Temporal Relationship between Nystagmus and Perception during Bithermal Alternate Caloric Test

Objectives: During caloric irritation, the spinning/rotating sensation is predominant. However, there is no report on the temporal relationship between caloric nystagmus and perception.Methods: Consecutive 57 participants underwent bithermal caloric test in the dizziness clinic of Chungnam National University Hospital from February 2018 to September 2018. For vestibular perception, we asked the subject to report feelings of rotation and/or linear sensation during each warm and cold water irrigation period. Besides routine caloric parameters, the duration of nystagmus and vestibular sensation were analyzed.Results: In most participants, the caloric nystagmus preceded the vestibular sensation (79.6% in right warm, 83.3% in left warm, 88.5% in right cool, and 84.6% in left cool stimuli). The precedence of perception was observed in 5 normal persons and 15 patients with vestibular migraine (n=4), unilateral vestibulopathy (n=3), and Menière’s disease (n=2), multiple systemic atrophy (n=2), cerebellar ataxia (n=2), vertebrobasilar insufficiency (n=1), and post-earthquake dizziness (n=1). The mean latency between nystagmus and perception was 11.7 seconds. And the duration of nystagmus was longer than that of perception in all conditions. Non-spinning sensations during the caloric test were also observed in some participants (26.8% in right warm, 30.3% in left warm, 29.1% in right cool, and 24.1% in left cool stimuli).Conclusions: During the bithemal alternate caloric test, various vestibular perception and temporal relationship between perception and nystagmus suggest the bithermal caloric stimulation does not reflect only the signal originating from the horizontal canal pathway. A further validation study is needed.

Vestibular Agnosia is linked to abnormal functional brain networks

Activation of the peripheral vestibular apparatus simultaneously elicits a reflex vestibular nystagmus and the vestibular perception of self-motion (vestibular-motion perception) or vertigo. In a newly characterised condition called Vestibular Agnosia found in conditions with disrupted brain network connectivity, e.g. traumatic brain injury (TBI) or neurodegeneration (Parkinson’s Disease), the link between vestibular reflex and perception is uncoupled, such that, peripheral vestibular activation elicits a vestibular ocular reflex nystagmus but without vertigo. Using structural brain imaging in acute traumatic brain injury, we recently linked vestibular agnosia to postural imbalance via disrupted right temporal white-matter circuits (inferior longitudinal fasciculus), however no white-matter tracts were specifically linked to vestibular agnosia. Given the relative difficulty in localizing the neuroanatomical correlates of vestibular-motion perception, and compatible with current theories of human consciousness (viz. the Global Neuronal Workspace Theory), we postulate that vestibular-motion perception (vertigo) is mediated by the coordinated interplay between fronto-parietal circuits linked to whole-brain broadcasting of the vestibular signal of self-motion. We thus used resting state functional MRI (rsfMRI) to map functional brain networks and hence test our postulate of an anterior-posterior cortical network mediating vestibular agnosia. Whole-brain rsfMRI was acquired from 39 prospectively recruited acute TBI patients (and 37 matched controls) with preserved peripheral and reflex vestibular function, along with self-motion perceptual thresholds during passive yaw rotations in the dark, and posturography. Following quality control of the brain imaging, 25 TBI patients’ images were analyzed. We classified 11 TBI patients with vestibular agnosia and 14 without vestibular agnosia based on laboratory testing of self-motion perception. Using independent component analysis, we found altered functional connectivity within posterior (right superior longitudinal fasciculus) and anterior networks (left rostral prefrontal cortex) in vestibular agnosia. Regions of interest analyses showed both inter-hemispheric and intra-hemispheric (left anterior-posterior) network disruption in vestibular agnosia. Assessing the brain regions linked via right inferior longitudinal fasciculus, a tract linked to vestibular agnosia in unbalanced patients (but now controlled for postural imbalance), seed-based analyses showed altered connectivity between higher order visual cortices involved in motion perception and mid-temporal regions. In conclusion, vestibular agnosia in our patient group is mediated by multiple brain network dysfunction, involving primarily left frontal and bilateral posterior networks. Understanding the brain mechanisms of vestibular agnosia provide both an insight into the physiological mechanisms of vestibular perception as well as an opportunity to diagnose and monitor vestibular cognitive deficits in brain disease such as TBI and neurodegeneration linked to imbalance and spatial disorientation.

