Effects of repetitive galvanic vestibular stimulation on spatial neglect and verticality perception—a randomised sham-controlled trial

References

• Adair, J. C., Na, D. L., Schwartz, R. L., & Heilman, K. M. (2003). Caloric stimulation in neglect: Evaluation of response as a function of neglect type. Journal of the International Neuropsychological Society, 9(7), 983–988. doi: 10.1017/S1355617703970020
   PubMed Web of Science ®Google Scholar
• Barra, J., Marquer, A., Joassin, R., Reymond, C., Metge, L., Chauvineau, V., & Perennou, D. (2010). Humans use internal models to construct and update a sense of verticality. Brain: A Journal of Neurology, 133(Pt 12), 3552–3563. doi: 10.1093/brain/awq311
   PubMedGoogle Scholar
• Been, G., Ngo, T. T., Miller, S. M., & Fitzgerald, P. B. (2007). The use of tDCS and CVS as methods of non-invasive brain stimulation. Brain Research Reviews, 56(2), 346–361. doi: 10.1016/j.brainresrev.2007.08.001
   PubMedGoogle Scholar
• Bense, S., Stephan, T., Yousry, T. A., Brandt, T., & Dieterich, M. (2001). Multisensory cortical signal increases and decreases during vestibular galvanic stimulation (fMRI). Journal of Neurophysiology, 85(2), 886–899. doi: 10.1152/jn.2001.85.2.886
   PubMed Web of Science ®Google Scholar
• Braem, B., Honore, J., Rousseaux, M., Saj, A., & Coello, Y. (2014). Integration of visual and haptic informations in the perception of the vertical in young and old healthy adults and right brain-damaged patients. Neurophysiologie Clinique/Clinical Neurophysiology, 44(1), 41–48. doi: 10.1016/j.neucli.2013.10.137
   PubMed Web of Science ®Google Scholar
• Brandt, T., Glasauer, S., Strupp, M., & Dieterich, M. (2009). Spatial neglect: Hypothetical mechanisms of disturbed interhemispheric crosstalk for orientation. Annals of the New York Academy of Sciences, 1164, 216–221. doi: 10.1111/j.1749-6632.2009.03860.x
   PubMed Web of Science ®Google Scholar
• Cappa, S., Sterzi, R., Vallar, G., & Bisiach, E. (1987). Remission of hemineglect and anosognosia during vestibular stimulation. Neuropsychologia, 25(5), 775–782. doi: 10.1016/0028-3932(87)90115-1
   PubMed Web of Science ®Google Scholar
• Di Monaco, M., Schintu, S., Dotta, M., Barba, S., Tappero, R., & Gindri, P. (2011). Severity of unilateral spatial neglect is an independent predictor of functional outcome after acute inpatient rehabilitation in individuals with right hemispheric stroke. Archives of Physical Medicine and Rehabilitation, 92(8), 1250–1256. doi: 10.1016/j.apmr.2011.03.018
   PubMed Web of Science ®Google Scholar
• Field, A. (2012). Discovering statistics using IBM SPSS statistics (4th ed.). London: Sage.
   Google Scholar
• Fink, G. R., Marshall, J. C., Weiss, P. H., Stephan, T., Grefkes, C., Shah, N. J., … Dieterich, M. (2003). Performing allocentric visuospatial judgments with induced distortion of the egocentric reference frame: An fMRI study with clinical implications. NeuroImage, 20(3), 1505–1517. doi: 10.1016/j.neuroimage.2003.07.006
   PubMed Web of Science ®Google Scholar
• Fitzpatrick, R. C., & Day, B. L. (2004). Probing the human vestibular system with galvanic stimulation. Journal of Applied Physiology, 96(6), 2301–2316. doi: 10.1152/japplphysiol.00008.2004
   PubMed Web of Science ®Google Scholar
• Fong, K. N., Yang, N. Y., Chan, M. K., Chan, D. Y., Lau, A. F., Chan, D. Y., … Chan C. C. (2013). Combined effects of sensory cueing and limb activation on unilateral neglect in subacute left hemiplegic stroke patients: A randomized controlled pilot study. Clinical Rehabilitation, 27(7), 628–637. doi: 10.1177/0269215512471959
   PubMed Web of Science ®Google Scholar
• Funk, J., Finke, K., Muller, H. J., Preger, R., & Kerkhoff, G. (2010). Systematic biases in the tactile perception of the subjective vertical in patients with unilateral neglect and the influence of upright vs. supine posture. Neuropsychologia, 48(1), 298–308. doi: 10.1016/j.neuropsychologia.2009.09.018
