Visual and proprioceptive interaction in patients with bilateral vestibular loss.

Nicholas J Cutfield,Adolfo M Bronstein,David J Sharp,Gregory Scott,Adam D Waldman

doi:10.1016/j.nicl.2013.12.013

Abstract

Following bilateral vestibular loss (BVL) patients gradually adapt to the loss of vestibular input and rely more on other sensory inputs. Here we examine changes in the way proprioceptive and visual inputs interact. We used functional magnetic resonance imaging (fMRI) to investigate visual responses in the context of varying levels of proprioceptive input in 12 BVL subjects and 15 normal controls. A novel metal-free vibrator was developed to allow vibrotactile neck proprioceptive input to be delivered in the MRI system. A high level (100 Hz) and low level (30 Hz) control stimulus was applied over the left splenius capitis; only the high frequency stimulus generates a significant proprioceptive stimulus. The neck stimulus was applied in combination with static and moving (optokinetic) visual stimuli, in a factorial fMRI experimental design. We found that high level neck proprioceptive input had more cortical effect on brain activity in the BVL patients. This included a reduction in visual motion responses during high levels of proprioceptive input and differential activation in the midline cerebellum. In early visual cortical areas, the effect of high proprioceptive input was present for both visual conditions but in lateral visual areas, including V5/MT, the effect was only seen in the context of visual motion stimulation. The finding of a cortical visuo-proprioceptive interaction in BVL patients is consistent with behavioural data indicating that, in BVL patients, neck afferents partly replace vestibular input during the CNS-mediated compensatory process. An fMRI cervico-visual interaction may thus substitute the known visuo-vestibular interaction reported in normal subject fMRI studies. The results provide evidence for a cortical mechanism of adaptation to vestibular failure, in the form of an enhanced proprioceptive influence on visual processing. The results may provide the basis for a cortical mechanism involved in proprioceptive substitution of vestibular function in BVL patients.

Highlights

Spatial orientation, balance and gaze stabilization involve integrating multiple sensory systems, including vestibular, visual and proprioceptive signals
We demonstrate that proprioceptive and visual processing interact in subjects with bilaterally reduced peripheral vestibular function (BVL patients)
Neck proprioceptive and visual motion signals interact, and this effect differs between normal subjects and patients with acquired bilateral vestibular loss

Summary

Introduction

Balance and gaze stabilization involve integrating multiple sensory systems, including vestibular, visual and proprioceptive signals. How and where these complementary sensory signals are integrated and processed in the human brain is not well understood. Multisensory compensation is thought to occur in the brain after the loss of sensory afferents and to play a role in clinical recovery in vestibular disorders (Dieterich et al, 2007). ⁎ Correspondence to: D.J. Sharp, The Computational, Cognitive and Clinical Neuroimaging Laboratory, 3rd Floor, Burlington Danes Building, The Hammersmith Hospital, Du Cane Road, London, W12 0NN, UK. Tel.: +44 2075947991 (Office), +44 2083833160 (Sec.), +44 7590250508 (Mobile); fax: +44 207 594 8921.

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