Reduced vestibular perception thresholds in persistent postural-perceptual dizziness- a cross-sectional study

Background Persistent postural-perceptual dizziness (PPPD) is the most common functional vestibular disorder. A multisensory mismatch altered by psychological influences is considered to be an important pathophysiological mechanism. Increased cortical and subcortical excitability may play a role in the pathophysiology of PPPD. We hypothesized that decreased motion perception thresholds reflect one mechanism of the abnormal vestibular responsiveness in this disorder. We investigated the vestibular perception thresholds and the vestibular ocular reflex with a rotatory chair experiment to gain insights in the processing and adaption to vestibular provocation. Methods In this cross-sectional study 26 female PPPD patients and 33 healthy female age matched controls (HC) were investigated sitting in a motorized rotary chair shielded regarding visual and acoustic stimuli. The chair was rotated for 20 minutes with slowly increasing velocity to a maximum of 72°/s. We functionally tested motion perception thresholds and vegetative responses to rotation as well as vestibular-ocular reflex thresholds. We additionally investigated several psychological comorbidities (i.e. depression, anxiety, somatosensory amplification) using validated scores. Conventional dizziness scores were obtained to quantify the experienced dizziness and impact on daily life. Results PPPD patients showed a significant reduced vestibulo-perceptual threshold (PPPD: 10.9°/s vs. HC: 29.5°/s; p<0.001) with increased motion sensitivity and concomitant vegetative response during and after the chair rotation compared to healthy controls. The extent of increased vestibular sensitivity was in correlation with the duration of the disease (p=0.043). No significant difference was measured regarding nystagmus parameters between both groups. Conclusion PPPD patients showed increased vegetative response as well as decreased vestibulo-perceptual thresholds which are related to disease duration. This is of interest as PPPD might be sustained by increased vestibular excitability leading to motion intolerance and induction of dizziness when exposed to movement.

Delineating neural responses and functional connectivity changes during vestibular and nociceptive stimulation reveal the uniqueness of cortical vestibular processing

Vestibular information is ubiquitous and often processed jointly with visual, somatosensory and proprioceptive information. Among the cortical brain regions associated with human vestibular processing, area OP2 in the parietal operculum has been proposed as vestibular core region. However, delineating responses uniquely to vestibular stimulation in this region using neuroimaging is challenging for several reasons: First, the parietal operculum is a cytoarchitectonically heterogeneous region responding to multisensory stimulation. Second, artificial vestibular stimulation evokes confounding somatosensory and nociceptive responses blurring responses contributing to vestibular perception. Furthermore, immediate effects of vestibular stimulation on the organization of functional networks have not been investigated in detail yet. Using high resolution neuroimaging in a task-based and functional connectivity approach, we compared two equally salient stimuli—unilateral galvanic vestibular (GVS) and galvanic nociceptive stimulation (GNS)—to disentangle the processing of both modalities in the parietal operculum and characterize their effects on functional network architecture. GNS and GVS gave joint responses in area OP1, 3, 4, and the anterior and middle insula, but not in area OP2. GVS gave stronger responses in the parietal operculum just adjacent to OP3 and OP4, whereas GNS evoked stronger responses in area OP1, 3 and 4. Our results underline the importance of considering this common pathway when interpreting vestibular neuroimaging experiments and underpin the role of area OP2 in central vestibular processing. Global network changes were found during GNS, but not during GVS. This lack of network reconfiguration despite the saliency of GVS may reflect the continuous processing of vestibular information in the awake human.

