Cerebellar Purkinje cells can differentially modulate coherence between sensory and motor cortex depending on region and behavior

• Published in: Proceedings of the National Academy of Sciences - PNAS 2021-01, Vol.118 (2), p.1-11
• Main Authors: Lindeman, Sander, Hong, Sungho, Kros, Lieke, Mejias, Jorge F., Romano, Vincenzo, Oostenveld, Robert, Negrello, Mario, Bosman, Laurens W. J., De Zeeuw, Chris I.
• Format: Article
• Language: English
• Subjects: Animals; Biological Sciences; Cell activation; Cerebellar Cortex; Cerebellum; Cerebellum - metabolism; Coherence; Computer applications; Cortex (motor); Female; Firing rate; Humans; Male; Mice; Mice, Transgenic; Motor Cortex - metabolism; Optogenetics; Purkinje cells; Purkinje Cells - metabolism; Sensorimotor Cortex; Sensorimotor integration; Sensory integration; Sleep; Somatosensory cortex; Somatosensory Cortex - metabolism; Stimulation; Thalamus; Ventral Thalamic Nuclei; Vibrissae - physiology
• ISSN: 0027-8424; 1091-6490
• DOI: 10.1073/pnas.2015292118

Activity of sensory and motor cortices is essential for sensorimotor integration. In particular, coherence between these areas may indicate binding of critical functions like perception, motor planning, action, or sleep. Evidence is accumulating that cerebellar output modulates cortical activity and coherence, but how, when, and where it does so is unclear. We studied activity in and coherence between S1 and M1 cortices during whisker stimulation in the absence and presence of optogenetic Purkinje cell stimulation in crus 1 and 2 of awake mice, eliciting strong simple spike rate modulation. Without Purkinje cell stimulation, whisker stimulation triggers fast responses in S1 and M1 involving transient coherence in a broad spectrum. Simultaneous stimulation of Purkinje cells and whiskers affects amplitude and kinetics of sensory responses in S1 and M1 and alters the estimated S1–M1 coherence in theta and gamma bands, allowing bidirectional control dependent on behavioral context. These effects are absent when Purkinje cell activation is delayed by 20 ms. Focal stimulation of Purkinje cells revealed site specificity, with cells in medial crus 2 showing the most prominent and selective impact on estimated coherence, i.e., a strong suppression in the gamma but not the theta band. Granger causality analyses and computational modeling of the involved networks suggest that Purkinje cells control S1–M1 phase consistency predominantly via ventrolateral thalamus and M1. Our results indicate that activity of sensorimotor cortices can be dynamically and functionally modulated by specific cerebellar inputs, highlighting a widespread role of the cerebellum in coordinating sensorimotor behavior.