The bilateral anatomical organization of the vestibular system provides three functional advantages: optimal differentiation of head motion and orientation, sensory substitution of a unilateral ...peripheral failure, and central compensation of a peripheral or central vestibular tone imbalance. The structure is based on bilaterally ascending and descending pathways and at least four crossings: three in the brain stem and one in the cortex. The resulting sensorimotor functions can be subdivided into three major groups: (1) reflexive control of gaze, head, and body in three spatial planes (yaw, pitch, roll) at the brain stem/cerebellar level; (2) perception of self‐motion and control of voluntary movement and balance at the cortical/subcortical level; and (3) higher vestibular cognitive functions (e.g., spatial memory and navigation). The bilateral representation of the vestibular system in multiple multisensory cortical areas and the vestibular dominance of the nondominant hemisphere raise the question of how one global percept of motion and orientation in space is formed.
To review current knowledge of the perception of verticality, its normal function and disorders. This is based on an integrative graviceptive input from the vertical semicircular canals and the ...otolith organs.
The special focus is on human psychophysics, neurophysiological and imaging data on the adjustments of subjective visual vertical (SVV) and the subjective postural vertical. Furthermore, examples of mathematical modeling of specific vestibular cell functions for orientation in space in rodents and in patients are briefly presented.
Pathological tilts of the SVV in the roll plane are most sensitive and frequent clinical vestibular signs of unilateral lesions extending from the labyrinths via the brainstem and thalamus to the parieto-insular vestibular cortex. Due to crossings of ascending graviceptive fibers, peripheral vestibular and pontomedullary lesions cause ipsilateral tilts of the SVV; ponto-mesencephalic lesions cause contralateral tilts. In contrast, SVV tilts, which are measured in unilateral vestibular lesions at thalamic and cortical levels, have two different characteristic features: (i) they may be ipsi- or contralateral, and (ii) they are smaller than those found in lower brainstem or peripheral lesions. Motor signs such as head tilt and body lateropulsion, components of ocular tilt reaction, are typical for vestibular lesions of the peripheral vestibular organ and the pontomedullary brainstem (vestibular nucleus). They are less frequent in midbrain lesions (interstitial nucleus of Cajal) and rare in cortical lesions. Isolated body lateropulsion is chiefly found in caudal lateral medullary brainstem lesions. Vestibular function in the roll plane and its disorders can be mathematically modeled by an attractor model of angular head velocity cell and head direction cell function. Disorders manifesting with misperception of the body vertical are the pusher syndrome, the progressive supranuclear palsy, or the normal pressure hydrocephalus; they may affect roll and/or pitch plane.
Clinical determinations of the SVV are easy and reliable. They indicate acute unilateral vestibular dysfunctions, the causative lesion of which extends from labyrinth to cortex. They allow precise topographical diagnosis of side and level in unilateral brainstem or peripheral vestibular disorders. SVV tilts may coincide with or differ from the perception of body vertical, e.g., in isolated body lateropulsion.
Vestibular migraine (VM) is the most common cause of episodic vertigo in adults as well as in children. The diagnostic criteria of the consensus document of the International Bárány Society for ...Neuro-Otology and the International Headache Society (2012) combine the typical signs and symptoms of migraine with the vestibular symptoms lasting 5 min to 72 h and exclusion criteria. Although VM accounts for 7 % of patients seen in dizziness clinics and 9 % of patients seen in headache clinics it is still underdiagnosed. This review provides an actual overview on the pathophysiology, the clinical characteristics to establish the diagnosis, the differential diagnosis, and the treatment of VM.
To present evidence of a functional interrelation between the vestibular and the anxiety systems based on a complex reciprocally organized network. The review focuses on the differential effects of ...various vestibular disorders, on psychiatric comorbidity, and on anxiety related to vertigo.
