Brief Report
Short and long-term motor skill learning in an accelerated rotarod training paradigm

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Abstract

Rodent models of motor skill learning include skilled forelimb reaching and acrobatic locomotor paradigms. This study characterizes motor skill learning in the accelerated rotarod task. Thirty Long–Evans rats (300–400 g) were trained on an accelerated rotarod (1 cm/s2) over eight consecutive sessions (=days, 20 trials each). Improvement in rotarod velocities mastered before falling off the rod was observed within and between sessions (plateau after five sessions). Intrasession improvement was incompletely retained at the beginning of the next day’s session. Over several training sessions, intrasession improvement diminished, suggesting a ceiling effect. After 1 week of pause, the rotarod skill was retained. Locomotor exercise in a running wheel for 30 min before the first rotarod session did not affect intrasession improvement. Running-wheel exposure for 6 days did not diminish the rate of rotarod skill learning (steepness of the learning curve) but improved overall performance (upward shift of curve). Video analysis of gait on the rotarod showed that rats developed a motor strategy by modifying their gait patterns during training. The data demonstrate that rotarod improvement is not the result of enhanced general locomotor ability or fitness, which are trained in the running wheel, but requires a change in the motor strategy to master the task. Accelerated rotarod training can be regarded a valid paradigm for motor skill learning over short (intrasession, minutes) and long time frames (intersession, days).

Introduction

Motor skill learning is a fundamental adaptive mechanism in human and animal life. Its significance for development as well as for recovery after brain injury is increasingly recognized (Halsband & Freund, 1993). Skills are acquired by training. Performance typically plateaus after a variable number of sessions depending on the complexity and the novelty of the task. Whereas complex skills require repetitive training sessions with intersession rest periods, simpler tasks, such as adjustments of force to external requirements, can be learned within one session (Muellbacher, Ziemann, Boroojerdi, Cohen, & Hallett, 2001; Witney, Vetter, & Wolpert, 2001). Like for non-motor learning (Genoux et al., 2002; Spear, 1978), spaced training is more efficient than continuous (massed) training (Hintzman, 1974).

Rodent models of motor learning include paradigms training a motor skill, i.e., a novel sequence of movements (Kleim, Barbay, & Nudo, 1998), and tasks that train cued reactions consisting of common or simple movements (Laubach, Wessberg, & Nicolelis, 2000). Whereas the latter aim at improving reaction times, skill training paradigms try to achieve greater movement precision through training. Skill paradigms for rodents are skilled forelimb reaching (Whishaw & Pellis, 1990) or acrobatic locomotor tasks (Kleim, Pipitone, Czerlanis, & Greenough, 1998; Klintsova, Goodlett, & Greenough, 2000).

The rotarod task is more commonly used for motor function assessment in animal models of disease (Hamm, Pike, O’Dell, Lyeth, & Jenkins, 1994; Mizoguchi, Yuzurihara, Ishige, Sasaki, & Tabira, 2002) than in studies of motor learning. It is an easily quantifiable test, in which animals maintain balance on a rotating rod with a diameter markedly smaller than their body length. Time to fall off the rod is recorded. Over several days of training rats improve in performance (Brandon et al., 1998). By adding constant acceleration, task complexity can be increased.

Here we characterize and compare improvement in rotarod performance within and between rotarod training sessions, and test whether improvement in rotarod performance reflects motor skill learning, i.e., learning of task-related motor strategies, or is a consequence of unspecific locomotor training or physical exercise.

Section snippets

Materials and methods

Thirty male Long–Evans adult rats (8–10-weeks-old or 300–400 g) were used in this study. Rats were kept in a 12/12 h light cycle with ad libido access to food and water. Motor training was performed at the beginning of the dark phase of the daily cycle. Body weight was recorded daily. All procedures were approved by the Animal Care and Use Committee of the University of Tübingen.

Experiment 1

Rotarod performance improved within sessions (intrasession) and between sessions (intersession). At the beginning of a session, animals typically did not reach the performance levels achieved at the end of the preceding session (Fig. 1A). Intersession improvement was highest between sessions 1 and 3 and reached a plateau after session 5 (Fig. 1B). Intrasession as well as intersession (average of 20 trials) improvement followed an asymptotic course and was approximated by an exponential equation

Discussion

The findings demonstrate that rotarod training leads to short- and long-term improvement in performance. Short-term improvement occurs over repeated running trials within one session (20 trails over 20–30 min, intrasession). Long-term improvement (intersession) develops over 4–6 days with rest periods in between sessions. During later training sessions, intrasession improvement diminishes. Prior training on an activity wheel does neither affect the rate of intrasession nor the rate of

Acknowledgements

This work was supported by a grant from the Deutsche Forschungsgemeinschaft (Lu 748/3). We thank Drs. Richard Macko and Patrick De Deyne, University of Maryland, Baltimore, for their advice and discussion.

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