Elsevier

Brain Research

Volume 1482, 30 October 2012, Pages 101-111
Brain Research

Review
Top-down approach to vestibular compensation: Translational lessons from vestibular rehabilitation

https://doi.org/10.1016/j.brainres.2012.08.040Get rights and content

Abstract

This review examines vestibular compensation and vestibular rehabilitation from a unified translational research perspective. Laboratory studies illustrate neurobiological principles of vestibular compensation at the molecular, cellular and systems levels in animal models that inform vestibular rehabilitation practice. However, basic research has been hampered by an emphasis on ‘naturalistic’ recovery, with time after insult and drug interventions as primary dependent variables. The vestibular rehabilitation literature, on the other hand, provides information on how the degree of compensation can be shaped by specific activity regimens. The milestones of the early spontaneous static compensation mark the re-establishment of static gaze stability, which provides a common coordinate frame for the brain to interpret residual vestibular information in the context of visual, somatosensory and visceral signals that convey gravitoinertial information. Stabilization of the head orientation and the eye orientation (suppression of spontaneous nystagmus) appear to be necessary by not sufficient conditions for successful rehabilitation, and define a baseline for initiating retraining. The lessons from vestibular rehabilitation in animal models offer the possibility of shaping the recovery trajectory to identify molecular and genetic factors that can improve vestibular compensation.

Introduction

Recent decades of basic research into cellular and molecular mechanisms of vestibular compensation have produced important insights into functional plasticity of the central nervous system. For example, a considerable body of evidence indicates that vestibulo-ocular reflex plasticity is mediated by protein kinase C (PKC)-dependent mechanisms in modular vestibulocerebellar cortico-nuclear microcircuits termed microcomplexes, which are small networks involving the inferior olive, vestibular nuclei, nucleus prepositus hypoglossi and the flocculonodular lobe (Ito, 2001). Inhibition of flocculonodular lobe Purkinje cell PKC blocks adaptive modification of vestibulo-ocular (De Zeeuw et al., 1998) and optokinetic (Shutoh et al., 2003) responses. In this regard, it is significant that Purkinje cells in different flocculonodular lobe microcomplexes show transient molecular changes in specific PKC isoform expression during compensation for unilateral ablation of vestibular endorgans (Balaban and Romero, 1998, Balaban et al., 1999, Goto et al., 1997) and that PKC inhibition retards the resolution of spontaneous nystagmus in these animals (Balaban et al., 1999). Inhibition of flocculus PKC also prevented a compensatory increase in the intrinsic excitability of medial vestibular nucleus neurons during early vestibular compensation (Johnston et al., 2002). Although cerebellar long term depression (LTD) is induced in Purkinje cells by processes that require simultaneous parallel and climbing fiber activity and PKC activation (De Zeeuw et al., 1998, Ito, 2001, Leitges et al., 2004, Linden and Connor, 1995), the PKC-mediated effects on both cerebellar motor learning and oculomotor aspects of vestibular compensation likely include mechanisms in addition to LTD (Faulstich et al., 2006, Schonewille et al., 2011). A number of comprehensive reviews provide additional examples of the value of vestibular compensation as a model system for investigating dynamic neural reorganization of sensorimotor processes (Cullen et al., 2009, Dutia, 2010, Gliddon et al., 2005, Lacour and Tighilet, 2010).

Unfortunately, these advances in understanding of basic processes of vestibular compensation have found very little translational application into therapies that improve compensation outcomes in patients. By contrast, vestibular rehabilitation therapy has been a remarkable success story. This communication explores implications of Lacour's (Lacour, 2006) observation that vestibular compensation includes a rapid, ‘vestibulo-centric’ static process and a longer term, dynamic, distributed learning process. We suggest that the focus of the basic scientific approach on spontaneous compensation after peripheral vestibular ablation elucidates only mechanisms that bring a patient to the functional point of entry into rehabilitation therapy. Vestibular rehabilitation therapy improves dynamic performance by replacing systematically some previously compensatory strategies with new, learned strategies that enhance functional recovery. The therapy is guided by three implicit assumptions. Firstly, spontaneous compensation is not optimal. Secondly, compensation is viewed as a top-down, ordered process, proceeding from eye–head stabilization to dynamic gait stabilization. Thirdly, effective rehabilitation involves stepwise guidance of adaptive learning to achieve interim goals of increasing complexity. For example, a first goal in vestibular rehabilitation is to overcome the voluntary (‘adaptive’) limitations on head movements that patients often adopt to minimize precipitating disequilibrium and nausea (Herdman and Whitney, 2007); other interim goals may only be intermediate steps to enable further improvement. The implication is obvious: scientific paradigms for studying vestibular compensation should be expanded to elucidate mechanisms that are likely to be clinically meaningful for improving rehabilitation outcomes.

There is a common fallacy that translational research is strictly a ‘bottom-up’ process from the laboratory bench, via animal model trials, to the clinic. To the contrary, the fundamental importance of the clinical to basic research path in experimental medicine was emphasized by Claude Bernard (Bernard, 1875, c1989) more than 130 years ago in the statement that experimental medicine “ …claims knowledge of the laws of healthy and diseased organisms, not only as to foresee phenomena, but also so as to be able to regulate and alter them within certain limits. Accordingly, we easily perceive that medicine tends to become experimental, and that every physician who gives his patients active medicine cooperates in building up experimental medicine.” Stated simply, basic investigators have the task of providing therapeutically relevant explanations for the outcomes of the patient-oriented and disease-oriented clinical research. Hence, this review focuses on lessons from procedures and outcomes of vestibular rehabilitation therapy that can inform the experimental analysis of vestibular compensation. Conversely, we discuss how principles from laboratory studies of vestibular compensation inform and are validated by clinical rehabilitation practice.

Section snippets

History and relationship with ‘stages of compensation’

Vestibular rehabilitation is a therapeutic approach to enhance functional vestibular compensation. Sir Terence Cawthorne and F.S. Cooksey (Cawthorne, 1945, Cawthorne, 1949, Cooksey, 1945) are credited with formalizing the concept of vestibular rehabilitation by developing a balance rehabilitation strategy for British soldiers injured in the Second World War. Despite the success of their work, vestibular rehabilitation was largely ignored until half a century later, when a number of

Therapeutic progression proceeds from head control to locomotion

Empirical principles for vestibular rehabilitation practice include an implicit top-down strategy for progression of exercises. The therapy progression can be summarized from the literature (Herdman and Whitney, 2007, Whitney and Sparto, 2011) as follows. If patient are incapable of standing safely, they remain seated and perform active eye and head movements while fixating on a point in a lighted room. If the patient is capable of standing safely, static postural control exercises are

Sensorimotor performance

Experience with vestibular rehabilitation indicates that outcomes are improved by stepwise achievement of interim goals, which may require replacing previously compensatory strategies with new, learned strategies that enhance functional recovery. The first benchmark, resolution of nausea, severe vertigo and spontaneous nystagmus, is typically achieved prior to initiating rehabilitation (Herdman and Whitney, 2007). It has long been recognized that this benchmark is a necessary but insufficient

Vestibular compensation is a life-long, trainable adaptive process

The term ‘vestibular compensation’ is used most commonly to describe phenomena that occur after unilateral impairment of the vestibular periphery (Curthoys and Halmagyi, 1999). The profound effects of compensatory processes on balance control were noted during the latter decades of the nineteenth century in some of the earliest descriptions of the phenomena. The most striking was von Bechterew's report (Bechterew, 1883) that unilateral, serial bilateral, and simultaneous bilateral damage to the

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