Episodic vertigo syndromes such as vestibular migraine, vestibular paroxysmia, and Menière's disease are associated with a significant increase of psychiatric comorbidity, in particular anxiety/phobic disorders and depression. Chronic unilateral and bilateral vestibulopathy (BVP) do not exhibit a higher than normal psychiatric comorbidity. Anxiety related to the vertigo symptoms is also increased in episodic structural vestibular disorders but not in patients with chronic unilateral or bilateral loss of vestibular function. The lack of vertigo-related anxiety in BVP is a novel finding. Several studies have revealed special features related to anxiety in patients suffering from BVP: despite objectively impaired postural balance with frequent falls, they usually do not complain about fear of falling; they do not report an increased susceptibility to fear of heights; they do not have an increased psychiatric comorbidity; and they do not report increased anxiety related to the perceived vertigo. Subtle or moderate vestibular stimulation (by galvanic currents or use of a swing) may have beneficial effects on stress or mood state in healthy adults, and promote sleep in humans and rodents. The intimate structural and functional linkage of the vestibular and anxiety systems includes numerous nuclei, provincial and connector hubs, the thalamocortical network, and the cerebellum with many neural transmitter systems.
The different involvement of emotional processes and anxiety - to the extent of 'excess anxiety' or 'less anxiety' - in structural vestibular disorders may be due to the specific dysfunction and whether the system activity is excited or diminished. Both psychiatric comorbidity and vertigo-related anxiety are maximal with excitation and minimal with loss of peripheral vestibular function.
This review summarizes our current knowledge of multisensory vestibular structures and their functions in humans. Most of it derives from brain activation studies with PET and fMRI conducted over the ...last decade. The patterns of activations and deactivations during caloric and galvanic vestibular stimulations in healthy subjects have been compared with those in patients with acute and chronic peripheral and central vestibular disorders. Major findings are the following: (1) In patients with vestibular neuritis the central vestibular system exhibits a spontaneous visual-vestibular activation–deactivation pattern similar to that described in healthy volunteers during unilateral vestibular stimulation. In the acute stage of the disease regional cerebral glucose metabolism (rCGM) increases in the multisensory vestibular cortical and subcortical areas, but simultaneously it significantly decreases in the visual and somatosensory cortex areas. (2) In patients with bilateral vestibular failure the activation–deactivation pattern during vestibular caloric stimulation shows a decrease of activations and deactivations. (3) Patients with lesions of the vestibular nuclei due to Wallenberg's syndrome show no activation or significantly reduced activation in the contralateral hemisphere during caloric irrigation of the ear ipsilateral to the lesioned side, but the activation pattern in the ipsilateral hemisphere appears ‘normal’. These findings indicate that there are bilateral ascending vestibular pathways from the vestibular nuclei to the vestibular cortex areas, and the contralateral tract crossing them is predominantly affected. (4) Patients with posterolateral thalamic infarctions exhibit significantly reduced activation of the multisensory vestibular cortex in the ipsilateral hemisphere, if the ear ipsilateral to the thalamic lesion is stimulated. Activation of similar areas in the contralateral hemisphere is also diminished but to a lesser extent. These data demonstrate the functional importance of the posterolateral thalamus as a vestibular gatekeeper. (5) In patients with vestibulocerebellar lesions due to a bilateral floccular deficiency, which causes downbeat nystagmus (DBN), PET scans reveal that rCGM is reduced in the region of the cerebellar tonsil and flocculus/paraflocculus bilaterally. Treatment with 4-aminopyridine lessens this hypometabolism and significantly improves DBN. These findings support the hypothesis that the (para-) flocculus and tonsil play a crucial role in DBN. Although we can now for the first time attribute particular activations and deactivations to functional deficits in distinct vestibular disorders, the complex puzzle of the various multisensory and sensorimotor functions of the phylogenetically ancient vestibular system is only slowly being unraveled.
