An fMRI study of visuo-vestibular interactions following vestibular neuritis

Vestibular neuritis (VN) is characterised by acute vertigo due to a sudden loss of unilateral vestibular function. A considerable proportion of VN patients proceed to develop chronic symptoms of dizziness, including visually induced dizziness, specifically during head turns. Here we investigated whether the development of such poor clinical outcomes following VN, is associated with abnormal visuo-vestibular cortical processing. Accordingly, we applied functional magnetic resonance imaging to assess brain responses of chronic VN patients and compared these to controls during both congruent (co-directional) and incongruent (opposite directions) visuo-vestibular stimulation (i.e. emulating situations that provoke symptoms in patients). We observed a focal significant difference in BOLD signal in the primary visual cortex V1 between patients and controls in the congruent condition (small volume corrected level of p < .05 FWE). Importantly, this reduced BOLD signal in V1 was negatively correlated with functional status measured with validated clinical questionnaires. Our findings suggest that central compensation and in turn clinical outcomes in VN are partly mediated by adaptive mechanisms associated with the early visual cortex

Vestibular Perception following Acute Unilateral Vestibular Lesions.

Little is known about the vestibulo-perceptual (VP) system, particularly after a unilateral vestibular lesion. We investigated vestibulo-ocular (VO) and VP function in 25 patients with vestibular neuritis (VN) acutely (2 days after onset) and after compensation (recovery phase, 10 weeks). Since the effect of VN on reflex and perceptual function may differ at threshold and supra-threshold acceleration levels, we used two stimulus intensities, acceleration steps of 0.5°/s(2) and velocity steps of 90°/s (acceleration 180°/s(2)). We hypothesised that the vestibular lesion or the compensatory processes could dissociate VO and VP function, particularly if the acute vertiginous sensation interferes with the perceptual tasks. Both in acute and recovery phases, VO and VP thresholds increased, particularly during ipsilesional rotations. In signal detection theory this indicates that signals from the healthy and affected side are still fused, but result in asymmetric thresholds due to a lesion-induced bias. The normal pattern whereby VP thresholds are higher than VO thresholds was preserved, indicating that any 'perceptual noise' added by the vertigo does not disrupt the cognitive decision-making processes inherent to the perceptual task. Overall, the parallel findings in VO and VP thresholds imply little or no additional cortical processing and suggest that vestibular thresholds essentially reflect the sensitivity of the fused peripheral receptors. In contrast, a significant VO-VP dissociation for supra-threshold stimuli was found. Acutely, time constants and duration of the VO and VP responses were reduced - asymmetrically for VO, as expected, but surprisingly symmetrical for perception. At recovery, VP responses normalised but VO responses remained shortened and asymmetric. Thus, unlike threshold data, supra-threshold responses show considerable VO-VP dissociation indicative of additional, higher-order processing of vestibular signals. We provide evidence of perceptual processes (ultimately cortical) participating in vestibular compensation, suppressing asymmetry acutely in unilateral vestibular lesions

Functional correlates of optic flow motion processing in Parkinson’s disease

The visual input created by the relative motion between an individual and the environment, also called optic flow, influences the sense of self-motion, postural orientation, veering of gait, and visuospatial cognition. An optic flow network comprising visual motion areas V6, V3A, and MT+, as well as visuo-vestibular areas including posterior insula vestibular cortex (PIVC) and cingulate sulcus visual area (CSv), has been described as uniquely selective for parsing egomotion depth cues in humans. Individuals with Parkinson’s disease (PD) have known behavioral deficits in optic flow perception and visuospatial cognition compared to age- and education-matched control adults (MC). The present study used functional magnetic resonance imaging (fMRI) to investigate neural correlates related to impaired optic flow perception in PD. We conducted fMRI on 40 non-demented participants (23 PD and 17 MC) during passive viewing of simulated optic flow motion and random motion. We hypothesized that compared to the MC group, PD participants would show abnormal neural activity in regions comprising this optic flow network. MC participants showed robust activation across all regions in the optic flow network, consistent with studies in young adults, suggesting intact optic flow perception at the neural level in healthy aging. PD participants showed diminished activity compared to MC particularly within visual motion area MT+ and the visuo-vestibular region CSv. Further, activation in visuo-vestibular region CSv was associated with disease severity. These findings suggest that behavioral reports of impaired optic flow perception and visuospatial performance may be a result of impaired neural processing within visual motion and visuo-vestibular regions in PD.Published versio

Systematic biases in human heading estimation.

