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

Neuronal oscillations occur in health and disease; however, their characteristics can differ across conditions. During voluntary movement in freely moving rats, cerebellar nuclei (CN) neurons display intermittent but coherent oscillations in the theta frequency band (4–12 Hz). However, in the rat ha...

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Main Authors: Yuval Baumel, Hagar Grazya Yamin, Dana Cohen
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-05-01
Series:Frontiers in Systems Neuroscience
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fnsys.2023.1135799/full
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author Yuval Baumel
Hagar Grazya Yamin
Dana Cohen
author_facet Yuval Baumel
Hagar Grazya Yamin
Dana Cohen
author_sort Yuval Baumel
collection DOAJ
description Neuronal oscillations occur in health and disease; however, their characteristics can differ across conditions. During voluntary movement in freely moving rats, cerebellar nuclei (CN) neurons display intermittent but coherent oscillations in the theta frequency band (4–12 Hz). However, in the rat harmaline model of essential tremor, a disorder attributed to cerebellar malfunction, CN neurons display aberrant oscillations concomitantly with the emergence of body tremor. To identify the oscillation features that may underlie the emergence of body tremor, we analyzed neuronal activity recorded chronically from the rat CN under three conditions: in freely behaving animals, in harmaline-treated animals, and during chemical suppression of the harmaline-induced body tremor. Suppression of body tremor did not restore single neuron firing characteristics such as firing rate, the global and local coefficients of variation, the likelihood of a neuron to fire in bursts or their tendency to oscillate at a variety of dominant frequencies. Similarly, the fraction of simultaneously recorded neuronal pairs oscillating at a similar dominant frequency (<1 Hz deviation) and the mean frequency deviation within pairs remained similar to the harmaline condition. Moreover, the likelihood that pairs of CN neurons would co-oscillate was not only significantly lower than that measured in freely moving animals, but was significantly worse than chance. By contrast, the chemical suppression of body tremor fully restored pairwise neuronal coherence; that is, unlike in the harmaline condition, pairs of neurons that oscillated at the same time and frequency displayed high coherence, as in the controls. We suggest that oscillation coherence in CN neurons is essential for the execution of smooth movement and its loss likely underlies the emergence of body tremor.
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spelling doaj.art-e372e00d98c545fda8ff83ce15139fff2023-05-11T14:33:42ZengFrontiers Media S.A.Frontiers in Systems Neuroscience1662-51372023-05-011710.3389/fnsys.2023.11357991135799Chemical suppression of harmaline-induced body tremor yields recovery of pairwise neuronal coherence in cerebellar nuclei neuronsYuval BaumelHagar Grazya YaminDana CohenNeuronal oscillations occur in health and disease; however, their characteristics can differ across conditions. During voluntary movement in freely moving rats, cerebellar nuclei (CN) neurons display intermittent but coherent oscillations in the theta frequency band (4–12 Hz). However, in the rat harmaline model of essential tremor, a disorder attributed to cerebellar malfunction, CN neurons display aberrant oscillations concomitantly with the emergence of body tremor. To identify the oscillation features that may underlie the emergence of body tremor, we analyzed neuronal activity recorded chronically from the rat CN under three conditions: in freely behaving animals, in harmaline-treated animals, and during chemical suppression of the harmaline-induced body tremor. Suppression of body tremor did not restore single neuron firing characteristics such as firing rate, the global and local coefficients of variation, the likelihood of a neuron to fire in bursts or their tendency to oscillate at a variety of dominant frequencies. Similarly, the fraction of simultaneously recorded neuronal pairs oscillating at a similar dominant frequency (<1 Hz deviation) and the mean frequency deviation within pairs remained similar to the harmaline condition. Moreover, the likelihood that pairs of CN neurons would co-oscillate was not only significantly lower than that measured in freely moving animals, but was significantly worse than chance. By contrast, the chemical suppression of body tremor fully restored pairwise neuronal coherence; that is, unlike in the harmaline condition, pairs of neurons that oscillated at the same time and frequency displayed high coherence, as in the controls. We suggest that oscillation coherence in CN neurons is essential for the execution of smooth movement and its loss likely underlies the emergence of body tremor.https://www.frontiersin.org/articles/10.3389/fnsys.2023.1135799/fullcerebellumtremoroscillationsharmalinesynchronychronic recordings
spellingShingle Yuval Baumel
Hagar Grazya Yamin
Dana Cohen
Chemical suppression of harmaline-induced body tremor yields recovery of pairwise neuronal coherence in cerebellar nuclei neurons
Frontiers in Systems Neuroscience
cerebellum
tremor
oscillations
harmaline
synchrony
chronic recordings
title Chemical suppression of harmaline-induced body tremor yields recovery of pairwise neuronal coherence in cerebellar nuclei neurons
title_full Chemical suppression of harmaline-induced body tremor yields recovery of pairwise neuronal coherence in cerebellar nuclei neurons
title_fullStr Chemical suppression of harmaline-induced body tremor yields recovery of pairwise neuronal coherence in cerebellar nuclei neurons
title_full_unstemmed Chemical suppression of harmaline-induced body tremor yields recovery of pairwise neuronal coherence in cerebellar nuclei neurons
title_short Chemical suppression of harmaline-induced body tremor yields recovery of pairwise neuronal coherence in cerebellar nuclei neurons
title_sort chemical suppression of harmaline induced body tremor yields recovery of pairwise neuronal coherence in cerebellar nuclei neurons
topic cerebellum
tremor
oscillations
harmaline
synchrony
chronic recordings
url https://www.frontiersin.org/articles/10.3389/fnsys.2023.1135799/full
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