Elsevier

Neural Networks

Volume 47, November 2013, Pages 72-80
Neural Networks

2013 Special Issue
Transfer of memory trace of cerebellum-dependent motor learning in human prism adaptation: A model study

https://doi.org/10.1016/j.neunet.2013.01.017Get rights and content

Abstract

Accumulating experimental evidence suggests that the memory trace of ocular reflex adaptation is initially encoded in the cerebellar cortex, and later transferred to the cerebellar nuclei for consolidation through repetitions of training. However, the memory transfer is not well characterized in the learning of voluntary movement. Here, we implement our model of memory transfer to interpret the data of prism adaptation (Martin et al., 1996a, Martin et al., 1996b), assuming that the cerebellar nuclear memory formed by memory transfer is used for normal throwing. When the subject was trained to throw darts wearing prisms in 30–40 trials, the short-term memory for recalibrating the throwing direction by gaze would be formed in the cerebellar cortex, which was extinguished by throwing with normal vision in a similar number of trials. After weeks of repetitions of short-term prism adaptation, the long-term memory would be formed in the cerebellar nuclei through memory transfer, which enabled one to throw darts to the center wearing prisms without any training. These two long-term memories, one for throwing with normal vision and the other for throwing wearing prisms, are assumed to be utilized automatically under volitional control. Moreover, when the prisms were changed to new prisms, a new memory for adapting to the new prisms would be formed in the cerebellar cortex, just to counterbalance the nuclear memory of long-term adaptation to the original prisms in a similar number of trials. These results suggest that memory transfer may occur in the learning of voluntary movements.

Introduction

The gain adaptation of the vestibulo-ocular reflex (VOR) and optokinetic response (OKR), as well as the delayed eyelid conditioning, provides an experimental paradigm of cerebellum-dependent motor learning (e.g.  Ito, 1984, Ito, 2001, Ito, 2011). Although both VOR and OKR are driven by the relatively simple neural network composed of the cerebellar flocculus and vestibular nuclei (Fig. 1), the site of the memory trace of adaptation was an issue of debate for over twenty years (Melvill-Jones, 2000). Now, the multiple distribution of the memory trace of adaptation, which was originally proposed conceptually (Galiana, 1986, Quinn et al., 1998, Raymond and Lisberger, 1996), has been supported by studies of the adaptation of mouse OKR (Okamoto et al., 2011a, Shutoh et al., 2006), and cat (Kassardjian et al., 2005) and monkey (Anzai et al., 2010, Nagao and Kitazawa, 2003) VOR. These experimental studies consistently suggest that the memory trace of adaptation is initially encoded in the cerebellar cortex, and later is transferred outside the cerebellar cortex after repetitions of training. The most likely site for the storage of long-term adaption of VOR/OKR is now assumed to be within the cerebellar (vestibular) nuclei (VN, Fig. 1). Recent computational studies have also supported such a training-history-dependent memory transfer in delayed eyelid conditioning (Ohyama, Nores, Medina, Riusech, & Mauk, 2006) and adaptation of ocular reflexes (Masuda and Amari, 2008, Yamazaki and Nagao, submitted for publication). However, whether memory transfer may occur in the learning of voluntary movements has not been clarified.

Several experimental paradigms have been developed to study the learning of human voluntary movement. Thomas Thach and his colleagues have developed a paradigm of throwing darts while viewing the target through prisms (Martin et al., 1996a, Martin et al., 1996b), also see Thach, Goodkin, and Keating (1992). In their study, when a subject threw darts wearing left-shifting prisms, initially the subject threw darts leftward, but soon recalibrated the throwing direction by gaze and threw darts to the center of the target. This short-term prism adaptation is considered to be dependent on cerebellar learning, because it is impaired in patients with cerebellar disease, most profoundly in the patient with lesions restricted to the inferior olive (Martin et al., 1996a). Monkey lesion (Baizer, Kralj-Hans, & Glickstein, 1999) and pharmacological inactivation (Norris, Hathaway, Taylor, & Thach, 2011) studies have also suggested that the cerebellum plays an essential role in prism adaptation. Interestingly, when a subject was trained to throw darts wearing the prisms repetitively for 3 months, a long-term prism adaptation occurred and the subject became able to throw darts to the center in the first trial even when wearing prisms (Martin et al., 1996b). We implemented our model (Yamazaki & Nagao, submitted for publication), in which the memories of short- and long-term adaptations are respectively formed in the cerebellar cortex and CN, to the data of Martin et al., 1996a, Martin et al., 1996b. We assume that the memory formed in CN through the memory transfer is robust and keeps much longer than the memory formed in the cerebellar cortex by short-term adaptation, so that we consider that the memory formed in CN is used for normal throwing. We interpreted some of the behavioral observations as being due to the cooperation of memories formed in the cerebellar cortex and CN. Results of our model study suggest that memory transfer may occur in the learning of voluntary movements which is controlled by cerebro-cerebellar networks.

Section snippets

Behavioral characteristics of short- and long-term prism adaptation

Fig. 2(a) shows the time course of short-term prism adaptation in the study by Martin et al. (1996a). In their experiment, the subject threw darts wearing 50 cm-left-shifting prisms (L-prisms). Initially, the subject threw darts 50 cm leftward from the center of the target. After 30–40 trials of dart throwing wearing L-prisms, the subject learned to throw darts to the center. After the completion of adaptation to L-prisms, the subject took off the L-prisms and threw darts. The dart shifted

Summary

We used our model of training history-dependent transfer of the memory trace of motor learning from the cerebellar cortex to CN to interpret the throwing movements observed in prism adaptation experiments by Martin et al., 1996a, Martin et al., 1996b. The model consists of the neural network of the cerebellar cortex and CN, which respectively contain the memory of short- and long-term prism adaptation. We assume that the long-term memory for throwing darts with normal vision is formed in CN

Conclusions

We suggest a model for the prism adaptation of the throwing movement in humans. In our model, the initial memory of prism adaptation induced by 30–40 trials is encoded in the cerebellar cortex, which is transferred to CN after 20–30 repetitions of adaptation. The memory formed in the cerebellar cortex is labile, whereas that formed in CN is solid, and both memories work additively. Moreover, the memory in the cerebellar cortex may be formed and extinguished independently of the memory

Acknowledgments

We thank Dr. Masao Ito (RIKEN Brain Science Institute, Wako, Saitama, Japan) for his critical reading of our manuscript. This work was supported by a Grant-in-Aid from the Japanese Society for the Promotion of Science (No. 22300112) and research funds of RIKEN.

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