Heading estimation is vital to everyday navigation and locomotion. Despite extensive behavioral and physiological research on both visual and vestibular heading estimation over more than two decades, the accuracy of heading estimation has not yet been systematically evaluated. Therefore human visual and vestibular heading estimation was assessed in the horizontal plane using a motion platform and stereo visual display. Heading angle was overestimated during forward movements and underestimated during backward movements in response to both visual and vestibular stimuli, indicating an overall multimodal bias toward lateral directions. Lateral biases are consistent with the overrepresentation of lateral preferred directions observed in neural populations that carry visual and vestibular heading information, including MSTd and otolith afferent populations. Due to this overrepresentation, population vector decoding yields patterns of bias remarkably similar to those observed behaviorally. Lateral biases are inconsistent with standard bayesian accounts which predict that estimates should be biased toward the most common straight forward heading direction. Nevertheless, lateral biases may be functionally relevant. They effectively constitute a perceptual scale expansion around straight ahead which could allow for more precise estimation and provide a high gain feedback signal to facilitate maintenance of straight-forward heading during everyday navigation and locomotion

Recurrent cerebellar architecture solves the motor-error problem

Current views of cerebellar function have been heavily influenced by the models of Marr and Albus, who suggested that the climbing fibre input to the cerebellum acts as a teaching signal for motor learning. It is commonly assumed that this teaching signal must be motor error (the difference between actual and correct motor command), but this approach requires complex neural structures to estimate unobservable motor error from its observed sensory consequences. We have proposed elsewhere a recurrent decorrelation control architecture in which Marr-Albus models learn without requiring motor error. Here, we prove convergence for this architecture and demonstrate important advantages for the modular control of systems with multiple degrees of freedom. These results are illustrated by modelling adaptive plant compensation for the three-dimensional vestibular ocular reflex. This provides a functional role for recurrent cerebellar connectivity, which may be a generic anatomical feature of projections between regions of cerebral and cerebellar cortex

A Low-Dimensional Model of Coordinated Eye and Head Movements

Eye and head movement data, were recorded under head fixed and head-free conditions, and compared with theoretical results obtained using a nonlinear model of eye-head coordination. The model explains slow, or pursuit movement correlated closely to target movement, and saccades, or quick phases of eye movement. Eye movement under head-fixed conditions was modeled by an externally forced Duffing equation, whilst properties of head movement are described by a second externally forced Duffing equation with lower eigen frequency. In the more natural, head-free conditions where both eye and head movements are used synergetically to pursue a visual target, the vestibulocular reflex (VOR) is represented by coefficients defining the mutual coupling between these two oscillatory systems. In the present model, the oscillator that models eye movement has an inhibitory influence on head movement; head to eye coupling coefficients are included to model the influence of the VOR mechanism. Individual eye and head movement patterns in different subjects can be adequately modeled by altering the coupling coefficients. In order to adequatcly simulate those changes introduced by microgravity conditions, the coefficients defining eye-head coordination (mutual coupling) must be changed. It may be hypothesized tlmt such changes in the neurovestibular system could introduce the instability in eye-head coordination, which is known to lead to space sickness.Whitehall Foundation (S93-24

Bilateral cochlear implantation or bimodal listening in the paediatric population : retrospective analysis of decisive criteria

