Potentiation of cerebellar Purkinje cells facilitates whisker reflex adaptation through increased simple spike activity

Abstract

Cerebellar plasticity underlies motor learning. However, how the cerebellum operates to enable learned changes in motor output is largely unknown. We developed a sensory-driven adaptation protocol for reflexive whisker protraction and recorded Purkinje cell activity from crus 1 and 2 of awake mice. Before training, simple spikes of individual Purkinje cells correlated during reflexive protraction with the whisker position without lead or lag. After training, simple spikes and whisker protractions were both enhanced with the spiking activity now leading behavioral responses. Neuronal and behavioral changes did not occur in two cell-specific mouse models with impaired long-term potentiation at their parallel fiber to Purkinje cell synapses. Consistent with cerebellar plasticity rules, increased simple spike activity was prominent in cells with low complex spike response probability. Thus, potentiation at parallel fiber to Purkinje cell synapses may contribute to reflex adaptation and enable expression of cerebellar learning through increases in simple spike activity.

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

“…More specifically, comparison of the impact of Purkinje cell stimulation on the extent of sensory-induced coherence revealed that Purkinje cells in medial crus 2 and lateral crus 1 differed in their impact on gamma band coherence, but showed no significant difference on theta band coherence. Since these data on regional heterogeneity were based on differential Purkinje cell modulations during different forms of adaptive and reflexive whisking behavior (Romano et al, 2018), they are consistent with the prominent dependency of the gamma, but not theta, band coherence on behavioral context (Fig. 3).…”

“…Air puff stimulation of the whiskers triggers reflexive protraction, the amplitude of which is correlated to cerebellar activity (Brown and Raman, 2018;Romano et al, 2018). This suggests an interaction between cerebellar activity, whisker protraction and wS1-wM1 coherence.…”

“…The direction of Purkinje cell modulation upon whisker stimulation is related to the location within crus 1 and crus 2 receiving the stimulus (Romano et al, 2018). More specifically, whereas the increase in simple spike firing is most prominent in medial crus 2, that of the complex spikes, which may facilitate execution of touch-induced whisker protraction, is more robust in lateral crus 1 (Romano et al, 2018).…”

“…Whisker stimulation triggers fast responses in wS1 and wM1 De Kock et al, 2007;Ferezou et al, 2007) as well as in the cerebellar cortex (Bosman et al, 2010;Brown and Raman, 2018;Romano et al, 2018). Before studying the impact of cerebellar stimulation on the cortical coherence between wS1 and wM1, we first needed to determine to what extent the individual cortical responses within wS1 and wM1 depended on cerebellar activity.…”

“…Even though the impact of cerebellar activity on cortical coherence is well established (Popa et al, 2013;Proville et al, 2014;Kros et al, 2015), it remains to be elucidated to what extent and how the cerebellum can differentially influence different frequency bands, to what extent such potentially different impacts depend on the behavioral context, and whether these differential effects are mediated through different cerebellar modules (Proske and Gandevia, 2009;De Zeeuw et al, 2011;Romano et al, 2018). Here, we set out to address these questions by investigating the impact of Purkinje cell activity on coherence between the whisker areas of the primary somatosensory (wS1) and motor cortex (wM1) during stimulation of the whiskers in awake behaving mice.…”