Top

Published in:

Open Access 01-12-2020 | Original Communication

Different EEG brain activity in right and left handers during visually induced self-motion perception

Authors: Michaela McAssey, James Dowsett, Valerie Kirsch, Thomas Brandt, Marianne Dieterich

Published in: Journal of Neurology | Special Issue 1/2020

Abstract

Visually induced self-motion perception (vection) relies on visual–vestibular interaction. Imaging studies using vestibular stimulation have revealed a vestibular thalamo-cortical dominance in the right hemisphere in right handers and the left hemisphere in left handers. We investigated if the behavioural characteristics and neural correlates of vection differ between healthy left and right-handed individuals. 64-channel EEG was recorded while 25 right handers and 25 left handers were exposed to vection-compatible roll motion (coherent motion) and a matched, control condition (incoherent motion). Behavioural characteristics, i.e. vection presence, onset latency, duration and subjective strength, were also recorded. The behavioural characteristics of vection did not differ between left and right handers (all p > 0.05). Fast Fourier Transform (FFT) analysis revealed significant decreases in alpha power during vection–compatible roll motion (p < 0.05). The topography of this decrease was handedness-dependent, with left handers showing a left lateralized centro-parietal decrease and right handers showing a bilateral midline centro-parietal decrease. Further time–frequency analysis, time locked to vection onset, revealed a comparable decrease in alpha power around vection onset and a relative increase in alpha power during ongoing vection, for left and right handers. No effects were observed in theta and beta bands. Left and right-handed individuals show vection-related alpha power decreases at different topographical regions, possibly related to the influence of handedness-dependent vestibular dominance in the visual–vestibular interaction that facilitates visual self-motion perception. Despite this difference in where vection-related activity is observed, left and right handers demonstrate comparable perception and underlying alpha band changes during vection.

Dichgans J, Brandt T (1978) Visual–vestibular interaction: effects on self-motion perception and postural control. In: Held R, Leibowitz HW, Teuber HL (eds) Handbook of sensory physiology, vol 8. Springer, Berlin, pp 755–804. https://doi.org/10.1007/978-3-642-46354-9_25

Brandt T, Bartenstein P, Janek A, Dieterich M (1998) Reciprocal inhibitory visual–vestibular interaction. Visual motion stimulation deactivates the parieto-insular vestibular cortex. Brain 121:1749–1758. https://doi.org/10.1093/brain/121.9.1749CrossRefPubMed

Deutschlander A, Bense S, Stephan T, Schwaiger M, Brandt T, Dieterich M (2002) Sensory system interactions during simultaneous vestibular and visual stimulation in PET. Hum Brain Mapp 16:92–103. https://doi.org/10.1002/hbm.10030CrossRefPubMedPubMedCentral

Deutschlander A, Bense S, Stephan T, Schwaiger M, Dieterich M, Brandt T (2004) Rollvection versus linearvection: comparison of brain activations in PET. Hum Brain Mapp 21:143–153. https://doi.org/10.1002/hbm.10155CrossRefPubMedPubMedCentral

Kleinschmidt A, Thilo KV, Buchel C, Gresty MA, Bronstein AM, Frackowiak RSJ (2002) Neural correlates of visual–motion perception as object- or self-motion. NeuroImage 16:873–882. https://doi.org/10.1006/nimg.2002.1181CrossRefPubMed

Brandt T, Glasauer S, Stephan T, Bense S, Yousry TA, Deutschlander A, Dieterich M (2002) Visual–vestibular and visuovisual cortical interaction: new insights from fMRI and pet. Ann N Y Acad Sci 956:230–241. https://doi.org/10.1111/j.1749-6632.2002.tb02822.xCrossRefPubMed

Becker-Bense S, Buchholz HG, zu Eulenburg P, Best C, Bartenstein P, Schreckenberger M, Dieterich M (2012) Ventral and dorsal streams processing visual motion perception (FDG-PET study). BMC Neurosci 13:81. https://doi.org/10.1186/1471-2202-13-81CrossRefPubMedPubMedCentral

Nishiike S, Nakagawa S, Nakagawa A, Uno A, Tonoike M, Takeda N, Kubo T (2002) Magnetic cortical responses evoked by visual linear forward acceleration. NeuroReport 13:1805–1808. https://doi.org/10.1097/00001756-200210070-00023CrossRefPubMed

Uesaki M, Ashida H (2015) Optic-flow selective cortical sensory regions associated with self-reported states of vection. Front Psychol 6:775. https://doi.org/10.3389/fpsyg.2015.00775CrossRefPubMedPubMedCentral

10.