Introduction: In children with bilateral severe to profound hearing loss, bilateral hearing can be achieved by either bimodal stimulation (CIHA) or bilateral cochlear implantation (BICI). The aim of this study was to analyse the audiologic test protocol that is currently applied to make decisions regarding the bilateral hearing modality in the paediatric population. Methods: Pre- and postoperative audiologic test results of 21 CIHA, 19 sequential BICI and 12 simultaneous BICI children were examined retrospectively. Results: Deciding between either simultaneous BICI or unilateral implantation was mainly based on the infant's preoperative Auditory Brainstem Response thresholds. Evolution from CIHA to sequential BICI was mainly based on the audiometric test results in the contralateral (hearing aid) ear after unilateral cochlear implantation. Preoperative audiometric thresholds in the hearing aid ear were significantly better in CIHA versus sequential BICI children (p < 0.001 and p = 0.001 in unaided and aided condition, respectively). Decisive values obtained in the hearing aid ear in favour of BICI were: An average hearing threshold measured at 0.5, 1, 2 and 4 kHz of at least 93 dB HL without, and at least 52 dB HL with hearing aid together with a 40% aided speech recognition score and a 70% aided score on the phoneme discrimination subtest of the Auditory Speech Sounds Evaluation test battery. Conclusions: Although pure tone audiometry offers no information about bimodal benefit, it remains the most obvious audiometric evaluation in the decision process on the mode of bilateral stimulation in the paediatric population. A theoretical test protocol for adequate evaluation of bimodal benefit in the paediatric population is proposed

Mechanisms of Action and Targets of Nitric Oxide in the Oculomotor System

Nitric oxide (NO) production by neurons in the prepositus hypoglossi (PH) nucleus is necessary for the normal performance of eye movements in alert animals. In this study, the mechanism(s) of action of NO in the oculomotor system has been investigated. Spontaneous and vestibularly induced eye movements were recorded in alert cats before and after microinjections in the PH nucleus of drugs affecting the NO–cGMP pathway. The cellular sources and targets of NO were also studied by immunohistochemical detection of neuronal NO synthase (NOS) and NO-sensitive guanylyl cyclase, respectively. Injections of NOS inhibitors produced alterations of eye velocity, but not of eye position, for both spontaneous and vestibularly induced eye movements, suggesting that NO produced by PH neurons is involved in the processing of velocity signals but not in the eye position generation. The effect of neuronal NO is probably exerted on a rich cGMP-producing neuropil dorsal to the nitrergic somas in the PH nucleus. On the other hand, local injections of NO donors or 8-Br-cGMP produced alterations of eye velocity during both spontaneous eye movements and vestibulo-ocular reflex (VOR), as well as changes in eye position generation exclusively during spontaneous eye movements. The target of this additional effect of exogenous NO is probably a well defined group of NO-sensitive cGMP-producing neurons located between the PH and the medial vestibular nuclei. These cells could be involved in the generation of eye position signals during spontaneous eye movements but not during the VOR.Fondo de Investigación Sanitaria Grants 94/0388 and 97/2054Comunidad Autónoma de Madrid Grant 08.5/0019/1997Dirección General de Investigación Científica y Technológica Grant PB 93–117

The Neuroanatomical Correlates of Training-Related Perceptuo-Reflex Uncoupling in Dancers

Sensory input evokes low-order reflexes and higher-order perceptual responses. Vestibular stimulation elicits vestibular-ocular reflex (VOR) and self-motion perception (e.g., vertigo) whose response durations are normally equal. Adaptation to repeated whole-body rotations, for example, ballet training, is known to reduce vestibular responses. We investigated the neuroanatomical correlates of vestibular perceptuo-reflex adaptation in ballet dancers and controls. Dancers' vestibular-reflex and perceptual responses to whole-body yaw-plane step rotations were: (1) Briefer and (2) uncorrelated (controls' reflex and perception were correlated). Voxel-based morphometry showed a selective gray matter (GM) reduction in dancers' vestibular cerebellum correlating with ballet experience. Dancers' vestibular cerebellar GM density reduction was related to shorter perceptual responses (i.e. positively correlated) but longer VOR duration (negatively correlated). Contrastingly, controls' vestibular cerebellar GM density negatively correlated with perception and VOR. Diffusion-tensor imaging showed that cerebral cortex white matter (WM) microstructure correlated with vestibular perception but only in controls. In summary, dancers display vestibular perceptuo-reflex dissociation with the neuronatomical correlate localized to the vestibular cerebellum. Controls' robust vestibular perception correlated with a cortical WM network conspicuously absent in dancers. Since primary vestibular afferents synapse in the vestibular cerebellum, we speculate that a cerebellar gating of perceptual signals to cortical regions mediates the training-related attenuation of vestibular perception and perceptuo-reflex uncoupling