Roles of the cerebellum and basal ganglia in temporal integration: Insights from a synchronized tapping task

Shin-Ichi Tokushige; Shunichi Matsuda; Masayoshi Tada; Ichiro Yabe; Atsushi Takeda; Hiroyasu Tanaka; Megumi Hatakenaka; Hiroyuki Enomoto; Shunsuke Kobayashi; Kazutaka Shimizu; Takahiro Shimizu; Naoki Kotsuki; Satomi Inomata-Terada; Toshiaki Furubayashi; Yaeko Ichikawa; Ritsuko Hanajima; Shoji Tsuji; Yoshikazu Ugawa; Yasuo Terao

doi:10.1016/j.clinph.2023.11.018

Roles of the cerebellum and basal ganglia in temporal integration: Insights from a synchronized tapping task

Clin Neurophysiol. 2024 Feb:158:1-15. doi: 10.1016/j.clinph.2023.11.018. Epub 2023 Dec 1.

Authors

Shin-Ichi Tokushige¹, Shunichi Matsuda², Masayoshi Tada³, Ichiro Yabe⁴, Atsushi Takeda⁵, Hiroyasu Tanaka⁵, Megumi Hatakenaka⁶, Hiroyuki Enomoto⁷, Shunsuke Kobayashi⁸, Kazutaka Shimizu⁹, Takahiro Shimizu¹⁰, Naoki Kotsuki¹¹, Satomi Inomata-Terada¹², Toshiaki Furubayashi¹³, Yaeko Ichikawa¹¹, Ritsuko Hanajima⁹, Shoji Tsuji¹⁴, Yoshikazu Ugawa¹⁵, Yasuo Terao¹⁶

Affiliations

¹ Department of Neurology, Graduate School of Medicine, the University of Tokyo, 7-3-1, Hongo, Bunkyo-ku, Tokyo 113-8655, Japan; Department of Neurology, Faculty of Medicine, Kyorin University, 6-20-2 Shinkawa, Mitaka-shi, Tokyo 181-8611, Japan.
² Department of Neurology, Graduate School of Medicine, the University of Tokyo, 7-3-1, Hongo, Bunkyo-ku, Tokyo 113-8655, Japan.
³ Department of Neurology, Brain Research Institute, Niigata University, 1-757 Asahimachidori, Chuo-ku, Niigata 951-8585, Japan.
⁴ Department of Neurology, Faculty of Medicine and Graduate School of Medicine, Hokkaido University, Kita 15, Nishi 7, Kita-ku, Sapporo 060-8638, Japan.
⁵ Department of Neurology, Sendai Nishitaga Hospital, 2-11-11, Kagitori-honcho, Taihaku-ku, Sendai 982-8555, Japan.
⁶ Department of Neurology, Morinomiya Hospital, 2-1-88, Morinomiya, Joto-ku, Osaka 536-0025, Japan.
⁷ Department of Neurology, Faculty of Medicine, Fukushima Medical University, 1 Hikarigaoka, Fukushima 960-1295, Japan.
⁸ Department of Neurology, Teikyo University School of Medicine, 2-11-1 Kaga, Itabashi-Ku, Tokyo 173-8606, Japan.
⁹ Division of Neurology, Department of Brain and Neurosciences, Faculty of Medicine, Tottori University, 36-1, Nishicho, Yonago, Tottori 683-8504, Japan.
¹⁰ Department of Neurology, Kitasato University School of Medicine, 1-15-1, Kitazato, Minami, Sagamihara, Kanagawa 252-0375, Japan.
¹¹ Department of Neurology, Faculty of Medicine, Kyorin University, 6-20-2 Shinkawa, Mitaka-shi, Tokyo 181-8611, Japan.
¹² Department of Medical Physiology, School of Medicine, Kyorin University, 6-20-2, Shinkawa, Mitaka, Tokyo 181-8611, Japan.
¹³ Graduate School of Health and Environment Science, Tohoku Bunka Gakuen University, 6-45-1 Kunimi, Sendai, Miyagi 981-8551, Japan.
¹⁴ Department of Molecular Neurology, the University of Tokyo and International University of Health and Welfare, 4-3, Kozunomori, Narita-shi, Chiba-ken 286-8686, Japan.
¹⁵ Department of Human Neurophysiology, Fukushima Medical University, 1 Hikarigaoka, Fukushima 960-1295, Japan.
¹⁶ Department of Neurology, Graduate School of Medicine, the University of Tokyo, 7-3-1, Hongo, Bunkyo-ku, Tokyo 113-8655, Japan; Department of Medical Physiology, School of Medicine, Kyorin University, 6-20-2, Shinkawa, Mitaka, Tokyo 181-8611, Japan. Electronic address: yterao@ks.kyorin-u.ac.jp.

PMID: 38113692
DOI: 10.1016/j.clinph.2023.11.018

Abstract

Objective: The aim of this study was to clarify the roles of the cerebellum and basal ganglia for temporal integration.

Methods: We studied 39 patients with spinocerebellar degeneration (SCD), comprising spinocerebellar atrophy 6 (SCA6), SCA31, Machado-Joseph disease (MJD, also called SCA3), and multiple system atrophy (MSA). Thirteen normal subjects participated as controls. Participants were instructed to tap on a button in synchrony with isochronous tones. We analyzed the inter-tap interval (ITI), synchronizing tapping error (STE), negative asynchrony, and proportion of delayed tapping as indicators of tapping performance.

Results: The ITI coefficient of variation was increased only in MSA patients. The standard variation of STE was larger in SCD patients than in normal subjects, especially for MSA. Negative asynchrony, which is a tendency to tap the button before the tones, was prominent in SCA6 and MSA patients, with possible basal ganglia involvement. SCA31 patients exhibited normal to supranormal performance in terms of the variability of STE, which was surprising.

Conclusions: Cerebellar patients generally showed greater STE variability, except for SCA31. The pace of tapping was affected in patients with possible basal ganglia pathology.

Significance: Our results suggest that interaction between the cerebellum and the basal ganglia is essential for temporal processing. The cerebellum and basal ganglia and their interaction regulate synchronized tapping, resulting in distinct tapping pattern abnormalities among different SCD subtypes.

Keywords: Basal ganglia; Cerebellum; Spinocerebellar degeneration; Synchronized tapping task; Temporal processing.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Basal Ganglia / pathology
Cerebellum
Humans
Multiple System Atrophy*
Spinocerebellar Ataxias* / pathology
Spinocerebellar Degenerations*

Supplementary concepts

Spinocerebellar Ataxia 31