   PubMed Web of Science ®Google Scholar
• Funk, J., Finke, K., Muller, H. J., Utz, K. S., & Kerkhoff, G. (2010). Effects of lateral head inclination on multimodal spatial orientation judgments in neglect: Evidence for impaired spatial orientation constancy. Neuropsychologia, 48(6), 1616–1627. doi: 10.1016/j.neuropsychologia.2010.01.029
   PubMed Web of Science ®Google Scholar
• Funk, J., Finke, K., Muller, H. J., Utz, K. S., & Kerkhoff, G. (2011). Visual context modulates the subjective vertical in neglect: Evidence for an increased rod-and-frame-effect. Neuroscience, 173, 124–134. doi: 10.1016/j.neuroscience.2010.10.067
   PubMed Web of Science ®Google Scholar
• Gillen, R., Tennen, H., & McKee, T. (2005). Unilateral spatial neglect: Relation to rehabilitation outcomes in patients with right hemisphere stroke. Archives of Physical Medicine and Rehabilitation, 86(4), 763–767. doi: 10.1016/j.apmr.2004.10.029
   PubMed Web of Science ®Google Scholar
• Guinet, M., & Michel, C. (2013). Prism adaptation and neck muscle vibration in healthy individuals: Are two methods better than one? Neuroscience, 254, 443–451. doi: 10.1016/j.neuroscience.2013.08.067
   PubMed Web of Science ®Google Scholar
• Heilman, K. M., Valenstein, E., & Watson, R. T. (2000). Neglect and related disorders. Seminars in Neurology, 20(4), 463–470. doi: 10.1055/s-2000-13179
   PubMed Web of Science ®Google Scholar
• Karnath, H. O. (1994). Disturbed coordinate transformation in the neural representation of space as the crucial mechanism leading to neglect. Neuropsychological Rehabilitation, 4(2), 147–150. doi: 10.1080/09602019408402273
   Google Scholar
• Karnath, H. O. (1997). Spatial orientation and the representation of space with parietal lobe lesions. Philosophical Transactions of the Royal Society B: Biological Sciences, 352(1360), 1411–1419. doi: 10.1098/rstb.1997.0127
   PubMed Web of Science ®Google Scholar
• Keller, I., Lefin-Rank, G., Losch, J., & Kerkhoff, G. (2009). Combination of pursuit eye movement training with prism adaptation and arm movements in neglect therapy: A pilot study. Neurorehabilitation and Neural Repair, 23(1), 58–66. doi: 10.1177/1545968308317438
   PubMed Web of Science ®Google Scholar
• Kerkhoff, G. (1999). Multimodal spatial orientation deficits in left-sided visual neglect. Neuropsychologia, 37(12), 1387–1405. doi: 10.1016/S0028-3932(99)00031-7
   PubMed Web of Science ®Google Scholar
• Kerkhoff, G., Bucher, L., Brasse, M., Leonhart, E., Holzgraefe, M., Volzke, V., … Reinhart, S. (2014). Smooth pursuit “bedside” training reduces disability and unawareness during the activities of daily Living in neglect: A randomized controlled trial. Neurorehabilitation and Neural Repair, 28(6), 554–563. doi: 10.1177/1545968313517757
   PubMed Web of Science ®Google Scholar
• Kerkhoff, G., Reinhart, S., Ziegler, W., Artinger, F., Marquardt, C., & Keller, I. (2013). Smooth pursuit eye movement training promotes recovery from auditory and visual neglect: A randomized controlled study. Neurorehabilitation and Neural Repair, 27(9), 789–798. doi: 10.1177/1545968313491012
   PubMed Web of Science ®Google Scholar
• Kerkhoff, G., & Schenk, T. (2012). Rehabilitation of neglect: An update. Neuropsychologia, 50(6), 1072–1079. doi: 10.1016/j.neuropsychologia.2012.01.024
   PubMed Web of Science ®Google Scholar
• Kerkhoff, G., & Zoelch, C. (1998). Disorders of visuospatial orientation in the frontal plane in patients with visual neglect following right or left parietal lesions. Experimental Brain Research Experimentelle Hirnforschung Experimentation Cerebrale, 122(1), 108–120. doi: 10.1007/s002210050497
   PubMed Web of Science ®Google Scholar
• Lisa, L. P., Jughters, A., & Kerckhofs, E. (2013). The effectiveness of different treatment modalities for the rehabilitation of unilateral neglect in stroke patients: A systematic review. NeuroRehabilitation, 33(4), 611–620.
   PubMed Web of Science ®Google Scholar
• Lobel, E., Kleine, J. F., Bihan, D. L., Leroy-Willig, A., & Berthoz, A. (1998). Functional MRI of galvanic vestibular stimulation. Journal of Neurophysiology, 80(5), 2699–2709. doi: 10.1152/jn.1998.80.5.2699
   PubMed Web of Science ®Google Scholar
• MacDougall, H. G., Brizuela, A. E., Burgess, A. M., & Curthoys, I. S. (2002). Between-subject variability and within-subject reliability of the human eye-movement response to bilateral galvanic (DC) vestibular stimulation. Experimental Brain Research Experimentelle Hirnforschung Experimentation Cerebrale, 144(1), 69–78. doi: 10.1007/s00221-002-1038-4
   PubMed Web of Science ®Google Scholar
• MacDougall, H. G., Brizuela, A. E., & Curthoys, I. S. (2003). Linearity, symmetry and additivity of the human eye-movement response to maintained unilateral and bilateral surface galvanic (DC) vestibular stimulation. Experimental Brain Research Experimentelle Hirnforschung Experimentation Cerebrale, 148(2), 166–175. doi: 10.1007/s00221-002-1289-0
   PubMed Web of Science ®Google Scholar
• Moon, S., Lee, B., & Na, D. (2006). Therapeutic effects of caloric stimulation and optokinetic stimulation on hemispatial neglect. Journal of Clinical Neurology, 2(1), 12–28. doi: 10.3988/jcn.2006.2.1.12
   PubMedGoogle Scholar
• Oppenlander, K., Keller, I., Karbach, J., Schindler, I., Kerkhoff, G., & Reinhart, S. (2015). Subliminal galvanic-vestibular stimulation influences ego- and object-centred components of visual neglect. Neuropsychologia, 74, 170–177. doi: 10.1016/j.neuropsychologia.2014.10.039
   PubMed Web of Science ®Google Scholar
• Oppenlander, K., Utz, K. S., Reinhart, S., Keller, I., Kerkhoff, G., & Schaadt, A. K. (2015). Subliminal galvanic-vestibular stimulation recalibrates the distorted visual and tactile subjective vertical in right-sided stroke. Neuropsychologia, 74, 178–183. doi: 10.1016/j.neuropsychologia.2015.03.004
   PubMed Web of Science ®Google Scholar
• Piccardi, L., Nico, D., Bureca, I., Matano, A., & Guariglia, C. (2006). Efficacy of visuo-spatial training in right-brain damaged patients with spatial hemineglect and attention disorders. Cortex; a Journal Devoted to the Study of the Nervous System and Behavior, 42(7), 973–982. doi: 10.1016/S0010-9452(08)70203-X
   PubMed Web of Science ®Google Scholar
• Pitteri, M., Arcara, G., Passarini, L., Meneghello, F., & Priftis, K. (2013). Is two better than one? Limb activation treatment combined with contralesional arm vibration to ameliorate signs of left neglect. Frontiers in Human Neuroscience, 7, 140–149. doi: 10.3389/fnhum.2013.00460
   PubMed Web of Science ®Google Scholar
• Pizzamiglio, L., Antonucci, G., Judica, A., Montenero, P., Razzano, C., & Zoccolotti, P. (1992). Cognitive rehabilitation of the hemineglect disorder in chronic patients with unilateral right brain damage. Journal of Clinical and Experimental Neuropsychology, 14(6), 901–923. doi: 10.1080/01688639208402543
   PubMed Web of Science ®Google Scholar
• Rode, G., & Perenin, M. T. (1994). Temporary remission of representational hemineglect through vestibular stimulation. Neuroreport, 5(8), 869–872. doi: 10.1097/00001756-199404000-00004
   PubMed Web of Science ®Google Scholar
• Rorsman, I., Magnusson, M., & Johansson, B. B. (1999). Reduction of visuo-spatial neglect with vestibular galvanic stimulation. Scandinavian Journal of Rehabilitation Medicine, 31(2), 117–124. doi: 10.1080/003655099444632
   PubMedGoogle Scholar
• Rubens, A. B. (1985). Caloric stimulation and unilateral visual neglect. Neurology, 35(7), 1019–1024. doi: 10.1212/WNL.35.7.1019
   PubMed Web of Science ®Google Scholar
• Saj, A., Honore, J., Bernati, T., Coello, Y., & Rousseaux, M. (2005). Subjective visual vertical in pitch and roll in right hemispheric stroke. Stroke; a Journal of Cerebral Circulation, 36(3), 588–591. doi: 10.1161/01.STR.0000155740.44599.48
   PubMed Web of Science ®Google Scholar
• Saj, A., Honore, J., & Rousseaux, M. (2006). Perception of the vertical in patients with right hemispheric lesion: Effect of galvanic vestibular stimulation. Neuropsychologia, 44(8), 1509–1512. doi: 10.1016/j.neuropsychologia.2005.11.018
   PubMed Web of Science ®Google Scholar
• Schmidt, L., Utz, K. S., Depper, L., Adams, M., Schaadt, A. K., Reinhart, S., Kerkhoff, G. (2013). Now you feel BOTH: Galvanic vestibular stimulation induces lasting improvements in the rehabilitation of chronic tactile extinction. Frontiers in Human Neuroscience, 7, 88–98.
   PubMed Web of Science ®Google Scholar
• Scott, N. W., McPherson, G. C., Ramsay, C. R., & Campbell, M. K. (2002). The method of minimization for allocation to clinical trials. A review. Controlled Clinical Trials, 23(6), 662–674. doi: 10.1016/S0197-2456(02)00242-8
   PubMedGoogle Scholar
• Severac Cauquil, A., Faldon, M., Popov, K., Day, B. L., & Bronstein, A. M. (2003). Short-latency eye movements evoked by near-threshold galvanic vestibular stimulation. Experimental Brain Research Experimentelle Hirnforschung Experimentation Cerebrale, 148(3), 414–418. doi: 10.1007/s00221-002-1326-z
   PubMed Web of Science ®Google Scholar
• Sturt, R., & David Punt, T. (2013). Caloric vestibular stimulation and postural control in patients with spatial neglect following stroke. Neuropsychological Rehabilitation, 23(2), 299–316. doi: 10.1080/09602011.2012.755831
   PubMed Web of Science ®Google Scholar
• Utz, K. S., Keller, I., Artinger, F., Stumpf, O., Funk, J., & Kerkhoff, G. (2011). Multimodal and multispatial deficits of verticality perception in hemispatial neglect. Neuroscience, 188, 68–79. doi: 10.1016/j.neuroscience.2011.04.068
   PubMed Web of Science ®Google Scholar
• Utz, K. S., Keller, I., Kardinal, M., & Kerkhoff, G. (2011). Galvanic vestibular stimulation reduces the pathological rightward line bisection error in neglect—A sham stimulation-controlled study. Neuropsychologia, 49(5), 1219–1225. doi: 10.1016/j.neuropsychologia.2011.02.046
   PubMed Web of Science ®Google Scholar
• Utz, K. S., Korluss, K., Schmidt, L., Rosenthal, A., Oppenlander, K., Keller, I., & Kerkhoff, G. (2011). Minor adverse effects of galvanic vestibular stimulation in persons with stroke and healthy individuals. Brain Injury: [BI], 25(11), 1058–1069. doi: 10.3109/02699052.2011.607789
   PubMed Web of Science ®Google Scholar
• Vallar, G. (1997). Spatial frames of reference and somatosensory processing: A neuropsychological perspective. Philosophical Transactions of the Royal Society B: Biological Sciences, 352(1360), 1401–1409. doi: 10.1098/rstb.1997.0126
   PubMed Web of Science ®Google Scholar
• Vallar, G., Sterzi, R., Bottini, G., Cappa, S., & Rusconi, M. L. (1990). Temporary remission of left hemianesthesia after vestibular stimulation. A sensory neglect phenomenon. Cortex; a Journal Devoted to the Study of the Nervous System and Behavior, 26(1), 123–131. doi: 10.1016/S0010-9452(13)80078-0
   PubMed Web of Science ®Google Scholar
• Volkening, K., Bergmann, J., Keller, I., Wuehr, M., Muller, F., & Jahn, K. (2014). Verticality perception during and after galvanic vestibular stimulation. Neuroscience Letters, 581, 75–79. doi: 10.1016/j.neulet.2014.08.028
   PubMed Web of Science ®Google Scholar
• Wilkinson, D., Zubko, O., Degutis, J., Milberg, W., & Potter, J. (2010). Improvement of a figure copying deficit during subsensory galvanic vestibular stimulation. Journal of Neuropsychology, 4(Pt 1), 107–118. doi: 10.1348/174866409X468205
   PubMedGoogle Scholar
• Wilkinson, D., Zubko, O., Sakel, M., Coulton, S., Higgins, T., & Pullicino, P. (2014). Galvanic vestibular stimulation in hemi-spatial neglect. Frontiers in Integrative Neuroscience, 8, 1–12. doi: 10.3389/fnint.2014.00004
   PubMedGoogle Scholar
• Yelnik, A. P., Lebreton, F. O., Bonan, I. V., Colle, F. M., Meurin, F. A., Guichard, J. P., & Vicaut, E. (2002). Perception of verticality after recent cerebral hemispheric stroke. Stroke; a Journal of Cerebral Circulation, 33(9), 2247–2253. doi: 10.1161/01.STR.0000027212.26686.48
   PubMed Web of Science ®Google Scholar
• Zwergal, A., Rettinger, N., Frenzel, C., Dieterich, M., Brandt, T., & Strupp, M. (2009). A bucket of static vestibular function. Neurology, 72(19), 1689–1692. doi: 10.1212/WNL.0b013e3181a55ecf
   PubMed Web of Science ®Google Scholar