: tenth revision. Annu. doi: 10.1523/JNEUROSCI.3988-03.2004, Salam, M., and Lehnen, N. (2014). They may see their visual field jiggle or bounce during head motion (oscillopsia) or have double vision (diplopia). DOI: 10.12751/g-node.sc1a64 Objective: We are still lacking a pathophysiological mechanism for functional disorders explaining the emergence and manifestation of characteristic, severely impairing bodily symptoms like chest pain or dizziness. 2021 | License CC BY-SA 4.0, These data contain eye and head velocity recordings during large gaze shifts. Both eye and head position and velocity were filtered with a low-pass Gaussian filter (cutoff frequency 20 Hz). . doi: 10.1177/014107687807101109, Rommelfanger, K. S., Factor, S. A., LaRoche, S., Rosen, P., Young, R., and Rapaport, M. H. (2017). A common debilitating symptom of Traumatic Brain Injury (TBI) is dizziness and balance issues. Of 43 gaze shifts in total, 34 2 (mean SEM) and 33 2 trials were taken into the analysis of mean CR and OSC gains, respectively, with no significant group differences [Wilks lambda (1,17) = 0.79, p = 0.15]. Data was recorded with the measuring system EyeSeeCam (EyeSeeTec GmbH, Munich). Geneva: World Health Organization. Functional neurological disorders: The neurological assessment as treatment. The original contributions presented in the study are publicly available. Because our vision plays a major role in our balance system, Oscillopsia brings with it many common symptoms seen in other vestibular disorders, such as BPPV, Visually-Induced Dizziness, and Meniere's Disease.. .. Vestibular rehabilitation therapy (VRT) is an . Neurosci. Beginning from the target position of the previous trial, quickly after the flashed target light (0, gray bar in A,B, and red spot in C) is extinguished, eyes and head begin to move jointly toward the remembered target position (dark spot in C) in a coordinated and voluntarily planned way, representing the start of the gaze shift movement (1). doi: 10.1007/s11682-019-00168-7, Martin, A., and Van Den Bergh, O. J. Neurol. Movement sequence over the course of a single 80 gaze shift. History and an extensive clinical workup including neurological exams, neuro-ophthalmological and neuro-otological exams, caloric irrigation, subjective visual vertical, laser ophthalmoscopy, posturography, video head impulse test (vHIT), head impulse testing devicefunctional test (HITD-FT; after Ramaioli et al., 2014), and cranial magnetic resonance imaging (MRI) did not show any organ pathology. Q. Altered brain function in persistent postural perceptual dizziness: A study on resting state functional connectivity. Medically Unexplained Symptoms and Bodily Distress: Four Challenges to Improve Understanding and Evidence-Based Care. Neurosurg. Please enable it to take advantage of the complete set of features! Anticipatory eye movements stabilize gaze during self-generated head movements. Psychosom. Lehnen, N. (2006). If the CNS fails to do so, e.g., in motion sickness (Money, 1970; Reason, 1978; Oman, 1982; Yardley, 1991; Oman and Cullen, 2014), the mismatch between expected and actual sensory input can elicit typical vertigo/dizziness feelings and nausea (Figure 1). A recent hypothesis reflecting this paradigm shift suggests that functional disorders emerge and manifest as a consequence of perceptual dysregulation in the central nervous system (CNS; Edwards et al., 2012; Van den Bergh et al., 2017; Henningsen et al., 2018; Pezzulo et al., 2019). 91, 496508. (2007). 71, 819829. doi: 10.3389/fneur.2018.00562, Lehnen, N., Schrder, L., Henningsen, P., Glasauer, S., and Ramaioli, C. (2019). 232, 24832492. Curr Opin Neurol. Summary: In every story worth telling, a hero would rise to the challenge of monsters and win the battle to save the world. Psychosom. This study investigates a dataset from patients with functional dizziness that has also been used in a prior publication (Lehnen et al., 2019). Would you like email updates of new search results? Psychiatr. The editor and reviewer's affiliations are the latest provided on their Loop research profiles and may not reflect their situation at the time of review. In patients >75 years, dizziness is the most common leading symptom ( 2 ). 1. Recognising and explaining functional neurological disorder. Exp. For me every time I got out of a car or walked up a flight of stairs if felt lightheaded and unstable. 