Sustained bias of spatial attention in a 3 T MRI scanner.
Adaptation
Egocentric frame of reference
Eye movements
MRI
Magnetic vestibular stimulation (MVS)
Nystagmus
Spatial attention
Spatial neglect
Vestibular ocular reflex (VOR)
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
03 06 2024
03 06 2024
Historique:
received:
27
02
2024
accepted:
23
05
2024
medline:
3
6
2024
pubmed:
3
6
2024
entrez:
2
6
2024
Statut:
epublish
Résumé
When lying inside a MRI scanner and even in the absence of any motion, the static magnetic field of MRI scanners induces a magneto-hydrodynamic stimulation of subjects' vestibular organ (MVS). MVS thereby not only causes a horizontal vestibular nystagmus but also induces a horizontal bias in spatial attention. In this study, we aimed to determine the time course of MVS-induced biases in both VOR and spatial attention inside a 3 T MRI-scanner as well as their respective aftereffects after participants left the scanner. Eye movements and overt spatial attention in a visual search task were assessed in healthy volunteers before, during, and after a one-hour MVS period. All participants exhibited a VOR inside the scanner, which declined over time but never vanished completely. Importantly, there was also an MVS-induced horizontal bias in spatial attention and exploration, which persisted throughout the entire hour within the scanner. Upon exiting the scanner, we observed aftereffects in the opposite direction manifested in both the VOR and in spatial attention, which were statistically no longer detectable after 7 min. Sustained MVS effects on spatial attention have important implications for the design and interpretation of fMRI-studies and for the development of therapeutic interventions counteracting spatial neglect.
Identifiants
pubmed: 38825633
doi: 10.1038/s41598-024-62981-5
pii: 10.1038/s41598-024-62981-5
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
12657Informations de copyright
© 2024. The Author(s).
Références
Marcelli, V. et al. Spatio-temporal pattern of vestibular information processing after brief caloric stimulation. Eur. J. Radiol. 70(2), 312–316. https://doi.org/10.1016/j.ejrad.2008.01.042 (2009).
doi: 10.1016/j.ejrad.2008.01.042
pubmed: 18342473
Roberts, D. C. et al. Mri magnetic field stimulates rotational sensors of the brain. Curr. Biol. 21(19), 1635–1640. https://doi.org/10.1016/j.cub.2011.08.029 (2011).
doi: 10.1016/j.cub.2011.08.029
pubmed: 21945276
pmcid: 3379966
Ward, B. K., Roberts, D. C., Otero-Millan, J. & Zee, D. S. A decade of magnetic vestibular stimulation: From serendipity to physics to the clinic. J. Neurophysiol. 121(6), 2013–2019. https://doi.org/10.1152/jn.00873.2018 (2019).
doi: 10.1152/jn.00873.2018
pubmed: 30969883
Lindner, A., Wiesen, D. & Karnath, H.-O. Lying in a 3T MRI scanner induces neglect-like spatial attention bias. eLife 10, e71076. https://doi.org/10.7554/eLife.71076 (2021).
doi: 10.7554/eLife.71076
pubmed: 34585665
pmcid: 8480976
Holé, J., Reilly, K. T., Nash, S. & Rode, G. Caloric vestibular stimulation reduces the directional bias in representational neglect. Brain Sci. 10(6), 323. https://doi.org/10.3390/brainsci10060323 (2020).
doi: 10.3390/brainsci10060323
pubmed: 32466608
pmcid: 7348904
Karnath, H.-O., Fetter, M. & Dichgans, J. Ocular exploration of space as a function of neck proprioceptive and vestibular input-observations in normal subjects and patients with spatial neglect after parietal lesions. Exp. Brain Res. 109(2), 333–342 (1996).
doi: 10.1007/BF00231791
pubmed: 8738380
Karnath, H.-O. Subjective body orientation in neglect and the interactive contribution of neck muscle proprioception and vestibular stimulation. Brain 117(5), 1001–1012 (1994).
doi: 10.1093/brain/117.5.1001
pubmed: 7953584
Jareonsettasin, P. et al. Multiple time courses of vestibular set-point adaptation revealed by sustained magnetic field stimulation of the labyrinth. Curr. Biol. 26(10), 1359–1366. https://doi.org/10.1016/j.cub.2016.03.066 (2016).
doi: 10.1016/j.cub.2016.03.066
pubmed: 27185559
pmcid: 4927084
Go, C. C. et al. Persistent horizontal and vertical, MR-induced nystagmus in resting state human connectome project data. NeuroImage 255, 119170. https://doi.org/10.1016/j.neuroimage.2022.119170 (2022).
doi: 10.1016/j.neuroimage.2022.119170
pubmed: 35367649
Karnath, H.-O. & Rorden, C. The anatomy of spatial neglect. Neuropsychologia 50(6), 1010–1017. https://doi.org/10.1016/j.neuropsychologia.2011.06.027 (2012).
doi: 10.1016/j.neuropsychologia.2011.06.027
pubmed: 21756924
Rubens, A. B. Caloric stimulation and unilateral visual neglect. Neurology 35(7), 1019–1024. https://doi.org/10.1212/wnl.35.7.1019 (1985).
doi: 10.1212/wnl.35.7.1019
pubmed: 4010940
Vallar, G., Papagno, C., Rusconi, M. L. & Bisiach, E. Vestibular stimulation, spatial hemineglect and dysphasia, selective effects?. Cortex 31(3), 589–593. https://doi.org/10.1016/s0010-9452(13)80070-6 (1995).
doi: 10.1016/s0010-9452(13)80070-6
pubmed: 8536486
Karnath, H.-O., Rosenzopf, H., Smaczny, S. & Lindner, A. Spatial neglect after stroke is reduced when lying inside a 3T MRI scanner. BioRxiv https://doi.org/10.1101/2022.08.01.502290 (2022).