Indovina I, Maffei V, Bosco G, Zago M, Macaluso E, Lacquaniti F (2005) Representation of visual gravitational motion in the human vestibular cortex. Science 308:416–419. https://doi.org/10.1126/science.1107961CrossRefPubMed

11.

Previc FH, Liotti M, Blakemore C, Beer J, Fox P (2000) Functional imaging of brain areas involved in the processing of coherent and incoherent wide field-of-view visual motion. Exp Brain Res 131:393–405. https://doi.org/10.1007/s002219900298CrossRefPubMed

12.

Beer J, Blakemore C, Previc FH, Liotti M (2002) Areas of the human brain activated by ambient visual motion, indicating three kinds of self-movement. Exp Brain Res 143:78–88. https://doi.org/10.1007/s00221-001-0947-yCrossRefPubMed

13.

de Jong BM, Shipp S, Skidmore B, Frackowiak RS, Zeki S (1994) The cerebral activity related to the visual perception of forward motion in depth. Brain 117:1039–1054. https://doi.org/10.1093/brain/117.5.1039CrossRefPubMed

14.

Cardin V, Smith AT (2010) Sensitivity of human visual and vestibular cortical regions to egomotion-compatible visual stimulation. Cereb Cortex 20:1964–1973. https://doi.org/10.1093/cercor/bhp268CrossRefPubMed

15.

Thilo KV, Probst T, Bronstein AM, Ito Y, Gresty MA (1999) Torsional eye movements are facilitated during perception of self-motion. Exp Brain Res 126:495–500. https://doi.org/10.1007/s002210050757CrossRefPubMed

16.

Kennedy RS, Hettinger LJ, Harm DL, Ordy JM, Dunlap WP (1996) Psychophysical scaling of circular vection (CV) produced by optokinetic (OKN) motion: individual differences and effects of practice. J Vestib Res 6:331–341. https://doi.org/10.3233/VES-1996-6502CrossRefPubMed

17.

Dieterich M, Bense S, Lutz S, Drzezga A, Stephan T, Bartenstein P, Brandt T (2003) Dominance for vestibular cortical function in the non-dominant hemisphere. Cereb Cortex 13:994–1007. https://doi.org/10.1093/cercor/13.9.994CrossRefPubMed

18.

Brandt T, Dieterich M (2015) Does the vestibular system determine the lateralization of brain functions? J Neurol 262:214–215. https://doi.org/10.1007/s00415-014-7548-8CrossRefPubMed

19.

Dieterich M, Brandt T (2018) Global orientation in space and the lateralization of brain functions. Curr Opin Neurol 31:96–104. https://doi.org/10.1097/WCO.0000000000000516CrossRefPubMed

20.

Janzen J, Schlindwein P, Bense S, Bauermann T, Vucurevic G, Stoeter P, Dieterich M (2008) Neural correlates of hemispheric dominance and ipsilaterality within the vestibular system. NeuroImage 42:1508–1518. https://doi.org/10.1016/j.neuroimage.2008.06.026CrossRefPubMed

21.

zu Eulenburg P, Caspers S, Roski C, Eickhoff SB (2012) Meta-analytical definition and functional connectivity of the human vestibular cortex. NeuroImage 60:162–169. https://doi.org/10.1016/j.neuroimage.2011.12.032CrossRefPubMed

22.

Bense S, Bartenstein P, Lutz S, Stephan T, Schwaiger M, Brandt T, Dieterich M (2003) Three determinants of vestibular hemispheric dominance during caloric stimulation—a positron emission tomography study. Ann NY Acad Sci 1004:440–445. https://doi.org/10.1111/j.1749-6632.2003.tb00256.xCrossRef

23.

Frank SM, Wirth AM, Greenlee MW (2016) Visual–vestibular processing in the human Sylvian fissure. J Neurophysiol 116:263–271. https://doi.org/10.1152/jn.00009.2016CrossRefPubMedPubMedCentral

24.

Suzuki M, Kitano H, Ito R, Kitanishi T, Yazawa Y, Ogawa T, Shiino A, Kitajima K (2001) Cortical and subcortical vestibular response to caloric stimulation detected by functional magnetic resonance imaging. Brain Res Cogn Brain Res 12:441–449. https://doi.org/10.1016/s0926-6410(01)00080-5CrossRefPubMed

25.