Objective
Vestibular evoked myogenic potentials (VEMPs) have been suggested as biomarkers in the differential diagnosis of Menière’s disease (MD) and vestibular migraine (VM). The aim of this study ...was to compare the degree of asymmetry for ocular (o) and cervical (c) VEMPs in large cohorts of patients with MD and VM and to follow up the responses.
Study design
Retrospective study in an interdisciplinary tertiary center for vertigo and balance disorders.
Methods
cVEMPs to air-conducted sound and oVEMPs to bone-conducted vibration were recorded in 100 patients with VM and unilateral MD, respectively. Outcome parameters were asymmetry ratios (ARs) of oVEMP n10p15 and cVEMP p13n23 amplitudes, and of the respective latencies (mean ± SD).
Results
The AR of cVEMP p13n23 amplitudes was significantly higher for MD (0.43 ± 0.34) than for VM (0.26 ± 0.24; adjusted
p
= 0.0002). MD—but not VM—patients displayed a higher AR for cVEMP than for oVEMP amplitudes (MD 0.43 ± 0.34 versus 0.23 ± 0.22,
p
< 0.0001; VM 0.26 ± 0.14 versus 0.19 ± 0.15,
p
= 0.11). Monitoring of VEMPs in single patients indicated stable or fluctuating amplitude ARs in VM, while ARs in MD appeared to increase or remain stable over time. No differences were observed for latency ARs between MD and VM.
Conclusions
These results are in line with (1) a more common saccular than utricular dysfunction in MD and (2) a more permanent loss of otolith function in MD versus VM. The different patterns of o- and cVEMP responses, in particular their longitudinal assessment, might add to the differential diagnosis between MD and VM.
Visually-induced self-motion perception (vection) relies on interaction of the visual and vestibular systems. Neuroimaging studies have identified a lateralization of the thalamo-cortical ...multisensory vestibular network, with left-handers exhibiting a dominance of the left hemisphere and right-handers exhibiting a dominance of the right hemisphere. Using electroencephalography (EEG), we compare the early processing of a vection-consistent visual motion stimulus against a vection-inconsistent stimulus, to investigate the temporal activation of the vection network by visual motion stimulation and the lateralization of these processes in left- versus right-handers. In both groups, vection-consistent stimulation evoked attenuated central event-related potentials (ERPs) in an early (160-220 ms) and a late (260-300 ms) time window. Differences in estimated source activity were found across visual, sensorimotor, and multisensory vestibular cortex in the early window, and were observed primarily in the posterior cingulate, retrosplenial cortex, and precuneus in the late window. Group comparisons revealed a larger ERP condition difference (i.e. vection-consistent stimulation minus vection-inconsistent stimulation) in left-handers, which was accompanied by group differences in the cingulate sulcus visual (CSv) area. Together, these results suggest that handedness may influence ERP responses and activity in area CSv during vection-consistent and vection-inconsistent visual motion stimulation.
•Longitudinal assessment of rat whole-brain networks during vestibular compensation.•Visualization of short-term changes in metabolic connectivity by 18F-FDG-PET.•Vestibular asymmetry results in ...recruitment and recalibration of multiple networks.•Cerebral metabolic connectivity follows the course of the behavioral recovery.
