Cargando…

Discrimination and learning of temporal input sequences in a cerebellar Purkinje cell model

INTRODUCTION: Temporal information processing is essential for sequential contraction of various muscles with the appropriate timing and amplitude for fast and smooth motor control. These functions depend on dynamics of neural circuits, which consist of simple neurons that accumulate incoming spikes...

Descripción completa

Detalles Bibliográficos
Autores principales: Tamura, Kaaya, Yamamoto, Yuki, Kobayashi, Taira, Kuriyama, Rin, Yamazaki, Tadashi
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9932327/
https://www.ncbi.nlm.nih.gov/pubmed/36816857
http://dx.doi.org/10.3389/fncel.2023.1075005
_version_ 1784889432087724032
author Tamura, Kaaya
Yamamoto, Yuki
Kobayashi, Taira
Kuriyama, Rin
Yamazaki, Tadashi
author_facet Tamura, Kaaya
Yamamoto, Yuki
Kobayashi, Taira
Kuriyama, Rin
Yamazaki, Tadashi
author_sort Tamura, Kaaya
collection PubMed
description INTRODUCTION: Temporal information processing is essential for sequential contraction of various muscles with the appropriate timing and amplitude for fast and smooth motor control. These functions depend on dynamics of neural circuits, which consist of simple neurons that accumulate incoming spikes and emit other spikes. However, recent studies indicate that individual neurons can perform complex information processing through the nonlinear dynamics of dendrites with complex shapes and ion channels. Although we have extensive evidence that cerebellar circuits play a vital role in motor control, studies investigating the computational ability of single Purkinje cells are few. METHODS: We found, through computer simulations, that a Purkinje cell can discriminate a series of pulses in two directions (from dendrite tip to soma, and from soma to dendrite), as cortical pyramidal cells do. Such direction sensitivity was observed in whatever compartment types of dendrites (spiny, smooth, and main), although they have dierent sets of ion channels. RESULTS: We found that the shortest and longest discriminable sequences lasted for 60 ms (6 pulses with 10 ms interval) and 4,000 ms (20 pulses with 200 ms interval), respectively. and that the ratio of discriminable sequences within the region of the interesting parameter space was, on average, 3.3% (spiny), 3.2% (smooth), and 1.0% (main). For the direction sensitivity, a T-type Ca(2+) channel was necessary, in contrast with cortical pyramidal cells that have N-methyl-D-aspartate receptors (NMDARs). Furthermore, we tested whether the stimulus direction can be reversed by learning, specifically by simulated long-term depression, and obtained positive results. DISCUSSION: Our results show that individual Purkinje cells can perform more complex information processing than is conventionally assumed for a single neuron, and suggest that Purkinje cells act as sequence discriminators, a useful role in motor control and learning.
format Online
Article
Text
id pubmed-9932327
institution National Center for Biotechnology Information
language English
publishDate 2023
publisher Frontiers Media S.A.
record_format MEDLINE/PubMed
spelling pubmed-99323272023-02-17 Discrimination and learning of temporal input sequences in a cerebellar Purkinje cell model Tamura, Kaaya Yamamoto, Yuki Kobayashi, Taira Kuriyama, Rin Yamazaki, Tadashi Front Cell Neurosci Cellular Neuroscience INTRODUCTION: Temporal information processing is essential for sequential contraction of various muscles with the appropriate timing and amplitude for fast and smooth motor control. These functions depend on dynamics of neural circuits, which consist of simple neurons that accumulate incoming spikes and emit other spikes. However, recent studies indicate that individual neurons can perform complex information processing through the nonlinear dynamics of dendrites with complex shapes and ion channels. Although we have extensive evidence that cerebellar circuits play a vital role in motor control, studies investigating the computational ability of single Purkinje cells are few. METHODS: We found, through computer simulations, that a Purkinje cell can discriminate a series of pulses in two directions (from dendrite tip to soma, and from soma to dendrite), as cortical pyramidal cells do. Such direction sensitivity was observed in whatever compartment types of dendrites (spiny, smooth, and main), although they have dierent sets of ion channels. RESULTS: We found that the shortest and longest discriminable sequences lasted for 60 ms (6 pulses with 10 ms interval) and 4,000 ms (20 pulses with 200 ms interval), respectively. and that the ratio of discriminable sequences within the region of the interesting parameter space was, on average, 3.3% (spiny), 3.2% (smooth), and 1.0% (main). For the direction sensitivity, a T-type Ca(2+) channel was necessary, in contrast with cortical pyramidal cells that have N-methyl-D-aspartate receptors (NMDARs). Furthermore, we tested whether the stimulus direction can be reversed by learning, specifically by simulated long-term depression, and obtained positive results. DISCUSSION: Our results show that individual Purkinje cells can perform more complex information processing than is conventionally assumed for a single neuron, and suggest that Purkinje cells act as sequence discriminators, a useful role in motor control and learning. Frontiers Media S.A. 2023-02-02 /pmc/articles/PMC9932327/ /pubmed/36816857 http://dx.doi.org/10.3389/fncel.2023.1075005 Text en Copyright © 2023 Tamura, Yamamoto, Kobayashi, Kuriyama and Yamazaki. 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 Cellular Neuroscience
Tamura, Kaaya
Yamamoto, Yuki
Kobayashi, Taira
Kuriyama, Rin
Yamazaki, Tadashi
Discrimination and learning of temporal input sequences in a cerebellar Purkinje cell model
title Discrimination and learning of temporal input sequences in a cerebellar Purkinje cell model
title_full Discrimination and learning of temporal input sequences in a cerebellar Purkinje cell model
title_fullStr Discrimination and learning of temporal input sequences in a cerebellar Purkinje cell model
title_full_unstemmed Discrimination and learning of temporal input sequences in a cerebellar Purkinje cell model
title_short Discrimination and learning of temporal input sequences in a cerebellar Purkinje cell model
title_sort discrimination and learning of temporal input sequences in a cerebellar purkinje cell model
topic Cellular Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9932327/
https://www.ncbi.nlm.nih.gov/pubmed/36816857
http://dx.doi.org/10.3389/fncel.2023.1075005
work_keys_str_mv AT tamurakaaya discriminationandlearningoftemporalinputsequencesinacerebellarpurkinjecellmodel
AT yamamotoyuki discriminationandlearningoftemporalinputsequencesinacerebellarpurkinjecellmodel
AT kobayashitaira discriminationandlearningoftemporalinputsequencesinacerebellarpurkinjecellmodel
AT kuriyamarin discriminationandlearningoftemporalinputsequencesinacerebellarpurkinjecellmodel
AT yamazakitadashi discriminationandlearningoftemporalinputsequencesinacerebellarpurkinjecellmodel