Fink GR, Marshall JC, Weiss PH, Stephan T, Grefkes C, Shah NJ, Zilles K, Dieterich M (2003) Performing allocentric visuospatial judgments with induced distortion of the egocentric reference frame: an fMRI study with clinical implications. NeuroImage 20:1505–1517. https://doi.org/10.1016/j.neuroimage.2003.07.006CrossRefPubMed

26.

Eickhoff SB, Weiss PH, Amunts K, Fink GR, Zilles K (2006) Identifying human parieto-insular vestibular cortex using fMRI and cytoarchitectonic mapping. Hum Brain Mapp 27:611–621. https://doi.org/10.1002/hbm.20205CrossRefPubMed

27.

Schlindwein P, Mueller M, Bauermann T, Brandt T, Stoeter P, Dieterich M (2008) Cortical representation of saccular vestibular stimulation: VEMPs in fMRI. NeuroImage 39:19–31. https://doi.org/10.1016/j.neuroimage.2007.08.016CrossRefPubMed

28.

Lopez C, Blanke O, Mast FW (2012) The human vestibular cortex revealed by coordinate-based activation likelihood estimation meta-analysis. Neuroscience 212:159–179. https://doi.org/10.1016/j.neuroscience.2012.03.028CrossRefPubMed

29.

Palmisano S, Barry RJ, De Blasio FM, Fogarty JS (2016) Identifying objective EEG based markers of linear vection in depth. Front Psychol 7:1205. https://doi.org/10.3389/fpsyg.2016.01205CrossRefPubMedPubMedCentral

30.

Dowsett J, Herrmann CS, Dieterich M, Taylor PCJ (2020) Shift in lateralization during illusory self-motion: EEG responses to visual flicker at 10 Hz and frequency-specific modulation by tACS. Eur J Neurosci 51:1657–1675. https://doi.org/10.1111/ejn.14543CrossRefPubMed

31.

Harquel S, Guerraz M, Barraud PA, Cian C (2020) Modulation of alpha waves in sensorimotor cortical networks during self-motion perception evoked by different visual–vestibular conflicts. J Neurophysiol 123:346–355. https://doi.org/10.1152/jn.00237.2019CrossRefPubMed

32.

Lange J, Keil J, Schnitzler A, van Dijk H, Weisz N (2014) The role of alpha oscillations for illusory perception. Behav Brain Res 271:294–301. https://doi.org/10.1016/j.bbr.2014.06.015CrossRefPubMedPubMedCentral

33.

Piantoni G, Romeijn N, Gomez-Herrero G, Van Der Werf YD, Van Someren EJW (2017) Alpha power predicts persistence of bistable perception. Sci Rep 7:5208. https://doi.org/10.1038/s41598-017-05610-8CrossRefPubMedPubMedCentral

34.

Struber D, Herrmann CS (2002) MEG alpha activity decrease reflects destabilization of multistable percepts. Brain Res Cogn Brain Res 14:370–382. https://doi.org/10.1016/s0926-6410(02)00139-8CrossRefPubMed

35.

Delorme A, Makeig S (2004) EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis. J Neurosci Methods 134:9–21. https://doi.org/10.1016/j.jneumeth.2003.10.009CrossRefPubMed

36.

Haller M, Donoghue T, Peterson E, Varma P, Sebastian P, Gao R, Noto T, Knight RT, Shestyuk A, Voytek B (2018) Parameterizing neural power spectra. bioRxiv. https://doi.org/10.1101/299859CrossRef

37.

Pascual-Marqui RD (2002) Standardized low-resolution brain electromagnetic tomography (sLORETA): technical details. Methods Find Exp Clin Pharmacol 24(Suppl D):5–12PubMed

38.

Pascual-Marqui RD (2007) Discrete, 3D distributed, linear imaging methods of electric neuronal activity. Part 1: exact, zero error localization. arXiv:07103341. https://arXiv.org/abs/arXiv:0710.3341

39.

Fuchs M, Kastner J, Wagner M, Hawes S, Ebersole JS (2002) A standardized boundary element method volume conductor model. Clin Neurophysiol 113:702–712. https://doi.org/10.1016/s1388-2457(02)00030-5CrossRefPubMed

40.

Cohen MX (2014) Analyzing neural time series data: theory and practice. The MIT Press, Cambridge (Massachusetts)CrossRef

41.

Maris E, Oostenveld R (2007) Nonparametric statistical testing of EEG- and MEG-data. J Neurosci Methods 164:177–190. https://doi.org/10.1016/j.jneumeth.2007.03.024CrossRefPubMed

42.

