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

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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.

Originele taal-2	Engels
Pagina's (van-tot)	6855-6865
Tijdschrift	Proceedings of the National Academy of Sciences of the United States of America
Volume	117
DOI's	https://doi.org/10.1073/pnas.1916163117
Status	Gepubliceerd - 09 mrt 2020

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10.1073/pnas.1916163117

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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

Carulli, Daniela ; Broersen, Robin ; de Winter, Fred ; Muir, Elizabeth M ; Mešković, Maja ; de Waal, Matthijs ; de Vries, Sharon ; Boele, Henk-Jan ; Canto, Cathrin B ; De Zeeuw, Chris I ; Verhaagen, Joost. / Cerebellar plasticity and associative memories are controlled by perineuronal nets. In: Proceedings of the National Academy of Sciences of the United States of America. 2020 ; Vol. 117. blz. 6855-6865.

@article{3fc81fa4e6de46dbb2eb8be342206185,

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, blz. 6855-6865. https://doi.org/10.1073/pnas.1916163117

Cerebellar plasticity and associative memories are controlled by perineuronal nets. / Carulli, Daniela ; Broersen, Robin ; de Winter, Fred; Muir, Elizabeth M; Mešković, Maja; de Waal, Matthijs; de Vries, Sharon; Boele, Henk-Jan; Canto, Cathrin B ; De Zeeuw, Chris I ; Verhaagen, Joost.

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 117, 09.03.2020, blz. 6855-6865.

Onderzoeksoutput: Bijdrage aan wetenschappelijk tijdschrift/periodieke uitgave › Artikel › Wetenschappelijk › peer review

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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

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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.

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DO - 10.1073/pnas.1916163117

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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

SN - 0027-8424

ER -