Introduction

People living with vestibular disorders report a considerable impact on their quality of life [1]. Vestibular disorders affect multiple functions (e.g., balance and gait), leading to incapacity and participation restriction [2]. Current treatments for vestibular disorders include pharmacological and non-pharmacological approaches [3,4]. Vestibular rehabilitation is an effective and specialized approach that aims to promote compensation for vestibular deficits, improve balance, reduce dizziness and vertigo symptoms, and enhance overall functional independence [5]. Vestibular rehabilitation techniques encompass a range of exercises and interventions targeting different aspects of the vestibular system [6,7]. Gaze stabilization exercises improve coordination between the vestibular and visual systems. Balance training exercises focus on postural control and stability. Habituation exercises gradually expose individuals to movements or stimuli that provoke their symptoms [8]. All these techniques enhance overall balance and functional performance. Recently, motor imagery has emerged as a promising technique targeting the cognitive processes involved in movement generation [9–11].

Motor imagery is based on the simulation theory [12,13], which posits that every action consists of two phases: an internal, invisible phase of anticipation, and a visible phase of execution [12]. The anticipation phase includes the purpose of the action, the meaning of the action and the consequences of the action on the organism and the outside world [13]. The simulation theory postulates that the anticipation phase involves all the neural mechanisms of an action that is internally generated but not physically executed [13]. Accordingly, motor imagery refers to the mental simulation of a movement without actual execution [9,11], a process that relies on intact sensory and cognitive systems. Among these, vestibular sensory processing both influences and is influenced by higher cognitive functions. Yardley et al. showed that vestibular pathology can cause interference between postural control and the execution of mental tasks in people with vestibular disorders [14]. Schönherr and May showed that caloric vestibular stimulation affects the perceptual component of body experience in healthy participants, highlighting its role in modulating the different perceptual qualities that contribute to our body experience [15]. In an experimental study, Zhang et al. [16] demonstrated specific vestibular activity after a program based on motor imagery and vestibular stimulation motor imagery. Pérush et al. (2011) also shows that vestibular damage disorganizes brain structures commonly involved in mental imagery, and more generally in mental representation [17]. Mast et al. 2005 show that vestibular stimulation affects mental imagery and mental rotation [18]. All of these studies highlight the impact of vestibular dysfunction—whether experimentally induced or pathological—on motor imagery abilities. They also raise the question of a possible bidirectional relationship between the vestibular system and motor cognitive processes.

Experts have made recommendations for using motor imagery in vestibular rehabilitation, but no literature has been cited supporting them. A recent narrative review [10] recommended integrating imagined body movements (i.e., motor imagery) into a vestibular rehabilitation protocol to improve functional recovery, without providing supporting evidence. A review of specific studies on this subject is therefore required. In addition, information is needed on the interventions to be applied, the specific effects and other characteristics useful to clinicians implementing these interventions and researchers aiming to better understand motor imagery in vestibular rehabilitation.

The aim of this study was to (1) identify motor imagery interventions used in the context of vestibular rehabilitation, (2) critically appraise them based on best practice elements from the fields of motor imagery and vestibular rehabilitation, and (3) synthesize their reported effects on clinical outcomes.

Materials and methods

To achieve our objective, we conducted a “systematic search and review” [19]. This approach combines the rigorous search strategy of a systematic review with the interpretive flexibility of a critical review, making it particularly well suited to broad and exploratory questions [19]. This method allows for the inclusion of diverse study types, enabling a comprehensive overview of the existing literature [19]. Unlike traditional systematic reviews, which aim to evaluate intervention effectiveness and therefore apply tools such as GRADE to rate the certainty of effect estimates, a systematic search and review focuses on describing interventions, examining their clinical applicability, and identifying conceptual or methodological gaps [19,20]. In this context, GRADE or equivalent frameworks, which are designed to assess confidence in pooled or comparative effect estimates, are not appropriate [21]. Moreover, this approach supports the integration of expert-informed appraisal criteria [20], which we used to evaluate the clinical relevance and feasibility of identified interventions based on best practice elements in motor imagery and vestibular rehabilitation. No methodological standards were available for this approach. To ensure a robust synthesis, an adapted version of the JBI Manual for Evidence Synthesis was used to fit with the systematic search and review typology [22]. The review and results are reported according to the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA-2020). The protocol was registered in PROSPERO (CRD42023444673).

