Electrical stimulation of the peripheral and central vestibular system.

PURPOSE OF REVIEW: Electrical stimulation of the peripheral and central vestibular system using noninvasive (galvanic vestibular stimulation, GVS) or invasive (intracranial electrical brain stimulation, iEBS) approaches have a long history of use in studying self-motion perception and balance control. The aim of this review is to summarize recent electrophysiological studies of the effects of GVS, and functional mapping of the central vestibular system using iEBS in awake patients. RECENT FINDINGS: The use of GVS has become increasingly common in the assessment and treatment of a wide range of clinical disorders including vestibulopathy and Parkinson's disease. The results of recent single unit recording studies have provided new insight into the neural mechanisms underlying GVS-evoked improvements in perceptual and motor responses. Furthermore, the application of iEBS in patients with epilepsy or during awake brain surgery has provided causal evidence of vestibular information processing in mostly the middle cingulate cortex, posterior insula, inferior parietal lobule, amygdala, precuneus, and superior temporal gyrus. SUMMARY: Recent studies have established that GVS evokes robust and parallel activation of both canal and otolith afferents that is significantly different from that evoked by natural head motion stimulation. Furthermore, there is evidence that GVS can induce beneficial neural plasticity in the central pathways of patients with vestibular loss. In addition, iEBS studies highlighted an underestimated contribution of areas in the medial part of the cerebral hemispheres to the cortical vestibular network.

Understanding the neural bases of bodily self-consciousness: recent achievements and main challenges.

The last two decades have seen a surge of interest in the mechanisms underpinning bodily self-consciousness (BSC). Studies showed that BSC relies on several bodily experiences (i.e., self-location, body ownership, agency, first-person perspective) and multisensory integration. The aim of this literature review is to summarize new insights and novel developments into the understanding of the neural bases of BSC, such as the contribution of the interoceptive signals to the neural mechanisms of BSC, and the overlap with the neural bases of conscious experience in general and of higher-level forms of self (i.e., the cognitive self). We also identify the main challenges and propose future perspectives that need to be conducted to progress into the understanding of the neural mechanisms of BSC. In particular, we point the lack of crosstalk and cross-fertilization between subdisciplines of integrative neuroscience to better understand BSC, especially the lack of research in animal models to decipher the neural networks and systems of neurotransmitters underpinning BSC. We highlight the need for more causal evidence that specific brain areas are instrumental in generating BSC and the need for studies tapping into interindividual differences in the phenomenal experience of BSC and their underlying mechanisms.

Visual perspective, distance, and felt presence of others in dreams.

The peripersonal space, that is, the limited space surrounding the body, involves multisensory coding and representation of the self in space. Previous studies have shown that peripersonal space representation and the visual perspective on the environment can be dramatically altered when neurotypical individuals self-identify with a distant avatar (i.e., in virtual reality) or during clinical conditions (i.e., out-of-body experience, heautoscopy, depersonalization). Despite its role in many cognitive/social functions, the perception of peripersonal space in dreams, and its relationship with the perception of other characters (interpersonal distance in dreams), remain largely uncharted. The present study aimed to explore the visuospatial properties of this space, which is likely to underlie self-location as well as self/other distinction in dreams. 530 healthy volunteers answered a web-based questionnaire to measure their dominant visuo-spatial perspective in dreams, the frequency of recall for felt distances between their dream self and other dream characters, and the dreamers' viewing angle of other dream characters. Most participants reported dream experiences from a first-person perspective (1PP) (82%) compared to a third-person perspective (3PP) (18%). Independent of their dream perspective, participants reported that they generally perceived other dream characters in their close space, that is, at distance of either between 0 and 90 cm, or 90-180 cm, than in further spaces (180-270 cm). Regardless of the perspective (1PP or 3PP), both groups also reported more frequently seeing other dream characters from eye level (0° angle of viewing) than from above (30° and 60°) or below eye level (-30° and -60°). Moreover, the intensity of sensory experiences in dreams, as measured by the Bodily Self-Consciousness in Dreams Questionnaire, was higher in individuals who habitually see other dream characters closer to their personal dream self (i.e., within 0-90 cm and 90-180 cm). These preliminary findings offer a new, phenomenological account of space representation in dreams with regards to the felt presence of others. They might provide insights not only to our understanding of how dreams are formed, but also to the type of neurocomputations involved in self/other distinction.