Unilateral damage to the inner ear results in an acute vestibular syndrome, which is compensated within days to weeks due to adaptive cerebral plasticity. This process, called central vestibular compensation (VC), involves a wide range of functional and structural mechanisms at the cellular and network level. The short-term dynamics of whole-brain functional network recruitment and recalibration during VC has not been depicted in vivo. The purpose of this study was to investigate the interplay of separate and distinct brain regions and in vivo networks in the course of VC by sequential 18F-FDG-PET-based statistical and graph theoretical analysis with the aim of revealing the metabolic connectome before and 1, 3, 7, and 15 days post unilateral labyrinthectomy (UL) in the rat. Temporal changes in metabolic brain connectivity were determined by Pearson's correlation (|r| > 0.5, p < 0.001) of regional cerebral glucose metabolism (rCGM) in 57 segmented brain regions. Metabolic connectivity analysis was compared to univariate voxel-wise statistical analysis of rCGM over time and to behavioral scores of static and dynamic sensorimotor recovery. Univariate statistical analysis revealed an ipsilesional relative rCGM decrease (compared to baseline) and a contralesional rCGM increase in vestibular and limbic networks and an increase in bilateral cerebellar and sensorimotor networks. Quantitative analysis of the metabolic connections showed a maximal increase from baseline to day 3 post UL (interhemispheric: 2-fold, ipsilesional: 3-fold, contralesional: 12-fold) and a gradual decline until day 15 post UL, which paralleled the dynamics of vestibular symptoms. In graph theoretical analysis, an increase in connectivity occurred especially within brain regions associated with brainstem-cerebellar and thalamocortical vestibular networks and cortical sensorimotor networks. At the symptom peak (day 3 post UL), brain networks were found to be organized in large ensembles of distinct and highly connected hubs of brain regions, which separated again with progressing VC. Thus, we found rapid changes in network organization at the subcortical and cortical level and in both hemispheres, which may indicate an initial functional substitution of vestibular loss and subsequent recalibration and reorganization of sensorimotor networks during VC.
This historical review on the semantic evolution of human senses and sensors revealed that Aristotle’s list of the five senses sight, hearing, touch, taste, and smell is still in use among ...non-scientific lay persons. It is no surprise that his classification in the work “De Anima” (On the Soul) from 350 BC confuses the sensor “touch” with the now more comprehensively defined somatosensory system and that senses are missing such as the later discovered vestibular system and the musculotendinous proprioception of the position of parts of the body in space. However, it is surprising that in the three most influential ancient cultures, Egypt, Greece, and China—which shaped the history of civilization—the concept prevailed that the heart rather than the brain processes perception, cognition, and emotions. This “cardiocentric view” can be traced back to the “Doctrine of Aristotle,” the “Book of the Dead” in ancient Egypt, and the traditional Chinese medicine of correspondence documented in the book “Huang di Neijing.” In Greek antiquity the philosophers Empedocles, Democritus and Aristotle were proponents of the allocation of the spirit and the soul to the heart connected to the body via the blood vessels. Opponents were the pre-Socratic mathematician Pythagoras, the philosopher Plato, and especially the Greek physician Hippocrates who regarded the brain as the most powerful organ in humans in his work “De Morbo Sacro.” The Greek physician Galen of Pergamon further elaborated on the concept of the brain (“cephalocentric hypothesis”) connected to the body by a network of nerves. The fundamental concepts for understanding functions and disorders of the vestibular system, the perception of self-motion, verticality and balance control were laid by a remarkable group of 19th century scientists including Purkynӗ, Mach, Breuer, Helmholtz, and Crum-Brown. It was also in the 19th century that Bell described a new sense of a reciprocal sensorimotor loop between the brain and the muscles which he called “muscular sense,” later termed “kinaesthesia” by Bastian and defined in 1906 as “proprioception” by Sherrington as “the perception of joint and body movements as well as position of the body or body segments, in space.” Both, the vestibular system and proprioception could be acknowledged as senses six or seven. However, we hesitate to recommend “pain”—which is variously assigned to the somatosensory system or extero-, intero-, visceroception—as a separate sensory system. Pain sensors are often not specific but have multisensory functions. Because of this inconsistent, partly contradictory classification even by experts in the current literature on senses and sensors we consider it justified to recommend a comprehensive reorganization of classification features according to the present state of knowledge with an expansion of the number of senses. Such a project has also to include the frequent task-dependent multisensory interactions for perceptual and sensorimotor achievements, and higher functions or disorders of the visual and vestibular systems as soon as cognition or emotions come into play. This requires a cooperation of sensory physiologists, neuroscientists and experienced physicians involved in the management of patients with sensory and multisensory disorders.
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