Beta‐gamma burst stimulations of the inferior olive induce high‐frequency oscillations in the deep cerebellar nuclei

Cheron, Julian; Chéron, Guy

doi:10.1111/ejn.13873

Cited by 8 publications

(5 citation statements)

References 83 publications

(99 reference statements)

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“…A first mechanism was hypothesized by Yarom (Jacobson et al, 2008; Chen et al, 2010) and involves DCN control of inferior olive (IO) oscillations that reverberate through climbing fibers into the DCN-PC-IO loop. Stimulus-induced oscillations similar to ours are indeed evident in the PSTH of DCN neurons following direct climbing fiber activation (Cheron and Cheron, 2018). A second mechanism hypothesized by De Zeeuw could involve signal reentry through extra-cerebellar circuits (Kistler and De Zeeuw, 2003; Gao et al, 2016) or through the more recently identified connections between DCN and granular layer (Ankri et al, 2015; Gao et al, 2016), therefore passing again through PCs.…”

Section: Discussionsupporting

confidence: 76%

“…We notice, however, that urethane is very conservative on the NMDA and GABA-A receptor-dependent mechanisms of neurotransmission and has been successfully used to demonstrate long-lasting changes at other cerebellar synapses in vivo (Roggeri et al, 2008; Ramakrishnan et al, 2016). Moreover, stimulus-induced oscillations in DCN neurons have been recently shown using ketamine-xylidodihydrothiazin anesthesia (Cheron and Cheron, 2018).…”

Section: Discussionmentioning

confidence: 99%

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Long-Lasting Response Changes in Deep Cerebellar Nuclei in vivo Correlate With Low-Frequency Oscillations

Moscato

Montagna

Propris³

et al. 2019

Front. Cell. Neurosci.

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The deep cerebellar nuclei (DCN) have been suggested to play a critical role in sensorimotor learning and some forms of long-term synaptic plasticity observed in vitro have been proposed as a possible substrate. However, till now it was not clear whether and how DCN neuron responses manifest long-lasting changes in vivo. Here, we have characterized DCN unit responses to tactile stimulation of the facial area in anesthetized mice and evaluated the changes induced by theta-sensory stimulation (TSS), a 4 Hz stimulation pattern that is known to induce plasticity in the cerebellar cortex in vivo. DCN units responded to tactile stimulation generating bursts and pauses, which reflected combinations of excitatory inputs most likely relayed by mossy fiber collaterals, inhibitory inputs relayed by Purkinje cells, and intrinsic rebound firing. Interestingly, initial bursts and pauses were often followed by stimulus-induced oscillations in the peri-stimulus time histograms (PSTH). TSS induced long-lasting changes in DCN unit responses. Spike-related potentiation and suppression (SR-P and SR-S), either in units initiating the response with bursts or pauses, were correlated with stimulus-induced oscillations. Fitting with resonant functions suggested the existence of peaks in the theta-band (burst SR-P at 9 Hz, pause SR-S at 5 Hz). Optogenetic stimulation of the cerebellar cortex altered stimulus-induced oscillations suggesting that Purkinje cells play a critical role in the circuits controlling DCN oscillations and plasticity. This observation complements those reported before on the granular and molecular layers supporting the generation of multiple distributed plasticities in the cerebellum following naturally patterned sensory entrainment. The unique dependency of DCN plasticity on circuit oscillations discloses a potential relationship between cerebellar learning and activity patterns generated in the cerebellar network.

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Section: Discussionsupporting

confidence: 76%

Section: Discussionmentioning

confidence: 99%

Long-Lasting Response Changes in Deep Cerebellar Nuclei in vivo Correlate With Low-Frequency Oscillations

Moscato

Montagna

Propris³

et al. 2019

Front. Cell. Neurosci.

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“…(2008) showed that the Purkinje cell layer produces 200 Hz oscillations in Wistar rats, which seem to entrain unit firing; high-frequency LFPs in the molecular and granule cell layers were far less pronounced. More recently, Cheron and Cheron (2018) found that stimulation of the inferior olive in mice induced high-frequency oscillations (350 Hz) in the cerebellum. Intracranial recordings from the human cerebellum are exceedingly rare, but Dalal et al.…”

Section: Why Is the Detection Of Cerebellar Activity With Eeg And Megmentioning

confidence: 99%

Can EEG and MEG detect signals from the human cerebellum?

