EEG responses induced by cerebellar TMS at rest and during visuomotor adaptation
Po-Yu Fong,
Danny Spampinato,
Kevin Michell,
Marco Mancuso,
Katlyn Brown,
Jaime Ibáñez,
Alessandro Di Santo,
Anna Latorre,
Kailash Bhatia,
John C Rothwell,
Lorenzo Rocchi
Affiliations
Po-Yu Fong
Department of Clinical and Movement Neurosciences, UCL Queen Square Institute of Neurology, University College London, 3rd floor, 33 Queen Square, London WC1N 3BG, UK; Division of Movement Disorders, Department of Neurology and Neuroscience Research Center, Chang Gung Memorial Hospital at Linkou, Taoyuan City, Taiwan, ROC; Medical School, College of Medicine, Chang Gung University, Taoyuan, Taiwan, ROC; Corresponding author at: Department of Clinical and Movement Neurosciences, UCL Queen Square Institute of Neurology, University College London, 3rd floor, 33 Queen Square, London WC1N 3BG, UK.
Danny Spampinato
Department of Clinical and Movement Neurosciences, UCL Queen Square Institute of Neurology, University College London, 3rd floor, 33 Queen Square, London WC1N 3BG, UK; Non-invasive Brain Stimulation Unit, IRCCS Santa Lucia Foundation, Via Ardeatina 306/354, Rome 00142, Italy
Kevin Michell
UCL Queen Square Institute of Neurology, University College London, London, UK
Marco Mancuso
Department of Human Neurosciences, Sapienza University of Rome, Rome, Italy
Katlyn Brown
Department of Kinesiology, University of Waterloo, Waterloo, ON, Canada
Jaime Ibáñez
Department of Clinical and Movement Neurosciences, UCL Queen Square Institute of Neurology, University College London, 3rd floor, 33 Queen Square, London WC1N 3BG, UK; BSICoS group, I3A Institute, University of Zaragoza, IIS Aragón, Zaragoza, Spain; Department of Bioengineering, Imperial College, London, UK
Alessandro Di Santo
NEuroMuscular Omnicentre (NEMO), Serena Onlus, AOS Monaldi, Naples, Italy; Unit of Neurology, Department of Medicine, Campus Bio-Medico University of Rome, Rome, Italy
Anna Latorre
Department of Clinical and Movement Neurosciences, UCL Queen Square Institute of Neurology, University College London, 3rd floor, 33 Queen Square, London WC1N 3BG, UK
Kailash Bhatia
Department of Clinical and Movement Neurosciences, UCL Queen Square Institute of Neurology, University College London, 3rd floor, 33 Queen Square, London WC1N 3BG, UK
John C Rothwell
Department of Clinical and Movement Neurosciences, UCL Queen Square Institute of Neurology, University College London, 3rd floor, 33 Queen Square, London WC1N 3BG, UK
Lorenzo Rocchi
Department of Clinical and Movement Neurosciences, UCL Queen Square Institute of Neurology, University College London, 3rd floor, 33 Queen Square, London WC1N 3BG, UK; Department of Medical Sciences and Public Health, University of Cagliari, Cagliari, Italy
Background: Connections between the cerebellum and the cortex play a critical role in learning and executing complex behaviours. Dual-coil transcranial magnetic stimulation (TMS) can be used non-invasively to probe connectivity changes between the lateral cerebellum and motor cortex (M1) using the motor evoked potential as an outcome measure (cerebellar-brain inhibition, CBI). However, it gives no information about cerebellar connections to other parts of cortex. Objectives: We used electroencephalography (EEG) to investigate whether it was possible to detect activity evoked in any areas of cortex by single-pulse TMS of the cerebellum (cerebellar TMS evoked potentials, cbTEPs). A second experiment tested if these responses were influenced by the performance of a cerebellar-dependent motor learning paradigm. Methods: In the first series of experiments, TMS was applied over either the right or left cerebellar cortex, and scalp EEG was recorded simultaneously. Control conditions that mimicked auditory and somatosensory inputs associated with cerebellar TMS were included to identify responses due to non-cerebellar sensory stimulation. We conducted a follow-up experiment that evaluated whether cbTEPs are behaviourally sensitive by assessing individuals before and after learning a visuomotor reach adaptation task. Results: A TMS pulse over the lateral cerebellum evoked EEG responses that could be distinguished from those caused by auditory and sensory artefacts. Significant positive (P80) and negative peaks (N110) over the contralateral frontal cerebral area were identified with a mirrored scalp distribution after left vs. right cerebellar stimulation. The P80 and N110 peaks were replicated in the cerebellar motor learning experiment and changed amplitude at different stages of learning. The change in amplitude of the P80 peak was associated with the degree of learning that individuals retained following adaptation. Due to overlap with sensory responses, the N110 should be interpreted with caution. Conclusions: Cerebral potentials evoked by TMS of the lateral cerebellum provide a neurophysiological probe of cerebellar function that complements the existing CBI method. They may provide novel insight into mechanisms of visuomotor adaptation and other cognitive processes.
