Quantitative evaluation of human cerebellum-dependent motor learning through prism adaptation of hand-reaching movement.

Ken Matsumura,Kazumasa Soga,Kazuhiko Katano,Hidehiro Mizusawa,Kinya Ishikawa,Yuji Hashimoto,Takanori Yokota,Lutz Jaencke,Soichi Nagao,Makoto Nakao,Takeru Honda

doi:10.1371/journal.pone.0119376

Abstract

The cerebellum plays important roles in motor coordination and learning. However, motor learning has not been quantitatively evaluated clinically. It thus remains unclear how motor learning is influenced by cerebellar diseases or aging, and is related with incoordination. Here, we present a new application for testing human cerebellum-dependent motor learning using prism adaptation. In our paradigm, the participant wearing prism-equipped goggles touches their index finger to the target presented on a touchscreen in every trial. The whole test consisted of three consecutive sessions: (1) 50 trials with normal vision (BASELINE), (2) 100 trials wearing the prism that shifts the visual field 25° rightward (PRISM), and (3) 50 trials without the prism (REMOVAL). In healthy subjects, the prism-induced finger-touch error, i.e., the distance between touch and target positions, was decreased gradually by motor learning through repetition of trials. We found that such motor learning could be quantified using the “adaptability index (AI)”, which was calculated by multiplying each probability of [acquisition in the last 10 trials of PRISM], [retention in the initial five trials of REMOVAL], and [extinction in the last 10 trials of REMOVAL]. The AI of cerebellar patients less than 70 years old (mean, 0.227; n = 62) was lower than that of age-matched healthy subjects (0.867, n = 21; p < 0.0001). While AI did not correlate with the magnitude of dysmetria in ataxic patients, it declined in parallel with disease progression, suggesting a close correlation between the impaired cerebellar motor leaning and the dysmetria. Furthermore, AI decreased with aging in the healthy subjects over 70 years old compared with that in the healthy subjects less than 70 years old. We suggest that our paradigm of prism adaptation may allow us to quantitatively assess cerebellar motor learning in both normal and diseased conditions.

Highlights

The cerebellum plays an important role in motor control [1]
Taking advantage of the fact that the hand-reaching task is very simple, we succeeded in developing a paradigm for quantitatively assessing the cerebellum-dependent motor learning in almost any individual by performing 200 trials within only 20–30 minutes with a relatively cheap and compact system (S2 Table)
A novel neurological biomarker (AI), which reflects acquisition, retention, and extinction of the prism adaptation of hand-reaching movement, was lower and its variability was larger in patients with cerebellar diseases than those in the age-matched healthy subjects

Summary

Introduction

The cerebellum plays an important role in motor control [1]. Experimental studies using adaptation of ocular reflexes and eyeblink conditioning have consistently suggested that the cerebellum controls gain and timing of movements through learning [1,2,3]. Patients with cerebellar diseases exhibit signs of ataxia that include imbalance and incoordination [4, 5], as well as impaired motor learning, which has been revealed with the paradigms of eyeblink conditioning [6,7,8], adaptation of ocular reflexes [9, 10], and adaptation of forelimb movements [11,12,13,14,15]. We propose that the adaptability index (AI), calculated on the basis of the data obtained using our paradigm, as a sensitive marker of human cerebellar motor learning for the practical diagnosis of cerebellar diseases

Participants

Results

Discussion