2020

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The cerebellum plays a key role in the regulation of motor learning, coordination and timing, and has been implicated in sensory and cognitive processes as well. However, our current knowledge of its electrophysiological mechanisms comes primarily from direct recordings in animals, as investigations into cerebellar function in humans have instead predominantly relied on lesion, haemodynamic and metabolic imaging studies. While the latter provide fundamental insights into the contribution of the cerebellum to various cerebellar-cortical pathways mediating behaviour, they remain limited in terms of temporal and spectral resolution. In principle, this shortcoming could be overcome by monitoring the cerebellum’s electrophysiological signals. Non-invasive assessment of cerebellar electrophysiology in humans, however, is hampered by the limited spatial resolution of electroencephalography (EEG) and magnetoencephalography (MEG) in subcortical structures, i.e., deep sources. Furthermore, it has been argued that the anatomical configuration of the cerebellum leads to signal cancellation in MEG and EEG. Yet, claims that MEG and EEG are unable to detect cerebellar activity have been challenged by an increasing number of studies over the last decade. Here we address this controversy and survey reports in which electrophysiological signals were successfully recorded from the human cerebellum. We argue that the detection of cerebellum activity non-invasively with MEG and EEG is indeed possible and can be enhanced with appropriate methods, in particular using connectivity analysis in source space. We provide illustrative examples of cerebellar activity detected with MEG and EEG. Furthermore, we propose practical guidelines to optimize the detection of cerebellar activity with MEG and EEG. Finally, we discuss MEG and EEG signal contamination that may lead to localizing spurious sources in the cerebellum and suggest ways of handling such artefacts. This review is to be read as a perspective review that highlights that it is indeed possible to measure cerebellum with MEG and EEG and encourages MEG and EEG researchers to do so. Its added value beyond highlighting and encouraging is that it offers useful advice for researchers aspiring to investigate the cerebellum with MEG and EEG.

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“…These conflicting results might involve differences in the electrode positions; nevertheless, this has not been examined. However, previous studies have demonstrated that gamma band activity also occurs in the cerebellum (de Solages et al, 2008 ; Cheron and Cheron, 2018 ), and it plays a role in synchronization of the sensory and motor cortices (Popa et al, 2013 ). It has been reported that activity of the cerebellar cortex region is also important for movement tasks requiring motor control (Ehsani et al, 2016 ; Spampinato et al, 2017 ); if the neural network between M1 and the cerebellar cortex region does not function properly, exercise cannot be performed efficiently and smoothly.…”

Section: Introductionmentioning

confidence: 98%

Transcranial Alternating Current Stimulation With Gamma Oscillations Over the Primary Motor Cortex and Cerebellar Hemisphere Improved Visuomotor Performance

Miyaguchi

Otsuru

Kojima

et al. 2018

Front. Behav. Neurosci.

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Transcranial alternating current stimulation (tACS) can be used to modulate oscillatory brain activity. In this study, we investigated whether tACS applied over the primary motor cortex (M1) and cerebellar cortex region improved motor performance. We applied tACS (1.0 mA) to 20 healthy adults while they performed an isometric force task with some visuomotor control using their right index finger. Gamma (70 Hz) oscillations in the Experiment 1 or beta (20 Hz) oscillations in the Experiment 2 were applied for 30 s over the left M1, right cerebellar hemisphere or both regions (“M1-Cerebellum”), and errors performing the task were compared. Beta-oscillation tACS did not affect motor performance. With the gamma-oscillation tACS, a negative correlation was found between the difference of error in the M1-Cerebellum condition and the number of errors in the sham condition (P = 0.005, Pearson’s r = −0.597), indicating that motor performance improved with M1-Cerebellum tACS for subjects with low motor performance in the sham condition. Those who performed poorly in the sham condition made significantly fewer errors with M1-Cerebellum tACS (P = 0.004). Thus, for subjects with poorer motor performance, tACS with gamma oscillations applied over the M1 and contralateral cerebellar hemisphere improved their performance.

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Beta‐gamma burst stimulations of the inferior olive induce high‐frequency oscillations in the deep cerebellar nuclei

Cited by 8 publications

References 83 publications

Long-Lasting Response Changes in Deep Cerebellar Nuclei in vivo Correlate With Low-Frequency Oscillations

Long-Lasting Response Changes in Deep Cerebellar Nuclei in vivo Correlate With Low-Frequency Oscillations

Can EEG and MEG detect signals from the human cerebellum?

Transcranial Alternating Current Stimulation With Gamma Oscillations Over the Primary Motor Cortex and Cerebellar Hemisphere Improved Visuomotor Performance

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