Rapid cross-sensory adaptation of self-motion perception

Perceptual adaptation is often studied within a single sense. However, our experience of the world is naturally multisensory. Here, we investigated cross-sensory (visual vestibular) adaptation of self motion perception. It was previously found that relatively long visual self-motion stimuli (greater or equal to 15s) are required to adapt subsequent vestibular perception, and that shorter duration stimuli do not elicit cross sensory (visual vestibular) adaptation. However, it is not known whether several discrete short duration stimuli may lead to cross sensory adaptation (even when their sum, if presented together, would be too short to elicit cross sensory adaptation). This would suggest that the brain monitors and adapts to supra modal statistics of events in the environment. Here we investigated whether cross sensory (visual vestibular) adaptation occurs after experiencing several short (1s) self-motion stimuli. Forty five participants discriminated the headings of a series of self motion stimuli. To expose adaptation effects, the trials were grouped in 140 batches, each comprising three prior trials, with headings biased to the right or left, followed by a single unbiased test trial. Right, and left biased batches were interleaved pseudo randomly. We found significant adaptation in both cross sensory conditions (visual prior and vestibular test trials, and vice versa), as well as both unisensory conditions (when prior and test trials were of the same modality, either visual or vestibular). Fitting the data with a logistic regression model revealed that adaptation was elicited by the prior stimuli (not prior choices). These results suggest that the brain monitors supra modal statistics of events in the environment, even for short duration stimuli, leading to functional (supra modal) adaptation of perception.

Delineating Neural Responses and Functional Connectivity Changes During Vestibular and Nociceptive Stimulation Reveal the Uniqueness of Cortical Vestibular Processing

Vestibular information is ubiquitous and often processed jointly with visual, somatosensory and proprioceptive information. Among the cortical brain regions associated with human vestibular processing, area OP2 in the parietal operculum has been proposed as vestibular core region. However, delineating responses uniquely to vestibular stimulation in this region using neuroimaging is challenging for several reasons: Firstly, the parietal operculum is a cytoarchitectonically heterogeneous region responding to multisensory stimulation. Secondly, artificial vestibular stimulation evokes confounding somatosensory and nociceptive responses blurring responses contributing to vestibular perception. Furthermore, immediate effects of vestibular stimulation on the organization of functional networks have not been investigated in detail yet.Here, we compared two equally salient stimuli - galvanic vestibular stimulation (GVS) and galvanic nociceptive stimulation (GNS)- to disentangle the processing of both modalities in the parietal operculum and characterize their effects on functional network architecture. GNS and GVS gave joint responses in area OP1,3,4, and the anterior and middle insula, but not in area OP2. Contrasting both stimulation modalities resulted in stronger responses in parts of the parietal operculum adjacent to OP3 and OP4 during GVS, whereas GNS evoked stronger responses in area OP1,3 and 4. Our results underline the importance of considering this common multisensory trunk when interpreting vestibular neuroimaging experiments and further underpin the role of area OP2 in central vestibular processing. Global network changes were found during GNS, but not during GVS. This lack of network reconfiguration despite the saliency of GVS may reflect the continuous processing of vestibular information in the awake human.

Spatial orientation during gondola centrifugation with subjects upright versus supine: Evidence for Gestalt psychological mechanisms in vestibular perception

