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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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Autores principales: Baumel, Yuval, Yamin, Hagar Grazya, Cohen, Dana
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10211344/
https://www.ncbi.nlm.nih.gov/pubmed/37251003
http://dx.doi.org/10.3389/fnsys.2023.1135799
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author Baumel, Yuval
Yamin, Hagar Grazya
Cohen, Dana
author_facet Baumel, Yuval
Yamin, Hagar Grazya
Cohen, Dana
author_sort Baumel, Yuval
collection PubMed
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 pubmed-102113442023-05-26 Chemical suppression of harmaline-induced body tremor yields recovery of pairwise neuronal coherence in cerebellar nuclei neurons Baumel, Yuval Yamin, Hagar Grazya Cohen, Dana Front Syst Neurosci Neuroscience 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. Frontiers Media S.A. 2023-05-11 /pmc/articles/PMC10211344/ /pubmed/37251003 http://dx.doi.org/10.3389/fnsys.2023.1135799 Text en Copyright © 2023 Baumel, Yamin and Cohen. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Neuroscience
Baumel, Yuval
Yamin, Hagar Grazya
Cohen, Dana
Chemical suppression of harmaline-induced body tremor yields recovery of pairwise neuronal coherence in cerebellar nuclei neurons
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 Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10211344/
https://www.ncbi.nlm.nih.gov/pubmed/37251003
http://dx.doi.org/10.3389/fnsys.2023.1135799
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