2nd edition. (AD left), Results of group analysis (controls n = 11, patients n = 8). (2009). (2010). Typically, by using expectations that rely on internal models about the body and the environment, the CNS establishes congruence between the different sensory or sensorimotor input sources, enabling stable positioning in and orientation within the environment. Mnchen: Ludwig-Maximilians Universitt Mnchen, Doctoral dissertation. In the OSC epoch, compensatory eye movements did not differ between the healthy subject and the functional dizziness patient. A recent hypothesis based on the predictive coding theory of brain function suggests that in functional disorders, internal expectations do not match the actual sensory body states . Med. Physiol. 9, 16. Post hoc testing revealed that functional dizziness patients displayed significantly lower gaze stabilization than healthy subjects in the CR epoch (p = 0.036) but not the OSC epoch (p = 0.26). Neurobiol. All authors reviewed and edited the manuscript. 27, 191208. When the head has finished its motion toward the target position, the active movement is completed (3). Gaze gains were computed for two gaze stabilization epochs: the internally-driven CR epoch as part of the planned gaze shift, using internal expectations and sensory information for stabilization, and the sensory-driven OSC epoch for sensory-dependent gaze stabilization after gaze shift end. 80, 422431. NL designed the study. 17, 369388. Neurol. Careers. Detailed Description: In older adults dizziness is a common condition which is associated with repeated falls, fear of falling, depression, anxiety and ultimately loss of independence during activities of daily living. : international statistical classification of diseases and related health problems? It describes a common chronic dysfunction of the vestibular system and brain that produces persistent dizziness, non-spinning vertigo and/or unsteadiness. During sensory-driven OSC epoch, when stabilization is only based on sensory input, gaze is stable. Psychiatry 84, 707708. Eye and head movements were recorded with the EyeSeeCam measuring system (EyeSeeTec GmbH, Munich, Germany), by tracking movements of the left eye with video-oculography and head movements with 3D inertial sensors (resting state noise 00.3/s, SD 0.07/s), placed in the middle of the forehead, both with a sampling rate of 220 Hz. The influence of anxiety on ocular motor control and gaze. Examples include hiatal hernia and bacterial overgrowth. doi: 10.1007/BF00227846. Neurologist 10, 154164. Dis. J. Anxiety Disord. doi: 10.1016/j.nbd.2019.02.013, Bogaerts, K., Van Eylen, L., Li, W., Bresseleers, J., Van Diest, I., De Peuter, S., et al. Copyrights and related rights for article metadata waived via CC0 1.0 Universal (CC0) Public Domain Dedication. Perfect gaze stabilization, i.e., a gaze gain of 1, is indicated by the dashed line. Orientat. - The diagnoses made in 3781 new patients. (AD left) Shown are representative eye (light) and head (dark) velocity traces of one typical healthy subject (A,B) and one typical functional patient (C,D) for the unweighted (natural, A,C) and weighted condition (increased head inertia, B,D). In the current paper, we assess a physiologically relevant parameter (gaze stability) in functional dizziness patients that helps to uncover this site. doi: 10.1093/brain/aws129, Eger Aydogmus, M. (2020). Functional and psychiatric disorders that cause vestibular symptoms (i.e., vertigo, unsteadiness, and dizziness) are common. doi: 10.1016/j.jpsychores.2018.01.007, Vroegop, S., Dijkgraaf, M. G. W., and Vermeulen, M. (2013). Dizziness and unsteady gait are not effects of normal aging but indicate potential: Deficits in peripheral and central sensory functions (visual, vestibular, somatosensory) Musculoskeletal deficits (sarcopenia, arthritis) Cognitive and mental disorders (dementia, anxiety). References. PDF | Objective: We are still lacking a pathophysiological mechanism for functional disorders explaining the emergence and manifestation of. Lehnen N, Schrder L, Henningsen P, Glasauer S, Ramaioli C. Prog Brain Res. Lehnen, N., Kellerer, S., Knorr, A. G., Schlick, C., Jahn, K., Schneider, E., et al. The study protocol was approved by the Ethics Committee of the University of Munich, the study design is in line with the Declaration of Helsinki. Brain responses to virtual reality visual motion stimulation are affected by neurotic personality traits in patients with persistent postural-perceptual dizziness, Journal of Vestibular Research-equilibrium & Orientation, Transsaccadic Perception Deficits in Schizophrenia Reflect the Improper Internal Monitoring of Eye Movement Rather Than Abnormal Sensory Processing, Biological Psychiatry: Cognitive Neuroscience and Neuroimaging, Constant error of visual egocentric orientation in patients with acute vestibular disorder. Clipboard, Search History, and several other advanced features are temporarily unavailable. Motion Sickness. NL and SG are shareholders of EyeSeeTec GmbH, manufacturers of the measurement system used. Frontiers in Neuroscience 2019;249:385-400. doi: 10.1016/bs.pbr.2019.02.006. doi: 10.1002/14651858.CD005397.pub2, Money, K. E. (1970). Brain Res. Unstable Gaze in Functional Dizziness: A Contribution to Understanding the Pathophysiology of Functional Disorders. Dizziness. Dizziness and unsteadiness are the most common symptoms associated with neck pain, especially after a whiplash injury [1]. Psychosom. (2018). 