Arshad Q, Ortega MC, Goga U, Lobo R, Siddiqui S, Mediratta S, Bednarczuk NF, Kaski D, Bronstein AM (2019) Interhemispheric control of sensory cue integration and self-motion perception. Neuroscience 408:378–387. https://doi.org/10.1016/j.neuroscience.2019.04.027CrossRefPubMed

43.

Delon-Martin C, Gobbele R, Buchner H, Haug BA, Antal A, Darvas F, Paulus W (2006) Temporal pattern of source activities evoked by different types of motion onset stimuli. NeuroImage 31:1567–1579. https://doi.org/10.1016/j.neuroimage.2006.02.013CrossRefPubMed

44.

Slobounov S, Wu T, Hallett M, Shibasaki H, Slobounov E, Newell K (2006) Neural underpinning of postural responses to visual field motion. Biol Psychol 72:188–197. https://doi.org/10.1016/j.biopsycho.2005.10.005CrossRefPubMed

45.

Pitzalis S, Sdoia S, Bultrini A, Committeri G, Di Russo F, Fattori P, Galletti C, Galati G (2013) Selectivity to translational egomotion in human brain motion areas. PLoS ONE 8:e60241. https://doi.org/10.1371/journal.pone.0060241CrossRefPubMedPubMedCentral

46.

Klimesch W (2012) alpha-band oscillations, attention, and controlled access to stored information. Trends Cogn Sci 16:606–617. https://doi.org/10.1016/j.tics.2012.10.007CrossRefPubMedPubMedCentral

47.

Pfurtscheller G, Stancak A Jr, Neuper C (1996) Event-related synchronization (ERS) in the alpha band-an electrophysiological correlate of cortical idling: a review. Int J Psychophysiol 24:39–46. https://doi.org/10.1016/s0167-8760(96)00066-9CrossRefPubMed

48.

Goldman RI, Stern JM, Engel J Jr, Cohen MS (2002) Simultaneous EEG and fMRI of the alpha rhythm. NeuroReport 13:2487–2492. https://doi.org/10.1097/01.wnr.0000047685.08940.d0CrossRefPubMedPubMedCentral

49.

Sadato N, Nakamura S, Oohashi T, Nishina E, Fuwamoto Y, Waki A, Yonekura Y (1998) Neural networks for generation and suppression of alpha rhythm: a PET study. NeuroReport 9:893–897. https://doi.org/10.1097/00001756-199803300-00024CrossRefPubMed

50.

Ehinger BV, Fischer P, Gert AL, Kaufhold L, Weber F, Pipa G, Konig P (2014) Kinesthetic and vestibular information modulate alpha activity during spatial navigation: a mobile EEG study. Front Hum Neurosci 8:71. https://doi.org/10.3389/fnhum.2014.00071CrossRefPubMedPubMedCentral

51.

Gould IC, Rushworth MF, Nobre AC (2011) Indexing the graded allocation of visuospatial attention using anticipatory alpha oscillations. J Neurophysiol 105:1318–1326. https://doi.org/10.1152/jn.00653.2010CrossRefPubMedPubMedCentral

52.

Rohenkohl G, Nobre AC (2011) alpha oscillations related to anticipatory attention follow temporal expectations. J Neurosci 31:14076–14084. https://doi.org/10.1523/JNEUROSCI.3387-11.2011CrossRefPubMedPubMedCentral

Title: Different EEG brain activity in right and left handers during visually induced self-motion perception
Authors: Michaela McAssey
James Dowsett
Valerie Kirsch
Thomas Brandt
Marianne Dieterich
Publication date: 01-12-2020
Publisher: Springer Berlin Heidelberg
Published in: Journal of Neurology / Issue Special Issue 1/2020
Print ISSN: 0340-5354
Electronic ISSN: 1432-1459
DOI: https://doi.org/10.1007/s00415-020-09915-z

At a glance: The STEP trials

Springer Medicine

Different EEG brain activity in right and left handers during visually induced self-motion perception

Abstract

At a glance: The STEP trials

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Special Issue 1/2020

EEG microstate architecture does not change during passive whole-body accelerations

Body-maps of emotions in bilateral vestibulopathy

Comparison of three video head impulse test systems for the diagnosis of bilateral vestibulopathy

Development and validation of a classification algorithm to diagnose and differentiate spontaneous episodic vertigo syndromes: results from the DizzyReg patient registry

Vestibular evoked myogenic potentials in vestibular migraine and Menière’s disease: cVEMPs make the difference

Key gait findings for diagnosing three syndromic categories of dynamic instability in patients with balance disorders