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Modulating Human Procedural Learning by Cerebellar Transcranial Direct Current Stimulation

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Abstract

Neuroimaging studies suggest that the cerebellum contributes to human cognitive processing, particularly procedural learning. This type of learning is often described as implicit learning and involves automatic, associative, and unintentional learning processes. Our aim was to investigate whether cerebellar transcranial direct current stimulation (tDCS) influences procedural learning as measured by the serial reaction time task (SRTT), in which subjects make speeded key press responses to visual cues. A preliminary modeling study demonstrated that our electrode montage (active electrode over the cerebellum with an extra-cephalic reference) generated the maximum electric field amplitude in the cerebellum. We enrolled 21 healthy subjects (aged 20–49 years). Participants did the SRTT, a visual analogue scale and a visual attention task, before and 35 min after receiving 20-min anodal and sham cerebellar tDCS in a randomized order. To avoid carry-over effects, experimental sessions were held at least 1 week apart. For our primary outcome measure (difference in RTs for random and repeated blocks) anodal versus sham tDCS, RTs were significantly slower for sham tDCS than for anodal cerebellar tDCS (p = 0.04), demonstrating that anodal tDCS influenced implicit learning processes. When we assessed RTs for procedural learning across the one to eight blocks, we found that RTs changed significantly after anodal stimulation (interaction “time” × “blocks 1/8”: anodal, p = 0.006), but after sham tDCS, they remained unchanged (p = 0.094). No significant changes were found in the other variables assessed. Our finding that anodal cerebellar tDCS improves an implicit learning type essential to the development of several motor skills or cognitive activity suggests that the cerebellum has a critical role in procedural learning. tDCS could be a new tool for improving procedural learning in daily life in healthy subjects and for correcting abnormal learning in neuropsychiatric disorders.

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Abbreviations

rTMS:

Repetitive transcranial magnetic stimulation

SRRT:

Serial reaction time task

tDCS:

Transcranial direct current stimulation

VAS:

Visual analogue scale

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Conflict of Interest

Roberta Ferrucci is a stakeholder in Newronika s.r.l., a spin-off company of the Fondazione IRCCS Ca’ Granda Ospedale Maggiore Policlinico and the Università degli Studi di Milano.

Andre R. Brunoni reported no financial interests or potential conflicts of interest.

Marta Parazzini reported no financial interests or potential conflicts of interest.

Maurizio Vergari is a stakeholder in Newronika s.r.l., a spin-off company of the Fondazione IRCCS Ca’ Granda Ospedale Maggiore Policlinico and of the Università degli Studi di Milano.

Elena Rossi is supported by “Dote ricerca”: FSE, Regione Lombardia and Newronika srl., a spin-off company of the Fondazione IRCCS Ca’ Granda Ospedale Maggiore Policlinico and the Università degli Studi di Milano.

Manuela Fumagalli reported no financial interests or potential conflicts of interest.

Francesca Mameli is a stakeholder in Newronika s.r.l., a spin-off company of the Fondazione IRCCS Ca’ Granda Ospedale Maggiore Policlinico and the Università degli Studi di Milano.

Manuela Rosa reported no financial interests or potential conflicts of interest.

Gaia Giannicola reported no financial interests or potential conflicts of interest.

Stefano Zago reported no financial interests or potential conflicts of interest.

Alberto Priori is a stakeholder in Newronika s.r.l., a spin-off company of the Fondazione IRCCS Ca’ Granda Ospedale Maggiore Policlinico and of the Università degli Studi di Milano.

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Authors and Affiliations

  1. Centro Clinico per la Neurostimolazione, le Neurotecnologie ed i Disordini del Movimento, Fondazione IRCCS Ca’ Granda Ospedale Maggiore Policlinico, Milan, Italy

    Roberta Ferrucci, Manuela Fumagalli, Francesca Mameli, Manuela Rosa, Gaia Giannicola & Alberto Priori

  2. Centro de Pesquisas Clínicas, Hospital Universitário, Universidade de São Paulo, São Paulo, Brasil

    Andre R. Brunoni

  3. CNR Consiglio Nazionale delle Ricerche, Istituto di Ingegneria Biomedica ISIB CNR, Milan, Italy

    Marta Parazzini

  4. U.O. Neurofisiopatologia, Fondazione IRCCS Ca’ Granda Ospedale Maggiore Policlinico, Milan, Italy

    Maurizio Vergari

  5. Dipartimento di Fisiopatologia medico-chirurgica e dei Trapianti, Università degli Studi di Milano, Milan, Italy

    Elena Rossi

  6. U.O. Neurologia, Fondazione IRCCS Ca’ Granda Ospedale Maggiore Policlinico, Milan, Italy

    Stefano Zago

  7. Dipartimento di Fisiopatologia medico-chirurgica e dei Trapianti, Università degli Studi di Milano, Milan, Italy

    Alberto Priori

Authors
  1. Roberta Ferrucci
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  2. Andre R. Brunoni
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  3. Marta Parazzini
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  4. Maurizio Vergari
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  5. Elena Rossi
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  6. Manuela Fumagalli
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  7. Francesca Mameli
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  8. Manuela Rosa
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  9. Gaia Giannicola
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  10. Stefano Zago
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  11. Alberto Priori
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Corresponding author

Correspondence to Alberto Priori.

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Ferrucci, R., Brunoni, A.R., Parazzini, M. et al. Modulating Human Procedural Learning by Cerebellar Transcranial Direct Current Stimulation. Cerebellum 12, 485–492 (2013). https://doi.org/10.1007/s12311-012-0436-9

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  • DOI: https://doi.org/10.1007/s12311-012-0436-9

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