Eligibility criteria

Table 1 presents the eligibility criteria for articles related to the research question according to the Population, Intervention, Comparator and Outcomes (PICO) framework [25].

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Table 1. Extraction grid.

https://doi.org/10.1371/journal.pone.0337445.t001

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https://doi.org/10.1371/journal.pone.0337445.t003

Selection process

A calibration training was performed for title and abstract screening using 10 randomly selected references. If the agreement percentage between the two reviewers was below 80% [27], the eligibility criteria were refined, and a new calibration phase was conducted.

Two reviewers (TR and DF) with expertise in the vestibular and motor imagery fields independently screened the title and abstract of each citation. The same two reviewers then screened the full texts of potential studies. Disagreement between reviewers was handled with a third reviewer (FN). The reasons for full-text exclusion (no human participants, adults, no motor imagery intervention, no vestibular rehabilitation, no vestibula desease or vestibular simulation) were documented and are reported in the PRISMA 2020 flow chart (Fig 1).

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Fig 1. Flow chart of the selection process.

https://doi.org/10.1371/journal.pone.0337445.g001

Results

The flow chart of the selection process is illustrated in Fig 1. A total of 2543 items, including duplicates, were identified. After removing the duplicates, 2404 citations remained for the selection process. 1 more article was included from handsearching. After the titles and abstracts stage, the initial search yielded 11 articles eligible for full-text screening. Only 10 were available in full-text; the last one was a protocol in progress. Of these articles, two met all the inclusion criteria and were selected for data extraction.

Critical appraisal of the studies

All extracted data are shown in Table 2: critical appraisal tool. A large proportion of data is missing. The data collected show low to no external validity, unrepresentative or poorly adapted assessment, lack of statistical validity, low internal validity, lack of use of motor imagery intervention recommendations, and lack of use of recommendations for practice in vestibular disorders. “See the supplementary material for explanations of the critical grid.”

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Table 2. Critical appraisal tool.

https://doi.org/10.1371/journal.pone.0337445.t002

Discussion

The aims of this study were 1. to identify motor imagery interventions used in the literature, 2. to critically appraise them, and 3. to report their impact on clinical outcomes. This systematic search and review identified two studies evaluating motor imagery: one in people with neuritis and the other in healthy people who underwent vestibular stimulation. Both studies had many limitations and risks of bias. Our findings suggest a possible effect of motor imagery on the vestibulo-ocular reflex (VOR), especially the SPV. However, several concerns were raised regarding the methodological choices and feasibility of the motor imagery interventions used in the included studies.

Although recommendations have been made regarding the use of motor imagery as part of vestibular rehabilitation [10], our review found little evidence to support this [23,24]. In addition to the fact only two studies have been published on this specific subject, the quality of the studies is limited. Only one study was controlled (in one, participants were their own controls), and it involved healthy individuals who underwent vestibular stimulation to simulate pathology. This method does not represent all vestibular pathologies and does not take into account all the dimensions of the pathological experience. The other study involved individuals with vestibular pathology, but the design did not allow the intervention to be controlled. Therefore, contrary to Lacour and Bernard-Demanze’s proposal [10], it does not seem appropriate to recommend using motor imagery in clinical practice as a first-line treatment based on the scientific literature.

However, motor imagery could positively impact people living with vestibular disorders. These two studies suggest a significant effect of motor imagery on the VOR, especially the SPV, which is altered in all vestibular disorders [23,24]. This is a decisive point in our review, as nystagmographic measurement and quantification of this reflex are considered the gold standard in the international indexed literature [34,35]. Videonystagmography evaluates the vestibular system in a reproducible and non-invasive manner. Nevertheless, several limitations were identified. Firstly, the external validity of the studies is limited by the use of videonystagmography alone (nystagmography, although useful, does not assess all the components of the vestibular system individually, and does not take into account compensatory strategies implemented by the individual) [36,37], and the absence of pathology and the high cost of the intervention and evaluation for one [24] of the studies. Internal validity is also limited by the lack of blinding, the absence of a control arm in one study and a non-explicit random allocation in the other, as well as the lack of evidence supporting the outcome measures used [31]. Finally, the motor imagery rehabilitation programs used cannot be reproduced or optimized since no description of the motor imagery modalities or perspectives used was provided, and there was no motor imagery quality evaluation or progression of the program [33].

From a clinical point of view, the results suggest a potential benefit of using motor imagery as part of vestibular rehabilitation. However, these results need to be weighed against methodological considerations. Firstly, the number of studies selected, and the number of subjects involved in these studies was small (total of 36). Secondly, the representativeness of the samples is questionable. Although Jahn et al. evaluated individuals with vestibular pathology, this was limited to neuritis, which does not represent the diversity of pathophysiological processes involved in vestibular disorders. Nigmatulina et al. evaluated healthy subjects who underwent stimulation to reproduce a symptom, which also does not represent all vestibular diseases. Regarding the question posed in this review about recommendations for using motor imagery in vestibular rehabilitation [10], the limited data in the literature does not support such a recommendation despite some consistent findings in fundamental research [14–16].

However, from a research point of view, these results, together with the large body of theoretical models and literature showing the impact of vestibular diseases on the quality of motor imagery, suggest that studies should continue to investigate the clinical application of this method. Specifically, future research should include: 1. assessment of subjects’ motor imaging quality (vestibular damage may affect imaging quality); 2. a battery of vestibular tests (Video Head Impulse Test assessment, functional impact and quality of life as measured by the Dizziness Handicap Inventory); 3. a clear, reproducible, and realistic rehabilitation program for use in routine practice, in accordance with recommendations on motor imaging [33] and vestibular rehabilitation [6]. For example, it should include motor imagery exercises related to the practice of vestibular rehabilitation therapists, with imagery reproduction of these exercises, of a specific duration, intensity, and regularity. The number of subjects required should be determined based on a primary endpoint predefined before the study. The study must be multicenter in order to avoid a “center effect.” Given the heterogeneity of vestibular pathologies, future studies should focus on a specific vestibular pathology (e.g., neuritis, Meniere’s syndrome, etc.) to test these hypotheses. Finally, studies on healthy subjects receiving vestibular stimulation could be conducted.

The low quality of the studies included does not allow firm conclusions to be drawn regarding future research. Methodologically robust studies including representative samples of individuals with vestibular pathology are required. Comprehensive assessments should be conducted, as stated above. Studies should report a complete description of the motor imagery intervention, including an imagery quality assessment [38], the perspective and modality used to produce the image [11,33,39], prior familiarization, and the practice of imagery during or outside the sessions to enable a better understanding and reproducibility of the proposed rehabilitation program [11,33,39]. Finally, a long-term evaluation of the retention of the effect is necessary to determine the clinical benefit.

Conclusion

This systematic search and review identified two studies evaluating the efficacy of motor imagery interventions for the rehabilitation of vestibular disorders. While studies suggest that motor imagery rehabilitation reduces the vestibulo-ocular reflex, there are some methodological concerns included the small sample size, absence of imagery quality assessment, and poor generalizability. However, although motor imagery appears to be affected by vestibular pathology, the paucity and lack of quality of the available evidence does not allow us to recommend its use in routine practice at this time.

Supporting information

Acknowledgments

We thank Johanna Robertson, PT, PhD for English editing.