103, 95101. Equilib. Results: Gaze stabilization differed between functional patients and healthy controls only when internal movement expectations were involved [F(1,17) = 14.63, p = 0.001, and partial 2 = 0.463]: functional dizziness patients showed reduced gaze stabilization during the CR (p = 0.036) but not OSC epoch (p = 0.26). doi: 10.3109/03005369109076616, Keywords: functional dizziness, pathophysiology, predictive coding, internal models, somatic symptom disorder, bodily distress disorder, Citation: Schrder L, von Werder D, Ramaioli C, Wachtler T, Henningsen P, Glasauer S and Lehnen N (2021) Unstable Gaze in Functional Dizziness: A Contribution to Understanding the Pathophysiology of Functional Disorders. Gaze gains are displayed as the slope of the solid lines, which represent the linear regression of eye velocity in head depending on head velocity in space. Doctors call this sensation presyncope. Expectations about sensory consequences of movement are derived from internal models about the world and the body that constitute central nervous system (CNS)-internal representations of previously learned or experienced causal relations within the body, the environment, and their interaction. https://doi.org/10.3389/fnins.2021.685590, Attribution-ShareAlike 4.0 International (CC BY-SA 4.0) license, CC0 1.0 Universal (CC0) Public Domain Dedication. (2010). doi: 10.1016/j.jpsychores.2017.10.007, Yardley, L. (1991). Animals use the sensation of optic flow to estimate their own movements and accordingly adjust their body posture and position and stabilize the direction of gaze. 24, 21022111. doi: 10.1007/s00221-014-3973-2, Park, J. W., Kim, T. S., Cha, E. H., Kang, B. C., and Park, H. J. Results of group analysis (controls n = 11, patients n = 8). doi: 10.1002/brb3.1622, Iodice, P., Porciello, G., Bufalari, I., Barca, L., and Pezzulo, G. (2019). Where too, it . Elderly people often have deficits in several areas. Group analysis confirming these differences have been published in Lehnen et al., 2019). In this weighted condition, when alterations in head characteristics are not yet reflected in CNS-internal representations, expectations are derived from the unweighted head internal model. 228, 6567. 119, 226234. 10.1037/a0017780 For breathlessness, fatigue and dizziness there are already established experimental paradigms to measure such dysfunctions in the absence of organic impairment. sharing sensitive information, make sure youre on a federal This experimental evidence supports the perceptual dysregulation hypothesis of functional disorders and is an important step toward understanding the underlying pathophysiology. Frontiers in Neuroscience, 15, 857 https://doi.org/10.3389/fnins.2021.685590 Reinert S, Hbener M, Bonhoeffer T, Goltstein PM. 2014 Feb;27(1):118-24. doi: 10.1097/WCO.0000000000000055. (2019). When they hold their heads still, these visual instability problems might resolve. J. Abnorm. Saccade detection was then inspected visually and corrected manually, by adding undetected saccades (<1% for all subjects) as well as correcting the detected minima (<1% for all subjects). Only gaze shifts where the point of eye maximum eccentricity as well as the first head zero crossing could be detected were considered for the analysis. Motion sickness adaptation: A neural mismatch model. - The diagnoses made in 3781 new patients. J. Abnorm. Figure 4. -, Bogaerts K., Van Eylen L., Li W., Bresseleers J., Van Diest I., De Peuter S., et al. Front. Bag ventilation, while gentler than jet ventilation, increases the risk of inadequate ventilation owing to prolonged inspiratory time and resultant shortened expiratory time. Open Access | Objective: We are still lacking a pathophysiological mechanism for functional disorders explaining the emergence and manifestation of characteristic, severely impairing bodily symptoms like chest pain or dizziness. Also, providing measurable alterations has the potential of improving positive diagnosis of functional dizziness. Altered functional