Vestibular rehabilitation improves spontaneous nystagmus normalization in patients with acute unilateral vestibulopathy.

Introduction: Spontaneous nystagmus (SN) can be observed after acute unilateral vestibulopathy (AUVP). The slow phase eye velocity of the SN progressively decreases in darkness as the result of rebalanced neurophysiological activity between both vestibular nuclei, a process that can take several months. Although this compensatory process can occur spontaneously, there is poor evidence that vestibular rehabilitation (VR) can facilitate the process. Methods: We documented the natural time course of SN reduction in patients with AUVP, as well as the effects of VR by means of a unilateral rotation paradigm. In a retrospective study (Study 1: n = 126 AUVP patients), we compared the time course of the SN reduction in patients with VR (n = 33) and without VR (n = 93). In a prospective study (Study 2: n = 42 AUVP patients), we compared the effects of early VR (n = 22; initiated within the first two weeks of symptoms onset) or late VR (n = 20; initiated after the second week of symptoms onset) on the time course of the SN reduction. Results: Study 1 showed shorter median time of SN normalization in patients with VR compared to patients without VR (14 days and 90 days, respectively). Study 2 showed that AUVP patients with early and late VR had a similar median time of SN normalization. The SN slow phase eye velocity was significantly decreased as early as the end of the first VR session in both groups, and kept decreasing at each subsequent VR session. In the early VR group, 38% of the patients had slow phase eye velocity below 2°/s after the first VR session, 100% after the fifth session. Similar findings were observed in the late VR group. Discussion: Taken together, these results indicate that VR with a unidirectional rotation paradigm speeds up the normalization of SN. This effect seems independent of the time between symptoms onset and commencement of VR, but early intervention is recommended to speed up the SN reduction.

The origin of pleasant sensations: Insight from direct electrical brain stimulation.

Research into the neuroanatomical basis of emotions has resulted in a plethora of studies over the last twenty years. However, studies about positive emotions and pleasant sensations remain rare and their anatomical-functional bases are less understood than that of negative emotions. Pleasant sensations can be evoked by electrical brain stimulations (EBS) during stereotactic electroencephalography (SEEG) performed for pre-surgical exploration in patients with drug-resistant epilepsy. We conducted a retrospective analysis of 10 106 EBS performed in 329 patients implanted with SEEG in our epileptology department. We found that 13 EBS in 9 different patients evoked pleasant sensations (.60% of all responses). By contrast we collected 111 emotional responses of negative valence (i.e., 5.13% of all responses). EBS evoking pleasant sensations were applied at 50 Hz with an average intensity of 1.4 ± .55 mA (range .5-2 mA). Pleasant sensations were reported by nine patients of which three patients presented responses to several EBS. We found a male predominance among the patients reporting pleasant sensations and a prominent role of the right cerebral hemisphere. Results show the preponderant role of the dorsal anterior insula and amygdala in the occurrence of pleasant sensations.

Neural bases of the bodily self as revealed by electrical brain stimulation: A systematic review.

An increasing amount of recent research has focused on the multisensory and neural bases of the bodily self. This pre-reflective form of self is considered as multifaceted, incorporating phenomenal components, such as self location, body ownership, first-person perspective, agency, and the perceptual body image. Direct electrical brain stimulation (EBS) during presurgical evaluation of epilepsy and brain tumor resection is a unique method to causally relate specific brain areas to the various phenomenal components of the bodily self. We conducted a systematic review of the literature describing altered phenomenal experience of the bodily self evoked by EBS. We included 42 articles and analyzed self reports from 221 patients. Three-dimensional density maps of EBS revealed that stimulation in the middle cingulum, inferior parietal lobule, supplementary motor area, posterior insula, hippocampal complex/amygdala, and precuneus most consistently altered one or several components of the bodily self. In addition, we found that only EBS in the parietal cortex induced disturbances of all five components of the bodily self considered in this review article. These findings inform current neuroscientific models of the bodily self.

Navigation strategies in patients with vestibular loss tested in a virtual reality T-maze.