doi: 10.1101/2022.08.01.502290
Boegle, R., Stephan, T., Ertl, M., Glasauer, S. & Dieterich, M. Magnetic vestibular stimulation modulates default mode network fluctuations. NeuroImage 127, 409–421. https://doi.org/10.1016/j.neuroimage.2015.11.065 (2016).
doi: 10.1016/j.neuroimage.2015.11.065
pubmed: 26666898
Zee, D. S., Jareonsettasin, P. & Leigh, R. J. Ocular stability and set-point adaptation. Philos. Trans. R. Soc. Lond. Ser. B Biol. Sci. 372(18), 2016–2199. https://doi.org/10.1098/rstb.2016.0199 (2017).
doi: 10.1098/rstb.2016.0199
Owens, A. D. & Leibowitz, H. W. Accommodation, convergence, and distance perception in low illumination: 540–50. Am. J. Optom. Physiol. Optics 57(9), 540–550 (1980).
doi: 10.1097/00006324-198009000-00004
Crawford, J. R. & Garthwaite, P. H. Investigation of the single case in neuropsychology: Confidence limits on the abnormality of test scores and test score differences. Neuropsychologia 40(8), 1196–1208. https://doi.org/10.1016/S0028-3932(01)00224-X (2002).
doi: 10.1016/S0028-3932(01)00224-X
pubmed: 11931923
Crawford, J. R. & Howell, D. C. Comparing an individual’s test score against norms derived from small samples. Clin. Neuropsychol. 12(4), 482–486. https://doi.org/10.1076/clin.12.4.482.7241 (1998).
doi: 10.1076/clin.12.4.482.7241
Otero-Millan, J., Zee, D. S., Schubert, M. C., Roberts, D. C. & Ward, B. K. Three-dimensional eye movement recordings during magnetic vestibular stimulation. J. Neurol. 264, 7–12. https://doi.org/10.1007/s00415-017-8420-4 (2017).
doi: 10.1007/s00415-017-8420-4
pubmed: 28271407
Lakens, D. Calculating and reporting effect sizes to facilitate cumulative science: A practical primer for t-tests and ANOVAs. Front. Psychol. 4, 863. https://doi.org/10.3389/fpsyg.2013.00863 (2013).
doi: 10.3389/fpsyg.2013.00863
pubmed: 24324449
pmcid: 3840331
Ferrè, E. R. & Haggard, P. Vestibular cognition: State-of-the-art and future directions. Cognit. Neuropsychol. 37(7–8), 413–420. https://doi.org/10.1080/02643294.2020.1736018 (2020).
doi: 10.1080/02643294.2020.1736018
Boegle, R., Ertl, M., Stephan, T. & Dieterich, M. Magnetic vestibular stimulation influences resting-state fluctuations and induces visual-vestibular biases. J. Neurol. 264(5), 999–1001. https://doi.org/10.1007/s00415-017-8447-6 (2017).
doi: 10.1007/s00415-017-8447-6
pubmed: 28271404
Boegle, R., Kirsch, V., Gerb, J. & Dieterich, M. Modulatory effects of magnetic vestibular stimulation on resting-state networks can be explained by subject-specific orientation of inner-ear anatomy in the MR static magnetic field. J. Neurol. 267(1), 91–103. https://doi.org/10.1007/s00415-020-09957-3 (2020).
doi: 10.1007/s00415-020-09957-3
pubmed: 32529576
pmcid: 7718185
Ward, B. K. et al. Magnetic vestibular stimulation (MVS) as a technique for understanding the normal and diseased labyrinth. Front. Neurol. 8, 122. https://doi.org/10.3389/fneur.2017.00122 (2017).
doi: 10.3389/fneur.2017.00122
pubmed: 28424657
pmcid: 5380677
Ertl, M. & Boegle, R. Investigating the vestibular system using modern imaging techniques—A review on the available stimulation and imaging methods. J. Neurosci. Methods 326, 108363. https://doi.org/10.1016/j.jneumeth.2019.108363 (2019).
doi: 10.1016/j.jneumeth.2019.108363
pubmed: 31351972
Mian, O. S., Lin, Y., Antunes, A., Glover, P. M. & Day, B. L. On the vertigo due to static magnetic fields. PloS one 8(10), e78748. https://doi.org/10.1371/journal.pone.0078748.g001 (2013).
doi: 10.1371/journal.pone.0078748.g001
pubmed: 24205304
pmcid: 3813712
Mian, O. S., Glover, P. M. & Day, B. L. Reconciling magnetically induced vertigo and nystagmus. Front. Neurol. 6, 201. https://doi.org/10.3389/fneur.2015.00201 (2015).
doi: 10.3389/fneur.2015.00201
pubmed: 26441821
pmcid: 4569971
Mian, O. S., Li, Y., Antunes, A., Glover, P. M. & Day, B. L. Effect of head pitch and roll orientations on magnetically induced vertigo. J. Physiol. 594(4), 1051–1067. https://doi.org/10.1113/JP271513 (2016).
doi: 10.1113/JP271513
pubmed: 26614577
Karnath, H.-O. Disturbed coordinate transformation in the neural representation of space as the crucial mechanism leading to neglect. Neuropsychol. Rehabilit. 4(2), 147–150 (1994).
doi: 10.1080/09602019408402273
Karnath, H.-O. Spatial attention systems in spatial neglect. Neuropsychologia 75, 61–73. https://doi.org/10.1016/j.neuropsychologia.2015.05.019 (2015).
doi: 10.1016/j.neuropsychologia.2015.05.019
pubmed: 26004064