Trends in Cognitive Sciences
Volume 2, Issue 9, 1 September 1998, Pages 313-321
Journal home page for Trends in Cognitive Sciences

Cerebellar learning in the vestibulo–ocular reflex

https://doi.org/10.1016/S1364-6613(98)01222-4Get rights and content

Abstract

The vestibulo–ocular reflex, because of its close relationship with the cerebellum and its marked adaptiveness, has become a model system for studying the functions of the cerebellum. It has been hypothesized that an evolutionarily old part of the cerebellum, the flocculus, forms a modifiable accessory pathway for the vestibulo–ocular reflex arc for adaptive control, and that the modification is due to the synaptic plasticity induced by retinal errors conveyed by a unique structure of the cerebellum, the climbing fibers. The flocculus hypothesis has been supported by several lines of evidence, including lesioning or functionally impairing the flocculus and recording the activity of flocculus Purkinje cells, and, more recently, from pharmacologically or genetically inhibited synaptic plasticity, which produces long-term depression. There has also been debate on a possible site for memory retention in vestibulo–ocular-reflex adaptation, and about the signal content in flocculus Purkinje cells. This article reviews recent studies on the learning mechanisms of the cerebellum that underlie the adaptation of the vestibulo–ocular reflex.

Section snippets

The neuronal circuit for the VOR–flocculus system

Of the many component pathways of the VOR arc operating under the influences of the flocculus[7], that serving the horizontal VOR is illustrated in Fig. 1. The horizontal semicircular canals are stimulated by ipsilateral head rotations (as indicated by broken arrows in Fig. 1 for the left horizontal canal). The stimulated horizontal semicircular canal on either side of the head sends neural signals via the primary vestibular nerve fibers to the relay cells of the VOR located in the vestibular

The VOR and its adaptation

In laboratory experiments, the horizontal VOR is induced by sinusoidal or velocity-step head rotation, and the VOR gain is measured as the ratio of the attained eye velocity to the applied head velocity. Using sinusoidal rotation is convenient for measuring the gain and phase of the VOR separately, while velocity steps enable us to separate components of VOR responses, which arise with different latencies. The measurement of the VOR is performed in the dark or with the eyes closed, in order to

Evidence for the flocculus hypothesis

The first lines of evidence in support of the flocculus hypothesis were derived by lesioning the flocculus or impairing its function. VOR adaptation no longer occurs after surgical ablation of, or the injection of toxic amino acids into, the flocculus in cats[28], rabbits29, 30, monkeys[31]and goldfish32, 33. Microdialysis of lidocaine into the goldfish cerebellum blocked both adaptive increase and decrease of VOR gain[34]. Interruption of the climbing-fiber input to the flocculus reproduced

Debate 1: Memory site for the VOR adaptation

Although the aforementioned three lines of evidence consistently indicate that the flocculus plays a crucial role in the induction of the VOR adaptation, there has been dichotomy of opinion about the role of this structure in its retention. To determine whether the VOR adaptation is retained in the flocculus or not, the effects of the (surgical or functional) removal of flocculus functions after the VOR adaptation had developed was studied. In goldfish, no less than 30% of the altered VOR gain

Debate 2: Purkinje-cell behavior associated with VOR adaptation

Another debate concerns the behavior of flocculus Purkinje cells. Even though this behavior conforms to the flocculus hypothesis in the rabbit H zone (Appendix Aand Appendix D), inconsistent results have been reported in monkey and goldfish experiments. However, these experiments involve serious technical problems: the earlier data on monkeys were obtained without distinguishing between the ventral paraflocculus and the flocculus[8]. It is also questionable whether the vestibular responses of

Debate 3: implications of oculomotor signals

In the aforementioned visual-suppression method, the difference between the responses during VOR and those during visual suppression was considered to represent oculomotor signals encoding eye velocity or eye position. As the oculomotor signals so derived were large, it has been hypothesized that oculomotor signals provide positive feedback from the oculomotor system to the VOR-relay neurons via the flocculus[53](Fig. 3B). If this were the case, changes in Purkinje-cell behavior observed during

Conclusion

The VOR–flocculus system conforms to the general idea of a cerebellar corticonuclear microcomplex as a module capable of error-driven learning to modify its input–output relationships59, 60. Controversies about the neuronal mechanisms in a microcomplex need to be resolved in future but, as the microcomplex includes both a cerebellar cortical zone and a nuclear cell group (Fig. 4), the debate on the memory site for VOR adaptation is not critical for the microcomplex concept. Such microcomplexes

Outstanding questions

  • Does LTD account for long-term or even permanent memory? This has not been answered because of technical difficulties that currently do not allow us to follow the time course of LTD for more than three hours. This question is central to the cerebellar-learning theories and, to answer it, new technologies for marking LTD are required.

  • Is the memory in VOR adaptation controlled by the flocculus alone or by brainstem pathways, or by both of them? Although the available evidence consistently

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