During navigation, humans mainly rely on egocentric and allocentric spatial strategies, two different frames of reference working together to build a coherent representation of the environment. Spatial memory deficits during navigation have been repeatedly reported in patients with vestibular disorders. However, little is known about how vestibular disorders can change the use of spatial navigation strategies. Here, we used a new reverse T-maze paradigm in virtual reality to explore whether vestibular loss specifically modifies the use of egocentric or allocentric spatial strategies in patients with unilateral (n = 23) and bilateral (n = 23) vestibular loss compared to healthy volunteers (n = 23) matched for age, sex and education level. Results showed that the odds of selecting and using a specific strategy in the T-maze were significantly reduced in both unilateral and bilateral vestibular loss. An exploratory analysis suggests that only right vestibular loss decreased the odds of adopting a spatial strategy, indicating an asymmetry of vestibular functions. When considering patients who used strategies to navigate, we observed that a bilateral vestibular loss reduced the odds to use an allocentric strategy, whereas a unilateral vestibular loss decreased the odds to use an egocentric strategy. Age was significantly associated with an overall lower chance to adopt a navigation strategy and, more specifically, with a decrease in the odds of using an allocentric strategy. We did not observe any sex difference in the ability to select and use a specific navigation strategy. Findings are discussed in light of previous studies on visuo-spatial abilities and studies of vestibulo-hippocampal interactions in peripheral vestibular disorders. We discuss the potential impact of the history of the disease (chronic stage in patients with a bilateral vestibulopathy vs. subacute stage in patients with a unilateral vestibular loss), of hearing impairment and non-specific attentional deficits in patients with vestibular disorders.

Vestibular-Evoked Cerebral Potentials.

The human vestibular cortex has mostly been approached using functional magnetic resonance imaging and positron emission tomography combined with artificial stimulation of the vestibular receptors or nerve. Few studies have used electroencephalography and benefited from its high temporal resolution to describe the spatiotemporal dynamics of vestibular information processing from the first milliseconds following vestibular stimulation. Evoked potentials (EPs) are largely used to describe neural processing of other sensory signals, but they remain poorly developed and standardized in vestibular neuroscience and neuro-otology. Yet, vestibular EPs of brainstem, cerebellar, and cortical origin have been reported as early as the 1960s. This review article summarizes and compares results from studies that have used a large range of vestibular stimulation, including natural vestibular stimulation on rotating chairs and motion platforms, as well as artificial vestibular stimulation (e.g., sounds, impulsive acceleration stimulation, galvanic stimulation). These studies identified vestibular EPs with short latency (<20 ms), middle latency (from 20 to 50 ms), and late latency (>50 ms). Analysis of the generators (source analysis) of these responses offers new insights into the neuroimaging of the vestibular system. Generators were consistently found in the parieto-insular and temporo-parietal junction-the core of the vestibular cortex-as well as in the prefrontal and frontal areas, superior parietal, and temporal areas. We discuss the relevance of vestibular EPs for basic research and clinical neuroscience and highlight their limitations.

Interoception and embodiment in patients with bilateral vestibulopathy.

There are tight functional and anatomical links between the vestibular and interoceptive systems, and both systems have shown to fundamentally underlie emotional processes and our sense of a bodily self. Yet, nothing is known about how long-term bilateral vestibulopathy (BVP) influences interoception and its relation to embodiment and the sense of self. We thus compared cardiac interoceptive accuracy, confidence in the performance, and general body awareness in 25 BVP patients and healthy controls using a heartbeat tracking task, self-reports about interoceptive awareness, as well as measures of self-localization and of self-body closeness. Results showed no difference between patients and controls regarding interoceptive accuracy, confidence and body awareness, suggesting that long-term BVP does not influence cardiac interoception. Patients and controls did not differ either regarding self-location and self-body closeness. However, in our overall sample of patients and controls, we found that interoceptive accuracy increased with perceived self-body closeness, suggesting that anchoring the self to the body is generally linked with better cardiac interoception. This result is in line with previous suggestions of an important contribution of interoception to the sense of embodiment.

Vestibular rehabilitation in Europe: a survey of clinical and research practice.

