Unraveling the Twist: Spatial Navigational Challenges in Cervical Dystonia.


Journal

Movement disorders : official journal of the Movement Disorder Society
ISSN: 1531-8257
Titre abrégé: Mov Disord
Pays: United States
ID NLM: 8610688

Informations de publication

Date de publication:
Nov 2023
Historique:
received: 24 05 2023
accepted: 05 09 2023
medline: 1 12 2023
pubmed: 2 11 2023
entrez: 2 11 2023
Statut: ppublish

Résumé

Cervical dystonia (CD) is an intricate neurological condition with motor and nonmotor symptoms. These include disruptions in visual perception, self-orientation, visual working memory, and vestibular functions. However, the specific impact of CD on perceiving self-motion direction, especially with isolated visual or vestibular stimuli, remains largely unexplored. This study aimed to examine the effects of CD on linear motion perception, hypothesizing impaired heading discrimination in both vestibular and visual tasks, and that such deficits correlate with the disease severity. We employed a cutting-edge motion platform to precisely control whole-body linear motion. Through repeated two-alternative forced-choice tasks, we assessed vestibular heading direction discrimination. Participants observed dynamic star clouds in immersive virtual reality and indicated their perceived self-motion direction, evaluating visual heading direction discrimination. Sensitivity to direction variations and response accuracy errors were analyzed using robust Gaussian cumulative distribution psychometric functions. Heading perception is impaired in individuals with CD, particularly evident in vestibular heading discrimination. CD severity correlated with elevated thresholds for both vestibular and visual heading discrimination. Surprisingly, lateralized CD did not introduce bias in either system, suggesting widespread disruption over localized effects. Contrary to previous beliefs, our findings challenge the idea that CD-related heading discrimination issues mainly arise from peripheral vestibular effects. Instead, abnormal proprioceptive input from dystonic neck muscles introduces noise into the central mechanism integrating visual, vestibular, and proprioceptive signals. These insights into spatial navigation deficits have implications for future CD research. © 2023 The Authors. Movement Disorders published by Wiley Periodicals LLC on behalf of International Parkinson and Movement Disorder Society. This article has been contributed to by U.S. Government employees and their work is in the public domain in the USA.

Sections du résumé

BACKGROUND BACKGROUND
Cervical dystonia (CD) is an intricate neurological condition with motor and nonmotor symptoms. These include disruptions in visual perception, self-orientation, visual working memory, and vestibular functions. However, the specific impact of CD on perceiving self-motion direction, especially with isolated visual or vestibular stimuli, remains largely unexplored.
OBJECTIVE OBJECTIVE
This study aimed to examine the effects of CD on linear motion perception, hypothesizing impaired heading discrimination in both vestibular and visual tasks, and that such deficits correlate with the disease severity.
METHODS METHODS
We employed a cutting-edge motion platform to precisely control whole-body linear motion. Through repeated two-alternative forced-choice tasks, we assessed vestibular heading direction discrimination. Participants observed dynamic star clouds in immersive virtual reality and indicated their perceived self-motion direction, evaluating visual heading direction discrimination. Sensitivity to direction variations and response accuracy errors were analyzed using robust Gaussian cumulative distribution psychometric functions.
RESULTS RESULTS
Heading perception is impaired in individuals with CD, particularly evident in vestibular heading discrimination. CD severity correlated with elevated thresholds for both vestibular and visual heading discrimination. Surprisingly, lateralized CD did not introduce bias in either system, suggesting widespread disruption over localized effects.
CONCLUSIONS CONCLUSIONS
Contrary to previous beliefs, our findings challenge the idea that CD-related heading discrimination issues mainly arise from peripheral vestibular effects. Instead, abnormal proprioceptive input from dystonic neck muscles introduces noise into the central mechanism integrating visual, vestibular, and proprioceptive signals. These insights into spatial navigation deficits have implications for future CD research. © 2023 The Authors. Movement Disorders published by Wiley Periodicals LLC on behalf of International Parkinson and Movement Disorder Society. This article has been contributed to by U.S. Government employees and their work is in the public domain in the USA.

Identifiants

pubmed: 37914913
doi: 10.1002/mds.29612
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

2116-2121

Subventions

Organisme : American Academy of Neurology
Organisme : American Parkinson's Disease Association George C. Cotzias Memorial Fellowhsip
Organisme : Caresource Ohio Community Partnership Grant
Organisme : U.S. Department of Veterans Affairs
ID : I01CX002086

Informations de copyright

© 2023 The Authors. Movement Disorders published by Wiley Periodicals LLC on behalf of International Parkinson and Movement Disorder Society. This article has been contributed to by U.S. Government employees and their work is in the public domain in the USA.

