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Damage to one vestibular labyrinth or nerve causes a central tone imbalance, reflected by prominent spontaneous nystagmus. Central adaptive mechanisms eliminate the nystagmus over several days, and the mechanisms underlying this process have received extensive study. The characteristics of vestibular compensation when the tone imbalance is presented gradually or repeatedly have never been studied. We used high-frequency electrical stimulation of semicircular canal afferents to generate a vestibular tone imbalance and recorded the nystagmus produced when the stimulation was started abruptly or gradually and when it was repeatedly cycled on and off. In the acute-onset protocol, brisk nystagmus occurred when stimulation started, gradually resolved within 1 day, and reversed direction when the stimulation was stopped after 1 week. Repeated stimulation cycles resulted in progressively smaller nystagmus responses. In the slow-onset protocol, minimal nystagmus occurred while the stimulation ramped-up to its maximum rate over 12 h, but a reversal still occurred when the stimulation was stopped after 1 week, and repeated stimulation cycles did not affect this pattern. The absence of nystagmus during the 12 h ramp of stimulation demonstrates that central vestibular tone can rebalance relatively quickly, and the reduction in the stimulation-off nystagmus with repeated cycles of the acute-onset but not the slow-onset stimulation suggests that dual-state adaptation may have occurred with the former paradigm but not the latter.
The central vestibular system is highly plastic and can adapt to changes in peripheral labyrinthine inputs or changes in visually mediated demands. The former is typically studied with lesions of the labyrinth or vestibular nerve (e.g., Fetter and Zee 1988) that eliminate all input from the affected ear and produce substantial static and dynamic abnormalities in eye movements, posture, and perception (Dieringer 1995). Many studies have focused on vestibular-mediated eye movements as a way to quantify adaptation. Ablative lesions such as labyrinthectomy produce strong spontaneous nystagmus, the static oculomotor abnormality that results from a central imbalance in tonic activity between the vestibular nuclei on the ablated and normal sides (Vidal et al. 1998). The process of vestibular compensation eliminates the spontaneous nystagmus over a period of days, but this form of adaptation has been studied exclusively as a monophasic process that occurs when an acute lesion of the vestibular periphery produces a large, abrupt imbalance in central vestibular tone (Curthoys 2000). This approach mimics the changes that occur clinically after acute peripheral damage (e.g., vestibular neuritis, Halmagyi et al. 2010).
While vestibular deficits can also develop gradually (e.g., with a vestibular schwannoma, Day et al. 2008), the compensation that occurs when a central tone imbalance is introduced gradually has never been explored. Furthermore, it has become clear that the vestibulo-ocular reflex (VOR) can adapt to more than one condition simultaneously and that the appropriate motor responses can be accessed using sensory cues linked to the condition. By tailoring retinal image motion to different contexts, for example, the VOR gain can be differentially adapted for different orbital eye positions (Shelhamer et al. 1992). This context-specific adaptation allows rapid changes in motor output to occur when the demands on the system change abruptly. Since the training that elicits this multi-state adaptation requires repeated switching between two or more sensori-motor conditions, an experimental approach to evaluate the possibility of multi-state adaptation of static vestibular tone has not been available.
It has been observed that high-frequency electrical stimulation of vestibular afferents from one ear closely mimics the static behavioral syndrome (e.g., spontaneous nystagmus, postural instability) that occurs after unilateral vestibular ablation (Vidal et al. 1998; Merfeld et al. 2006). Electrical stimulation, however, allows one to alter central vestibular tone in a controlled and reversible manner that cannot be replicated with standard ablative procedures. Using this approach, an imbalance in central vestibular tone can be introduced gradually or rapidly. Furthermore, since electrical stimulation can be switched on and off, this method allows one to probe the capacity for dual-state adaptation of the vestibular tone balance between the stimulated and unstimulated sides. In the current study, we compared the eye movements elicited by gradual and rapid changes in the central vestibular tone balance produced by electrical stimulation of canal afferents to investigate if the rate at which the tone imbalance develops affects static compensation. We also examined the effects of repeated cycles of electrical stimulation to investigate the capacity for dual-state adaptation of vestibular tone.
We thank S. Fukuda, M. Saginaw, and J-P Guyot. This work was supported by the Geneva Charity Foundation “Valeria Rossi di Montelera” and the Swiss Foundation for Fellowships in Medicine and Biology (PASMP3-123225) in collaboration with the Swiss National Science Foundation (K. Nicoucar); by the National Institute of Deafness and Other Communication Disorders Grants DC-6909 and DC-8362 to R.F. Lewis and DC-8167 to D.M. Merfeld; and by the European Commission contract 225929 to D.M. Merfeld.
Richard F. Lewis, Phone: +1-617-5733501, Fax: +1-617-5734154, Email: Richard_lewis/at/meei.harvard.edu.
Keyvan Nicoucar, Email: Keyvan_nicourcar/at/meei.harvard.edu.
Wangsong Gong, Email: Wangsong_gong/at/meei.harvard.edu.
Csilla Haburcakova, Email: Csilla_haburckova/at/meei.harvard.edu.
Daniel M. Merfeld, Email: Dan_merfeld/at/meei.harvard.edu.