Vestibular rehabilitation (VR) is practiced across Europe but little in this area has been quantified. The aim of this study was to investigate current VR assessment, treatment, education, and research practices. This was an online, cross-sectional survey with 39 VR specific questions and four sections: demographics, current practice, education, and research. The survey was disseminated through the Dizzynet network to individual therapists through country-specific VR special interest groups. Results were analysed descriptively. A thematic approach was taken to analyse open questions. A total of 471 individuals (median age 41, range 23 - 68 years, 73.4% women), predominately physiotherapists (89.4%) from 20 European countries responded to the survey. They had worked for a median of 4 years (range < 1 - 35) in VR. The majority (58.7%) worked in hospital in-patient or out-patient settings and 21.4% in dedicated VR services. Most respondents specialized in neurology, care of the elderly (geriatrics), or otorhinolaryngology. VR was reported as hard/very hard to access by 48%, with the main barriers to access identified as lack of knowledge of health care professionals (particularly family physicians), lack of trained therapists, and lack of local services. Most respondents reported to know and treat benign paroxysmal positional vertigo (BPPV 87.5%), unilateral vestibular hypofunction (75.6%), and cervicogenic dizziness (63%). The use of vestibular assessment equipment varied widely. Over 70% used high-density foam and objective gait speed testing. Over 50% used dynamic visual acuity equipment. Infrared systems, Frenzel lenses, and dynamic posturography were not commonly employed (< 20%). The most frequently used physical outcome measures were the Clinical Test of the Sensory Interaction of Balance, Functional Gait Assessment/Dynamic Gait Index, and Romberg/Tandem Romberg. The Dizziness Handicap Inventory, Visual Analogue Scale, Falls Efficacy Scale, and the Vertigo Symptom Scale were the most commonly used patient reported outcome measures. Adaptation, balance, and habituation exercises were most frequently used (> 80%), with virtual reality used by 15.6%. Over 70% reported knowledge/use of Semont, Epley and Barbeque-Roll manoeuvres for the treatment of BPPV. Most education regarding VR was obtained at post-registration level (89.5%) with only 19% reporting pre-registration education. There was strong (78%) agreement that therapists should have professionally accredited postgraduate certification in VR, with blended learning the most popular mode. Three major research questions were identified for priority: management of specific conditions, effectiveness of VR, and mechanisms/factors influencing vestibular compensation and VR. In summary, the survey quantified current clinical practice in VR across Europe. Knowledge and treatment of common vestibular diseases was high, but use of published subjective and objective outcome measures as well as vestibular assessment varied widely. The results stress the need of improving both training of therapists and standards of care. A European approach, taking advantage of best practices in some countries, seems a reasonable approach.

Vestibular function and cortical and sub-cortical alterations in an aging population.

While it is well known that the vestibular system is responsible for maintaining balance, posture and coordination, there is increasing evidence that it also plays an important role in cognition. Moreover, a growing number of epidemiological studies are demonstrating a link between vestibular dysfunction and cognitive deficits in older adults; however, the exact pathways through which vestibular loss may affect cognition are unknown. In this cross-sectional study, we sought to identify relationships between vestibular function and variation in morphometry in brain structures from structural neuroimaging. We used a subset of 80 participants from the Baltimore Longitudinal Study of Aging, who had both brain MRI and vestibular physiological data acquired during the same visit. Vestibular function was evaluated through the cervical vestibular-evoked myogenic potential (cVEMP). The brain structures of interest that we analyzed were the hippocampus, amygdala, thalamus, caudate nucleus, putamen, insula, entorhinal cortex (ERC), trans-entorhinal cortex (TEC) and perirhinal cortex, as these structures comprise or are connected with the putative "vestibular cortex." We modeled the volume and shape of these structures as a function of the presence/absence of cVEMP and the cVEMP amplitude, adjusting for age and sex. We observed reduced overall volumes of the hippocampus and the ERC associated with poorer vestibular function. In addition, we also found significant relationships between the shape of the hippocampus (p = 0.0008), amygdala (p = 0.01), thalamus (p = 0.008), caudate nucleus (p = 0.002), putamen (p = 0.02), and ERC-TEC complex (p = 0.008) and vestibular function. These findings provide novel insight into the multiple pathways through which vestibular loss may impact brain structures that are critically involved in spatial memory, navigation and orientation.

Imagined paralysis alters somatosensory evoked-potentials.

