Perineuronal nets (PNNs) are assemblies of extracellular matrix molecules, which surround the cell body and dendrites of many types of neuron and regulate neural plasticity. PNNs are prominently expressed around neurons of the deep cerebellar nuclei (DCN), but their role in adult cerebellar plasticity and behavior is far from clear. Here we show that PNNs in the mouse DCN are diminished during eyeblink conditioning (EBC), a form of associative motor learning that depends on DCN plasticity. When memories are fully acquired, PNNs are restored. Enzymatic digestion of PNNs in the DCN improves EBC learning, but intact PNNs are necessary for memory retention. At the structural level, PNN removal induces significant synaptic rearrangements in vivo, resulting in increased inhibition of DCN baseline activity in awake behaving mice. Together, these results demonstrate that PNNs are critical players in the regulation of cerebellar circuitry and function.

U2 - 10.1073/pnas.1916163117

DO - 10.1073/pnas.1916163117

M3 - Article

C2 - 32152108

SN - 0027-8424

VL - 117

SP - 6855

EP - 6865

JO - Proceedings of the National Academy of Sciences of the United States of America

JF - Proceedings of the National Academy of Sciences of the United States of America

ER -

Cerebellar plasticity and associative memories are controlled by perineuronal nets

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