Références

Stamelou M, Edwards MJ, Hallett M, Bhatia KP. The non-motor syndrome of primary dystonia: clinical and pathophysiological implications. Brain 2012;135(Pt 6):1668-1681.
Novaretti N, Cunha ALN, Bezerra TC, et al. The prevalence and correlation of non-motor symptoms in adult patients with idiopathic focal or segmental dystonia. Tremor Other Hyperkinet Mov (N Y) 2019;9:596.
Hinse P, Leplow B, Humbert T, Lamparter U, Junge A, Emskotter T. Impairment of visuospatial function in idiopathic spasmodic torticollis. J Neurol 1996;243(1):29-33.
Aleman GG, de Erausquin GA, Micheli F. Cognitive disturbances in primary blepharospasm. Mov Disord 2009;24(14):2112-2120.
Leplow B, Stübinger C. Visuospatial functions in patients with spasmodic torticollis. Percept Mot Skills 1994;78(3 Pt 2):1363-1375.
Chillemi G, Calamuneri A, Morgante F, et al. Spatial and temporal high processing of visual and auditory stimuli in cervical dystonia. Front Neurol 2017;8:66.
Ferrazzano G, Berardelli I, Belvisi D, et al. Awareness of dystonic posture in patients with cervical dystonia. Front Psychol 2020;11:1434.
Avanzino L, Cherif A, Crisafulli O, et al. Tactile and proprioceptive dysfunction differentiates cervical dystonia with and without tremor. Neurology 2020;94(6):e639-e650.
Bronstein AM, Rudge P. Vestibular involvement in spasmodic torticollis. J Neurol Neurosurg Psychiatry 1986;49(3):290-295.
Stell R, Gresty M, Metcalfe T, Bronstein AM. Cervico-ocular function in patients with spasmodic torticollis. J Neurol Neurosurg Psychiatry 1991;54(1):39-41.
Stell R, Bronstein AM, Marsden CD. Vestibulo-ocular abnormalities in spasmodic torticollis before and after botulinum toxin injections. J Neurol Neurosurg Psychiatry 1989;52(1):57-62.
Bronstein AM, Rudge P, Beechey AH. Spasmodic torticollis following unilateral VIII nerve lesions: neck EMG modulation in response to vestibular stimuli. J Neurol Neurosurg Psychiatry 1987;50(5):580-586.
Diamond SG, Markham CH, Baloh RW. Vestibular involvement in spasmodic torticollis: an old hypothesis with new data from otolith testing. Adv Otorhinolaryngol 1988;42:219-223.
Bisdorff AR, Anastasopoulos D, Bronstein AM, Gresty MA. Subjective postural vertical in peripheral and central vestibular disorders. Acta Otolaryngol Suppl 1995;520(Pt 1):68-71.
Anastasopoulos D, Bhatia K, Bronstein AM, Marsden CD, Gresty MA. Perception of spatial orientation in spasmodic torticollis. Part 2: the visual vertical. Mov Disord 1997;12(5):709-714.
Guedry FE. Psychophysics of Vestibular Sensation. Berlin-Heidelberg-New York: Springer-Verlag; 1974.
Maschke M, Gomez CM, Tuite PJ, Konczak J. Dysfunction of the basal ganglia, but not the cerebellum, impairs kinaesthesia. Brain 2003;126(Pt 10):2312-2322.
Neychev VK, Fan X, Mitev VI, Hess EJ, Jinnah HA. The basal ganglia and cerebellum interact in the expression of dystonic movement. Brain 2008;131(Pt 9):2499-2509.
Liedgren SR, Milne AC, Schwarz DW, Tomlinson RD. Representation of vestibular afferents in somatosensory thalamic nuclei of the squirrel monkey (Saimiri sciureus). J Neurophysiol 1976;39(3):601-612.
Gu Y, DeAngelis GC, Angelaki DE. A functional link between area MSTd and heading perception based on vestibular signals. Nat Neurosci 2007;10(8):1038-1047.

Auteurs

Hanieh Agharazi (H)

National VA Parkinson Consortium Center, Neurology Service, Louis Stokes Cleveland VA Medical Center, Cleveland, Ohio, USA.

Alexander Wang (A)

Department of Neurology, Case Western Reserve University, Cleveland, Ohio, USA.
Movement Disorders Center, Neurological Institute, University Hospitals, Cleveland, Ohio, USA.

Aratrik Guha (A)

National VA Parkinson Consortium Center, Neurology Service, Louis Stokes Cleveland VA Medical Center, Cleveland, Ohio, USA.
Department of Biomedical Engineering, Case Western Reserve University, Cleveland, Ohio, USA.

Palak Gupta (P)

National VA Parkinson Consortium Center, Neurology Service, Louis Stokes Cleveland VA Medical Center, Cleveland, Ohio, USA.
Department of Biomedical Engineering, Case Western Reserve University, Cleveland, Ohio, USA.

Aasef G Shaikh (AG)

National VA Parkinson Consortium Center, Neurology Service, Louis Stokes Cleveland VA Medical Center, Cleveland, Ohio, USA.
Department of Neurology, Case Western Reserve University, Cleveland, Ohio, USA.
Movement Disorders Center, Neurological Institute, University Hospitals, Cleveland, Ohio, USA.
Department of Biomedical Engineering, Case Western Reserve University, Cleveland, Ohio, USA.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH