Altered functional brain connectivity in patients with visually induced dizziness

Van Ombergen, Angelique; Heine, Lizette; Jillings, Steven; Roberts, Edward R.; Jeurissen, Ben; Van Rompaey, Vincent; Mucci, Viviana; Vanhecke, Stefanie; Sijbers, Jan; Vanhevel, Floris; Sunaert, Stefan; Bahri, Mohamed Ali; Van de Heyning, Paul H.; Laureys, Steven; Wuyts, Floris L.

doi:10.1016/j.nicl.2017.02.020

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Altered functional brain connectivity in patients with visually induced dizziness

Van Ombergen, Angelique; Heine, Lizette; Jillings, Steven et al.

2017 • In NeuroImage, 14, p. 538-545

Peer Reviewed verified by ORBi

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https://hdl.handle.net/2268/212316

DOI
10.1016/j.nicl.2017.02.020

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28331800

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Keywords :

rsfMRI; Visually induced dizziness; VID; Functional connectivity; Vertigo; Vestibular

Abstract :

[en] Background: Vestibular patients occasionally report aggravation or triggering of their symptoms by visual stimuli, which is called visually induced dizziness (VID). These patients therefore experience dizziness, discomfort, disorientation and postural unsteadiness. The underlying pathophysiology of VID is still poorly understood. Objective: The aimof the current explorative study was to gain a first insight in the underlying neural aspects of VID. Methods:We included 10 VID patients and 10 healthymatched controls, all ofwhich underwent a resting state fMRI scan session. Changes in functional connectivitywere explored bymeans of the intrinsic connectivity contrast (ICC). Seed-based analysis was subsequently performed in visual and vestibular seeds. Results: We found a decreased functional connectivity in the right central operculum (superior temporal gyrus), as well as increased functional connectivity in the occipital pole in VID patients as compared to controls in a hypothesis-free analysis. A weaker functional connectivity between the thalamus and most of the right putamen was measured in VID patients in comparison to controls in a seed-based analysis. Furthermore, also by means of a seed-based analysis, a decreased functional connectivity between the visual associative area and the left parahippocampal gyrus was found in VID patients. Additionally,we found increased functional connectivity between thalamus and occipital and cerebellar areas in the VID patients, as well as between the associative visual cortex and both middle frontal gyrus and precuneus. Conclusions:We found alterations in the visual and vestibular cortical network in VID patients that could underlie the typical VID symptoms such as a worsening of their vestibular symptoms when being exposed to challenging visual stimuli. These preliminary findings provide the first insights into the underlying functional brain connectivity in VID patients. Future studies should extend these findings by employing larger sample sizes, by investigating specific task-based paradigms in these patients and by exploring the implications for treatment.

Disciplines :

Neurology

Author, co-author :

Van Ombergen, Angelique

Heine, Lizette ; Université de Liège > Centre de recherches du cyclotron

Jillings, Steven ; University of Antwerp

Roberts, Edward R.

Jeurissen, Ben

Van Rompaey, Vincent

Mucci, Viviana

Vanhecke, Stefanie

Sijbers, Jan

Vanhevel, Floris

More authors (5 more)

Language :

English

Title :

Altered functional brain connectivity in patients with visually induced dizziness

Publication date :

2017

Journal title :

NeuroImage

ISSN :

1053-8119

eISSN :

1095-9572

Publisher :

Elsevier Science, Orlando, United States - Florida

Volume :

Pages :

538-545

Peer reviewed :

Peer Reviewed verified by ORBi

Available on ORBi :

since 29 June 2017

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Bibliography

Ahmad, H., Arshad, Q., Siddiqui, S., Nigmatullina, Y., Patel, M., Bronstein, A.M., Roberts, R.E., Applications of neuromodulation to explore vestibular cortical processing; new insights into the effects of direct current cortical modulation upon pursuit, VOR and VOR suppression. Journal of Vestibular Research: Equilibrium and Orientation, 2014, 453–458.
Aminoff, E., Gronau, N., Bar, M., The parahippocampal cortex mediates spatial and nonspatial associations. Cereb. Cortex 17 (2007), 1493–1503.
Arshad, Q., Nigmatullina, Y., Roberts, R., Bhrugubanda, V., Asavarut, P., Bronstein, A., Left cathodal trans-cranial direct current stimulation of the parietal cortex leads to an asymmetrical modulation of the vestibular-ocular reflex. Brain Stim 7 (2014), 85–91.
Behzadi, Y., Restom, K., Liau, J., Liu, T.T., A component based noise correction method (CompCor) for BOLD and perfusion based fMRI. NeuroImage 37 (2007), 90–101.
Bense, S., Stephan, T., Yousry, T.A., Brandt, T., Dieterich, M., Multisensory cortical signal increases and decreases during vestibular galvanic stimulation (fMRI) [online]. J. Neurophysiol. 85 (2001), 886–899 http://www.ncbi.nlm.nih.gov/pubmed/11160520.
Bergenius, J., Perols, O., Vestibular neuritis: a follow-up study. Acta Otolaryngol. 119 (1999), 895–899.
Bisdorff, A., von Brevern, M., Lempert, T., Newman-Toker, D., Classification of vestibular symptoms: towards an international classification of vestibular disorders. J. Vestib. Res. 19 (2009), 1–13.
Bottini, G., Sterzi, R., Paulesu, E., Vallar, G., Cappa, S.F., Erminio, F., Passingham, R.E., Frith, C.D., Frackowiak, R.S.J., Identification of the central vestibular projections in man: a positron emission tomography activation study. Exp. Brain Res. 99 (1994), 164–169.
Brandt, T., Phobic postural vertigo. Neurology 46 (1996), 1515–1519.
Brandt, T., Bartenstein, P., Janek, A., Dieterich, M., Reciprocal inhibitory visual-vestibular interaction. Visual motion stimulation deactivates the parieto-insular vestibular cortex. Brain 121 (1998), 1749–1758.
Bronstein, A.M., The visual vertigo syndrome. Acta Otolaryngol. Suppl. 520:Pt 1 (1995), 45–48.
Bronstein, A.M., Visual vertigo syndrome: clinical and posturography findings [online]. J. Neurol. Neurosurg. Psychiatry 59 (1995), 472–476 http://jnnp.bmj.com/content/59/5/472.short.
Cavanna, A.E., Trimble, M.R., The precuneus: a review of its functional anatomy and behavioural correlates. Brain 129 (2006), 564–583.
Cha, Y.-H., Deblieck, C., Wu, A.D., Double-blind sham-controlled crossover trial of repetitive transcranial magnetic stimulation for Mal de Debarquement Syndrome. Otol Neurotol 37 (2016), 805–812.
Cousins, S., Cutfield, N.J., Kaski, D., Palla, A., Seemungal, B.M., Golding, J.F., Staab, J.P., Bronstein, A.M., Visual dependency and dizziness after vestibular neuritis. PLoS One, 9, 2014.
Della-Justina, H.M., Gamba, H.R., Lukasova, K., Nucci-da-Silva, M.P., Winkler, A.M., Amaro, E., Interaction of brain areas of visual and vestibular simultaneous activity with fMRI. Exp. Brain Res. 233 (2014), 237–252.
Deutschländer, A., Bense, S., Stephan, T., Schwaiger, M., Brandt, T., Dieterich, M., Sensory system interactions during simultaneous vestibular and visual stimulation in PET. Hum. Brain Mapp. 16 (2002), 92–103.
Dieterich, M., Brandt, T., Thalamic infarctions: differential effects on vestibular function in the roll plane (35 patients). Neurology 43 (1993), 1732–1740.
Dieterich, M., Brandt, T., Vestibular system: anatomy and functional magnetic resonance imaging. Neuroimaging ClinNAm 11:ix (2001), 263–273.
Dieterich, M., Brandt, T., The bilateral central vestibular system: its pathways, functions, and disorders. Ann. N. Y. Acad. Sci. 1343 (2015), 10–26.
Dieterich, M., Bense, S., Lutz, S., Drzezga, A., Stephan, T., Bartenstein, P., Brandt, T., Dominance for vestibular cortical function in the non-dominant hemisphere. Cereb. Cortex 13 (2003), 994–1007.
Dieterich, M., Bartenstein, P., Spiegel, S., Bense, S., Schwaiger, M., Brandt, T., Thalamic infarctions cause side-specific suppression of vestibular cortex activations. Brain 128 (2005), 2052–2067.
Dieterich, M., Bauermann, T., Best, C., Stoeter, P., Schlindwein, P., Evidence for cortical visual substitution of chronic bilateral vestibular failure (an fMRI study). Brain 130 (2007), 2108–2116.
Fasold, O., von Brevern, M., Kuhberg, M., et al. Human vestibular cortex as identified with caloric stimulation in functional magnetic resonance imaging. NeuroImage 17 (2002), 1384–1393.
Fink, G.R., Marshall, J.C., Weiss, P.H., Stephan, T., Grefkes, C., Shah, N.J., Zilles, K., Dieterich, M., Performing allocentric visuospatial judgments with induced distortion of the egocentric reference frame: an fMRI study with clinical implications. NeuroImage 20 (2003), 1505–1517.
Goldberg, J.M., Wilson, V.J., Cullen, K.E., Angelaki, D.E., Broussard, D.M., Buttner-Ennever, J., Fukushima, K., Minor, L.B., The Vestibular System: A Sixth Sense. 2012.
Göttlich, M., Jandl, N.M., Wojak, J.F., Sprenger, A., Von Der Gablentz, J., Münte, T.F., Krämer, U.M., Helmchen, C., Altered resting-state functional connectivity in patients with chronic bilateral vestibular failure. NeuroImage Clin 4 (2014), 488–499.
Guerraz, M., Yardley, L., Bertholon, P., Pollak, L., Rudge, P., Gresty, M.A., Bronstein, A.M., Visual vertigo: symptom assessment, spatial orientation and postural control. Brain 124 (2001), 1646–1656.
Habas, C., Kamdar, N., Nguyen, D., Prater, K., Beckmann, C.F., Menon, V., Greicius, M.D., Distinct cerebellar contributions to intrinsic connectivity networks. J. Neurosci. 29 (2009), 8586–8594.
Hallquist, M., Hwang, K., Luna, B., The nuisance of nuisance regression: spectral misspecification in a common approach to resting-state fMRI preprocessing reintroduces noise and obscures functional connectivity. NeuroImage 82 (2013), 208–225.
Hitier, M., Besnard, S., Smith, P.F., Vestibular pathways involved in cognition. Front. Integr. Neurosci., 8, 2014, 59.
Hong, S.K., Kim, H.J., Lee, H.J., Changes in the gray matter volume during compensation after vestibular neuritis: a longitudinal VBM study. Restor. Neurol. Neurosci. 32 (2014), 663–673.
Hwang, S., Agada, P., Kiemel, T., Jeka, J.J., Dynamic reweighting of three modalities for sensor fusion. PLoS One, 9, 2014.
Iglói, K., Doeller, C.F., Paradis, A.L., Benchenane, K., Berthoz, A., Burgess, N., Rondi-Reig, L., Interaction between hippocampus and cerebellum crus i in sequence-based but not place-based navigation. Cereb. Cortex 25 (2015), 4146–4154.
Indovina, I., Maffe, V., Bosco, G., Zago, M., Macaluso, E., Lacquaniti, F., Representation of visual gravitational motion in the human vestibular cortex. Science (80- ) 208 (2005), 416–419.
Indovina, I., Riccelli, R., Chiarella, G., Petrolo, C., Augimeri, A., Giofre, L., Lacquaniti, F., Staab, J., Passamonti, L., Role of the insula and vestibular system in patients with chronic subjective dizziness: an fMRI study using sound-evoked vestibular stimulation. Front. Behav. Neurosci., 9, 2015, 334.
Jacob, R.G., Lilienfeld, S.O., Furman, J.M.R., Durrant, J.D., Turner, S.M., Panic disorder with vestibular dysfunction: further clinical observations and description of space and motion phobic stimuli. J Anxiety Disord 3 (1989), 117–130.
Kapfhammer, H., Mayer, C., Hock, U., Huppert, D., Dieterich, M., Brandt, T., Course of illness in phobic postural vertigo. Acta Neurol. Scand. 95 (1997), 23–28.
Kellermann, T., Regenbogen, C., De Vos, M., Mossnang, C., Finkelmeyer, A., Habel, U., Effective connectivity of the human cerebellum during visual attention. J. Neurosci. 32 (2012), 11453–11460.
Kelly, C., Toro, R., Di Martino, A., Cox, C., Bellec, P., Castellanos, F., Milham, M., A convergent functional architecture of the insula emerges across imaging modalities. NeuroImage 61 (2012), 1129–1142.
Kikuchi, M., Naito, Y., Senda, M., Okada, T., Shinohara, S., Fujiwara, K., Hori, S.-Y., Tona, Y., Yamazaki, H., Cortical activation during optokinetic stimulation - an fMRI study. Acta Otolaryngol. 129 (2009), 440–443.
Kirsch, V., Keeser, D., Hergenroeder, T., Erat, O., Ertl-Wagner, B., Brandt, T., Dieterich, M., Structural and functional connectivity mapping of the vestibular circuitry from human brainstem to cortex. Brain Struct. Funct. 221 (2016), 1291–1308.
Lai, H., Tsumori, T., Shiroyama, T., Yokota, S., Nakano, K., Yasui, Y., Morphological evidence for a vestibulo-thalamo-striatal pathway via the parafascicular nucleus in the rat. Brain Res. 872 (2000), 208–214.
Lee, P.H., Lee, J.H., Joo, U.S., Thalamic infarct presenting with thalamic astasia. Eur. J. Neurol. 12 (2005), 317–319.
Leichnetz, G., Connections of the medial posterior parietal cortex (area 7m) in the monkey. Anat. Rec. 263 (2001), 215–236.
Lobel, E., Kleine, J.F., Bihan, D.L., Leroy-Willig, A., Berthoz, A., Functional MRI of galvanic vestibular stimulation. J. Neurophysiol. 80 (1998), 2699–2709.
Longridge, N.S., Mallinson, A.I., Denton, A., Visual vestibular mismatch in patients treated with intratympanic gentamicin for Meniere's disease. J. Otolaryngol. 31 (2002), 5–8.
Lopez, C., Blanke, O., The thalamocortical vestibular system in animals and humans. Brain Res. Rev. 67 (2011), 119–146.
Lopez, C., Blanke, O., Mast, F., The vestibular cortex in the human brain revealed by coordinate-based activation likelihood estimation meta-analysis. Neuroscience 60 (2012), 162–169.
Mallinson, A.I., Visual Vestibular Mismatch: A Poorly Understood Presentation of Balance System Disease. 2011.
Martuzzi, R., Ramani, R., Qiu, M., Shen, X., Papademetris, X., Constable, R.T., A whole-brain voxel based measure of intrinsic connectivity contrast reveals local changes in tissue connectivity with anesthetic without a priori assumptions on thresholds or regions of interest. NeuroImage 58 (2011), 1044–1050.
Mikl, M., Mareček, R., Hluštík, P., Pavlicová, M., Drastich, A., Chlebus, P., Brázdil, M., Krupa, P., Effects of spatial smoothing on fMRI group inferences. Magn. Reson. Imaging 26 (2008), 490–503.
Miller, W.L., Maffei, V., Bosco, G., Iosa, M., Zago, M., Macaluso, E., Lacquaniti, F., Vestibular nuclei and cerebellum put visual gravitational motion in context. J. Neurophysiol. 99 (2008), 1969–1982.
Murphy, K., Birn, R.M., Handwerker, D.A., Jones, T.B., Bandettini, P.A., The impact of global signal regression on resting state correlations: are anti-correlated networks introduced?. NeuroImage 44 (2009), 893–905.
Okinaka, Y., Sekitani, T., Okazaki, H., Miura, M., Tahara, T., Progress of caloric response of vestibular neuronitis. Acta Otolaryngol. Suppl. 503 (1993), 18–22.
Page, N.G., Gresty, M.A., Motorist's vestibular disorientation syndrome. J. Neurol. Neurosurg. Psychiatry 48 (1985), 729–735.
Pavlou, M., Davies, R., Bronstein, A., The assessment of increased sensitivity to visual stimuli in patients with chronic dizziness. J. Vestib. Res. 16 (2006), 223–231.
Pavlou, M., Quinn, C., Murray, K., Spyridakou, C., Faldon, M., Bronstein, A.M., The effect of repeated visual motion stimuli on visual dependence and postural control in normal subjects. Gait Posture 33 (2011), 113–118.
Pavlou, M., Bronstein, A.M., Davies, R.A., Randomized trial of supervised versus unsupervised optokinetic exercise in persons with peripheral vestibular disorders. Neurorehabil. Neural Repair 27 (2013), 208–218.
Peterka, R.J., Sensorimotor integration in human postural control. J. Neurophysiol. 88 (2002), 1097–1118.
Pollak, L., Osherov, M., Berkovitz, N., Beckerman, I., Stryjer, R., Tal, S., Magnetic resonance brain imaging in patients with visual vertigo. Brain Behav, 5, 2015.
Powell, H., Guye, M., Parker, G., Symms, M., Boulby, P., Koepp, M., Barker, G., Duncan, J., Noninvasive in vivo demonstration of the connections of the human parahippocampal gyrus. NeuroImage 22 (2004), 740–747.
Roberts, D., Marcelli, V., Gillen, J., Carey, J., Della Santina, C., Zee, D., MRI magnetic field stimulates rotational sensors of the brain. Curr. Biol. 21 (2011), 1635–1640.
Roberts, R., Ahmad, H., Arshad, Q., Patel, M., Dima, D., Leech, R., Seemungal, B., Sharp, D., Bronstein, A., Functional neuroimaging of visuo-vestibular interaction. Brain Struct. Funct., 2016, 10.1007/s00429-016-1344-4.
Saad, Z.S., Gotts, S.J., Murphy, K., Chen, G., Jo, H.J., Martin, A., Cox, R.W., Trouble at rest: how correlation patterns and group differences become distorted after global signal regression. Brain Connect. 2 (2012), 25–32.
Sang, L., Qin, W., Lui, Y., Han, W., Zhang, Y., Jiang, T., Yu, C., Resting-state functional connectivity of the vermal and hemispheric subregions of the cerebellum with both the cerebral cortical networks and subcortical structures. NeuroImage 61 (2012), 1213–1225.
Sato, N., Nakamura, K., Visual response properties of neurons in the parahippocampal cortex of monkeys [online]. J. Neurophysiol. 90 (2003), 876–886 (papers://fd89a684-cdfc-42fd-9184-d7b50afefca5/Paper/p14).
Staab, J.P., Ruckenstein, M.J., Chronic dizziness and anxiety: effect of course of illness on treatment outcome. Arch. Otolaryngol. Head Neck Surg. 131 (2005), 675–679.
Staab, J.P., Ruckenstein, M.J., Amsterdam, J.D., A prospective trial of sertraline for chronic subjective dizziness. Laryngoscope 114 (2004), 1637–1641.
Staab, J.P., Rohe, D.E., Eggers, S.D.Z., Shepard, N.T., Anxious, introverted personality traits in patients with chronic subjective dizziness. J. Psychosom. Res. 76 (2014), 80–83.
Stephan, T., Deutschländer, A., Nolte, A., Schneider, E., Wiesmann, M., Brandt, T., Dieterich, M., Functional MRI of galvanic vestibular stimulation with alternating currents at different frequencies. NeuroImage 26 (2005), 721–732.
Stiles, L., Smith, P.F., The vestibular-basal ganglia connection: balancing motor control. Brain Res. 1597 (2015), 180–188.
Suzuki, M., Kitano, H., Ito, R., Kitanishi, T., Yazawa, Y., Ogawa, T., Shiino, A., Kitajima, K., Cortical and subcortical vestibular response to caloric stimulation detected by functional magnetic resonance imaging. Cogn. Brain Res. 12 (2001), 441–449.
Van Ombergen, A., Lubeck, A.J., Van Rompaey, V., Maes, L.K., Stins, J.F., Van De Heyning, P.H., Wuyts, F.L., Bos, J.E., The effect of optokinetic stimulation on perceptual and postural symptoms in visual vestibular mismatch patients. PLoS One, 11, 2016.
Whitfield-Gabrieli, S., Nieto-Castanon, A., A functional connectivity toolbox for correlated and anticorrelated brain networks. Brain Connect. 2 (2012), 125–141.
Witkin, H., The perception of the upright. Sci. Am. 200 (1959), 51–56.
Witkin, H., Asch, S., Studies in space orientation; further experiments on perception of the upright with displaced visual fields. J. Exp. Psychol. 38 (1948), 762–782.
Wong, C.W., Olafsson, V., Tal, O., Liu, T.T., Anti-correlated networks, global signal regression, and the effects of caffeine in resting-state functional MRI. NeuroImage 63 (2012), 356–364.
Wuyts, F.L., Van Rompaey, V., Maes, L.K., “SO STONED”: common sense approach of the dizzy patient. Front Surg, 3, 2016.
Zeki, S., Watson, J.D., Lueck, C.J., Friston, K.J., Kennard, C., Frackowiak, R.S., A direct demonstration of functional specialization in human visual cortex. J. Neurosci. 11 (1991), 641–649.
Zu Eulenburg, P., Stoeter, P., Dieterich, M., Voxel-based morphometry depicts central compensation after vestibular neuritis. Ann. Neurol. 68 (2010), 241–249.
Zu Eulenburg, P., Caspers, S., Roski, C., Eickhoff, S.B., Meta-analytical definition and functional connectivity of the human vestibular cortex. NeuroImage 60 (2012), 162–169.