BACKGROUND: Recent theories suggest that perception of complex self-motion is governed by familiarity of the motion pattern as a whole in 3D. OBJECTIVE: To explore how familiarity determines the perceived angular displacement with respect to the Earth during a simulated coordinated turn in a gondola centrifuge. METHOD: The centrifuge was accelerated to 2G (gondola displacement 60°) within 12.5 s. Using visual indicators in darkness, responses to the gondola displacement were recorded with subjects (n = 10) in two positions: sitting-upright, facing-forward versus lying-supine, feet-forwards. Each subject underwent 2×2 6-minute runs. RESULT: When upright, subjects indicated a tilt of initially 18.8±11.3°, declining with T = 66±37 s. In the supine position (subject’s yaw plane coinciding with the plane of gondola displacement) the indicated displacement was negligible (–0.3±4.8°). CONCLUSION: Since the canal system is most responsive to stimuli in yaw, these findings are difficult to explain by bottom-up models. Rather, the motion pattern during acceleration would be recognized as a familiar or meaningful whole (entering a co-ordinated turn) only when the subject is upright. Presumably, the degree of familiarity is reflected in the subject’s ability to discern and estimate a single stimulus component. Findings are discussed in connection with human factors in aviation and the principles of Gestalt psychology.

Vestibular Thresholds: A Review of Advances and Challenges in Clinical Applications

Vestibular disorders pose a substantial burden on the healthcare system due to a high prevalence and the severity of symptoms. Currently, a large portion of patients experiencing vestibular symptoms receive an ambiguous diagnosis or one that is based solely on history, unconfirmed by any objective measures. As patients primarily experience perceptual symptoms (e.g., dizziness), recent studies have investigated the use of vestibular perceptual thresholds, a quantitative measure of vestibular perception, in clinical populations. This review provides an overview of vestibular perceptual thresholds and the current literature assessing use in clinical populations as a potential diagnostic tool. Patients with peripheral and central vestibular pathologies, including bilateral vestibulopathy and vestibular migraine, show characteristic changes in vestibular thresholds. Vestibular perceptual thresholds have also been found to detect subtle, sub-clinical declines in vestibular function in asymptomatic older adults, suggesting a potential use of vestibular thresholds to augment or complement existing diagnostic methods in multiple populations. Vestibular thresholds are a reliable, sensitive, and specific assay of vestibular precision, however, continued research is needed to better understand the possible applications and limitations, especially with regard to the diagnosis of vestibular disorders.

Reduced Vestibular Perception Thresholds in Persistent Postural-Perceptual Dizziness- A Cross-Sectional Study

BACKGROUND: Persistent postural-perceptual dizziness (PPPD) is the most common functional vestibular disorder which is maintained by an interaction of psychological and physiological factors. PPPD patients develop inappropriate postural control strategies characterized by increased self-motion perception. Increased cortical and subcortical excitability may play a role in the pathophysiology of PPPD. We hypothesized that decreased motion perception thresholds reflect one mechanism of the abnormal vestibular responsiveness in this disorder. We investigated the vestibular perception thresholds and the vestibular ocular reflex with a rotatory chair experiment to gain insights in the processing and adaption to vestibular provocation. METHODS: In this cross-sectional study 26 female PPPD patients and 33 healthy female age and matched controls (HC) were investigated sitting in a motorized rotary chair shielded regarding visual and acoustic stimuli. The chair was rotated for 20 minutes with slowly increasing velocity to a maximum of 72°/s. We functionally tested motion perception thresholds and vegetative responses to rotation as well as vestibular-ocular reflex thresholds. We additionally investigated several psychological comorbidities (i.e. depression, anxiety, somatosensory amplification) using validated scores. Conventional dizziness scores were obtained to quantify the experienced dizziness and impact on daily life. RESULTS: PPPD patients showed a significant reduced vestibulo-perceptual threshold (PPPD: 10.9°/s vs. HC: 29.5°/s; p<0.001) with increased motion sensitivity and concomitant vegetative response during and after the chair rotation compared to healthy controls. The extent of increased vestibular sensitivity was in correlation with the duration of the disease (p=0.043). No significant difference was measured regarding nystagmus parameters between both groups.CONCLUSION: PPPD patients showed increased vegetative response as well as decreased vestibulo-perceptual thresholds which are related to disease duration. This is of interest as PPPD might be sustained by increased vestibular excitability leading to motion intolerance and induction of dizziness when exposed to movement.