brain connectivity in patients with visually induced dizziness . Pathogenesis and pathophysiology of functional (psychogenic) movement disorders. -, Baizabal-Carvallo J. F., Hallett M., Jankovic J. 2020, 17. doi: 10.1080/09540260701278879, Henningsen, P., Gndel, H., Kop, W. J., Lwe, B., Martin, A., Rief, W., et al. Within this paradigm shift, identifying apotentially unifyingpathophysiological mechanism is of high clinical relevance, as it would help to improve the positive definition, swift diagnosis, and treatment of functional disorders. The healthy subject shows intact CR-gaze stabilization in the unweighted condition, which is reduced by increasing the head inertia in the weighted condition. Results: Gaze stabilization differed between functional patients and healthy controls only when internal movement expectations were involved [F(1,17) = 14.63, p = 0.001, and partial 2 = 0.463]: functional dizziness patients showed reduced gaze stabilization during the CR (p = 0.036) but not OSC epoch (p = 0.26). Unstable Gaze in Functional Dizziness: A Contribution to Understanding the Pathophysiology of Functional Disorders. A heuristic mathematical model for the dynamics of sensory conflict and motion sickness hearing in classical musicians. Parieto-frontal coding of reaching: an integrated framework. doi: 10.1097/psy.0000000000000824, Carson, A., Stone, J., Hibberd, C., Murray, G., Duncan, R., Coleman, R., et al. Conclusion: While sensory-driven gaze stabilization is intact, there are marked, well-measurable deficits in internally-driven gaze stabilization in functional dizziness pointing at internal expectations that do not match actual body states. Scribd is the world's largest social reading and publishing site. Med. Smith-Kettlewell Eye Research Institute, United States, Department of Neurology, National and Kapodistrian University of Athens, Eginition Hospital, Greece. Predictive coding understands perception as a constant interplay between incoming sensory information and internal expectations about such sensory input. In fact, they are more common than many well-known structural vestibular disorders. Arch. Sci. 94, 444. 66, 417424. Every subject performed two rounds of the experiment: one in the natural condition (unweighted) and one with experimentally altered head characteristics (weighted). (2020). The stigma of mental illness: Anticipation and attitudes among patients with epileptic, dissociative or somatoform pain disorder. Structural gray matter decline (Wurthmann et al., 2017) as well as reduced functional resting state activity (Li et al., 2020) in functional dizziness patients were reported for brain areas that are important for spatial orientation and multisensory vestibular integration. J. R. Soc. . J. Neurosci. The functional patient displays reduced CR-gaze stabilization in the unweighted condition, which is further reduced in the weighted condition. During large eye-head gaze shifts toward visual targets gaze is unstable in the internally-driven CR epoch, i.e., when internal expectations are used to drive gaze stabilization, additionally to sensory input. Unable to load your collection due to an error, Unable to load your delegates due to an error. We understand this piece of evidence as a first experimental cornerstone that might guide future research toward transdiagnostic mechanisms for a positive definition of functional disorders. Disability, distress and unemployment in neurology outpatients with symptoms unexplained by organic disease.. Somatosensory illusions elicited by sham electromagnetic field exposure: experimental evidence for a predictive processing account of somatic symptom perception. Conclusion: While sensory-driven gaze stabilization is intact, there are marked, well-measurable deficits in internally-driven gaze stabilization in functional dizziness pointing at internal expectations that do not match actual body states. However, our clinical experience, supported by empirical data [ 2 ], is that self-reported symptoms of PPPD are underreported. Somatic Symptom Perception from a Predictive Coding Perspective an Empirical Test Using the Thermal Grill Illusion. 