State-dependent entrainment of cerebellar nuclear neurons to the local field potential during voluntary movements

Abstract

Understanding the relationship between the local field potential (LFP) and single neurons is essential if we are to understand network dynamics and the entrainment of neuronal activity. Here, we investigated the interaction between the LFP and single neurons recorded in the rat cerebellar nuclei (CN), which are part of the sensorimotor network, in freely moving rats. During movement, the LFP displayed persistent oscillations in the theta band frequency whereas CN neurons displayed intermittent oscillations in the same frequency band contingent on the instantaneous LFP power; the neurons oscillated primarily when the concurrent LFP power was either high or low. Quantification of the relative instantaneous frequency and phase locking showed that CN neurons exhibited phase locked rhythmic activity at a frequency similar to that of the LFP or at a shifted frequency during high and low LFP power, respectively. We suggest that this nonlinear interaction between cerebellar neurons and the LFP power, which occurs solely during movement, contributes to the shaping of cerebellar output patterns.

Chemical suppression of harmaline-induced body tremor yields recovery of pairwise neuronal coherence in cerebellar nuclei neurons

“…We showed elsewhere that during voluntary movement, CN neurons tend to oscillate intermittently in the theta band frequency ( Baumel and Cohen, 2021 ; Baumel et al, 2021 ) and that the oscillation characteristics are significantly altered after the induction of body tremor by harmaline ( Baumel et al, 2021 ). Figures 2A–C shows example spectrograms and the corresponding power spectra of CN neurons that oscillated in the theta band frequency in the control ( Figure 2A ), Harm ( Figure 2B ), and Harm+NNC ( Figure 2C ) conditions.…”

“…We previously showed that during voluntary movement, CN neurons display intermittent oscillations with a precise spectral structure ( Baumel and Cohen, 2021 ). This accurate spectral structure breaks down during the emergence of body tremor after harmaline administration ( Baumel et al, 2021 ).…”

“…The surgical procedures have been described elsewhere in Baumel et al (2009) , Jacobson et al (2009) , Baumel and Cohen (2021) . In brief, 18 rats were initially sedated by 5% isoflurane and then injected intramuscularly with ketamine HCl and xylazine HCl (100 and 10 mg/kg, respectively).…”

“…In a study on freely moving rats we previously reported that CN neurons display highly coherent oscillations during repetitive and non-repetitive voluntary movements ( Baumel and Cohen, 2021 ; Baumel et al, 2021 ). We also showed that concomitantly with the emergence of body tremor, harmaline enhanced rhythmic activity in single CN neurons; however, the spectral structure of the oscillations was impaired, causing loss of coherence in the majority of simultaneously recorded neuronal pairs ( Baumel et al, 2021 ).…”

Cerebello-Thalamo-Cortical Network Dynamics in the Harmaline Rodent Model of Essential Tremor

“…We also observed a ~7–8 Hz oscillations during pre-harmaline control conditions in motor thalamus LFP when rats were moving and not resting. A recent study by Baumel and Cohen ( 2021 ) demonstrated that a 7–8 Hz theta oscillation in the cerebellar nuclei was higher in power when the animals were moving compared to rest. Therefore, cerebellar output during movement may shape thalamic oscillations and may account for the intrinsic movement related cerebellar nuclear oscillations that we observed, although the functional relevance of this interaction is unknown.…”