Early Insights into Eyeblink Conditioning Using Optically Pumped Magnetometer-Based MEG

Chin-Hsuan Sophie Lin^1,2*Tim M Tierney³Stephanie Mellor³George C O'Neill³Sven Bestmann³Gareth R Barnes³R Chris Miall¹

• ¹University of Birmingham, Birmingham, United Kingdom
• ²The University of Melbourne, Melbourne, Australia
• ³University College London, London, United Kingdom

There is a profound lack of electrophysiological data from the cerebellum in humans, as compared to animals, because it is difficult to record cerebellar activity non-invasively using magnetoencephalography (MEG) or electroencephalography (EEG). Recent developments in wearable MEG sensors hold potential to overcome this limitation, as they allow the placement of sensors closer to the cerebellum. We leveraged the development of wearable optically pumped magnetometers to record on-scalp MEG (OP-MEG) during an established cerebellar learning paradigm - eyeblink conditioning. In four healthy human adults, we first validated that OP-MEG can reliably detect cerebellar responses by showing significant responses in sensors over the cerebellar region in response to an air puff stimulus in all four adults. We then indirectly tested the hypothesis that these responses reflect the population-level spiking activity of Purkinje cells. We demonstrated these air-puff evoked responses diminished during the acquisition of conditioned responses, corresponding with previously observed changes in Purkinje cell activities in animals. Additionally, in three out of four participants, we observed a cerebellar evoked response just prior to the peak of the conditioned blink, similar to learning-associated shifts in Purkinje cell response latencies. This study demonstrates that OP-MEG is a viable method for recording cerebellar activity and further supports the role of the cerebellum in human learning by bridging findings from invasive animal recordings with human neuroimaging.