25, 405413. [Epidemiology of dizziness and vertigo]. This debris, called otoconia, is made up of small crystals of calcium carbonate (sometimes referred to informally as "ear rocks"). . Only patients without any known prior or current structural peripheral or central vestibular dysfunction were included. CR collected the data. Nervenarzt 80, 887894. fear of falling, or unstable gaze. Med. Washington, D.C: American Psychiatric Publishing, 10.1176/appi.books.9780890425596 Compensatory eye movements are driven by sensory feedback loops, mainly the VOR that is not suppressed anymore. Annu. Figure 2. Neurosci. Biobehav. DOAJ 2022 default by all rights reserved unless otherwise specified. We defined this epoch as the time window from the first zero crossing of head velocity until 0.1 s after the next LED flash. data:image/png;base64,iVBORw0KGgoAAAANSUhEUgAAAKAAAAB4CAYAAAB1ovlvAAAAAXNSR0IArs4c6QAAAnpJREFUeF7t17Fpw1AARdFv7WJN4EVcawrPJZeeR3u4kiGQkCYJaXxBHLUSPHT/AaHTvu . Head position was computed as the integral of head velocity over time for each time point, normalized by initial head position, where participants were asked to fixate the central LED for 10 s. Eye position was calculated from pupil rotation vectors, also normalized by initial eye position. Head oscillationsand counteracting eye movementsare illustrated in the window with increased y-axis scale (note that the functional dizziness patient display more pronounced head oscillations than the healthy participant, even in the natural condition. -, Angelaki D. E., Cullen K. E. (2008). Gaze, i.e., the position of the eyes in space, is composed of eye position (recorded in relation to the head) and head position (recorded in relation to space). PNAS 116, 1389713902. Based on the perceptual dysregulation theory (Edwards et al., 2012; Van den Bergh et al., 2017; Henningsen et al., 2018; Pezzulo et al., 2019), during large eyehead gaze shifts, we expect functional dizziness patients to rely on incorrect internal models of their head, thus showing unstable gaze during the CR, but not the OSC epoch. Peripheral vestibular hypofunction is one of the major causes of dizziness. PLoS One 9, 15. Ideally, such internal models match reality; i.e., they are a valid and reliable representation of the true causal relations. Untreated dizziness and fatigue can cause a fall. eCollection 2021. Distorted Symptom Perception in Patients With Medically Unexplained Symptoms. (Jul 2021). Together with the present results, by using the example of functional dizziness patients, we are one step closer in locating an erroneous site of perceptual dysregulation in functional disorders (Edwards et al., 2012; Van den Bergh et al., 2017; Henningsen et al., 2018; Pezzulo et al., 2019). World Health Organization (2004). Eur. Disentangling stigma from functional neurological disorders: Conference report and roadmap for the future. [1] Rev. (2017). This study reveals marked deficits in gaze stabilization in functional dizziness patients. Unstable Gaze in Functional Dizziness: A Contribution to Understanding the Pathophysiology of Functional Disorders. If this is not the case, resulting expectations about sensory input do not match the actual sensory activation. All participants were unexperienced with respect to the experimental design and had never worn the helmet before. Psychol. This effectalready present in the natural, unweighted conditionbecomes even more pronounced when the head inertia is increased. (2020). Functional dizziness patients were recruited from the German Center for Vertigo and Balance Disorders, a tertiary vertigo/dizziness center of the University Hospital of Munich where they presented with permanent dizziness symptoms (>3 months). Oculomotor programming disturbances in the dementia syndrome. Rev. 10.1016/j.nbd.2019.02.013 Gaze anchoring to a pointing target is present during the entire pointing movement and is driven by a non-visual signal. Anxiety disorders and other psychiatric subgroups in patients complaining of dizziness. BMJ 371, 110. CNS Spectr. 133, 170176. *Correspondence: Lena Schrder, Lena.Schroeder@tum.de, https://doi.org/10.3389/fnins.2021.685590, Creative Commons Attribution License (CC BY). Filtered raw data of experimental movement recordings with illustrated gain computation. J. Vestib. Internal model and sensory input contribution to these two gaze stabilization epochs have been validated in a previous study using the same experimental design (Salam and Lehnen, 2014): patients with complete bilateral vestibular loss show better gaze stabilization in the CR epoch than the OSC epoch, confirming the contribution of internal model and efference copy use in this stabilization epoch. The patients/participants provided their written informed consent to participate in this study. This was implemented by using the time window between the eye maximum eccentricity point and the point where head velocity reached 0/s. Res. Photos used throughout the site by David Jorre, Jean-Philippe Delberghe, JJ Ying, Luca Bravo, Brandi Redd, & Christian Perner from Unsplash.
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