Recent studies employing body illusions have shown that multisensory conflict can alter body representations and modulate low-level sensory processing. One defining feature of these body illusions is that they are sensory driven and thus passive on behalf of the participant. Thus, it remained to establish whether explicit alteration of own-body representations modulates low-level sensory processing. We investigated whether tibial nerve somatosensory-evoked potentials were modulated when participants imagined paralysis of their legs and arms. Imagined paralysis of the legs decreased P40 amplitude, but not imagined paralysis of the arms. These results show modulation of early somatosensory processing via explicit, top-down alteration to the internal representation of the body. Interestingly, P40 suppression positively correlated with bodily awareness scores whereas it negatively correlated with body dissociation scores. This suggests that the ability to actively alter own-body representation and its corresponding sensory processing depends upon dispositions to attend to and focus on bodily sensations.

Measuring perceived self-location in virtual reality.

Third-person perspective full-body illusions (3PP-FBI) enable the manipulation, through multisensory stimulation, of perceived self-location. Perceived self-location is classically measured by a locomotion task. Yet, as locomotion modulates various sensory signals, we developed in immersive virtual reality a measure of self-location without locomotion. Tactile stimulation was applied on the back of twenty-five participants and displayed synchronously or asynchronously on an avatar's back seen from behind. Participants completed the locomotion task and a novel mental imagery task, in which they self-located in relation to a virtual ball approaching them. Participants self-identified with the avatar more during synchronous than asynchronous visuo-tactile stimulation in both tasks. This was accentuated for the mental imagery task, showing a larger self-relocation toward the avatar, together with higher reports of presence, bi-location and disembodiment in the synchronous condition only for the mental imagery task. In conclusion, the results suggest that avoiding multisensory updating during walking, and using a perceptual rather than a motor task, can improve measures of illusory self-location.

Unilateral vestibular deafferentation impairs embodied spatial cognition.

A growing number of studies indicate that cognitive complaints are common in patients with peripheral vestibular disorders. A better understanding of how vestibular disorders influence cognition in these patients requires a clear delineation of the cognitive domains affected by vestibular disorders. Here, we compared the consequences of left and right vestibular neurectomy on third-person perspective taking-a visuo-spatial task requiring mainly own-body mental imagery, and on 3D objects mental rotation imagery-requiring object-based mental imagery, but no perspective taking. Patients tested 1 week after a unilateral vestibular neurectomy and a group of age- and gender-matched healthy participants played a virtual ball-tossing game from their own first-person perspective (1PP) and from the perspective of a distant avatar (third-person perspective, 3PP). Results showed larger response times in the patients with respect to their controls for the 3PP taking task, but not for the 1PP task and the 3D objects mental imagery. In addition, we found that only patients with left vestibular neurectomy presented altered 3PP taking abilities when compared to their controls. This study suggests that unilateral vestibular loss affects mainly own-body mental transformation and that only left vestibular loss seems to impair this cognitive process. Our study also brings further evidence that vestibular signals contribute to the sensorimotor bases of social cognition and strengthens the connections between the so far distinct fields of social neuroscience and human vestibular physiology.

The Tilted Self: Visuo-Graviceptive Mismatch in the Full-Body Illusion.

The bodily self is a fundamental part of human self-consciousness and relies on online multimodal information and prior beliefs about one's own body. While the contribution of the vestibular system in this process remains under-investigated, it has been theorized to be important. The present experiment investigates the influence of conflicting gravity-related visual and bodily information on the sense of a body and, vice versa, the influence of altered embodiment on verticality and own-body orientation perception. In a full-body illusion setup, participants saw in a head-mounted display a projection of their own body 2 m in front of them, on which they saw a tactile stimulation on their back displayed either synchronously or asynchronously. By tilting the seen body to one side, an additional visuo-graviceptive conflict about the body orientation was created. Self-identification with the seen body was measured explicitly with a questionnaire and implicitly with skin temperature. As measures of orientation with respect to gravity, we assessed subjective haptic vertical and the haptic body orientation. Finally, we measured the individual visual field dependence using the rod-and-frame test. The results show a decrease in self-identification during the additional visuo-graviceptive conflict, but no modulation of perceived verticality or subjective body orientation. Furthermore, explorative analyses suggest a stimulation-dependent modulation of the perceived body orientation in individuals with a strong visual field dependence only. The results suggest a mutual interaction of graviceptive and other sensory signals and the individual's weighting style in defining our sense of a bodily self.