Abstract
Based on animal studies, it has been shown that the nucleus ventralis intermedius (VIM) of the thalamus plays an important role within the vestibular system. A few human studies support the vestibular role of the VIM. In this study, we aimed to test the hypothesis whether changing the stimulation status in patients with unilateral deep brain stimulation in the VIM causally modulates the vestibular system, i.e., the graviceptive vertical perception. We tested six tremor patients for tilt of subjective visual vertical (SVV) with unilateral DBS in the VIM (mean age 67 years; mean time since electrode implantation 55 months). The mean tilt of the patients during the stimulator “on” condition was 1.4° to the contraversive side [standard deviation (SD) ± 0.4°] whereas during the “off” period a mean contraversive tilt of 4.4° (SD ± 3.0°) was obtained (p = 0.02). Thus, we were able to show that otolith-dominated graviceptive vertical perception can be directly modulated by changing the status of DBS VIM stimulation, indicating that the VIM is directly involved in (contraversive) vertical perception and its thalamic pathways.
References
Asanuma C, Thach WT, Jones EG (1983) Distribution of cerebellar terminations and their relation to other afferent terminations in the ventral lateral thalamic region of the monkey. Brain Res 286:237–265
Baier B, Bense S, Dieterich M (2008) Are signs of ocular tilt reaction in patients with cerebellar lesions mediated by the dentate nucleus? Brain 131:1445–1454
Baier B, Thömke F, Wilting J, Heinze C, Geber C, Dieterich M (2012a) A pathway in the brainstem for roll-tilt of the subjective visual vertical: evidence from a lesion-behavior mapping study. J Neurosci 32:14854–14858
Baier B, Suchan J, Karnath HO, Dieterich M (2012b) Neural correlates of disturbed perception of verticality. Neurology 78:728–735
Barra J, Marquer A, Joassin R, Reymond C, Metge L, Chauvineau V, Pérennou D (2010) Humans use internal models to construct and update sense of verticality. Brain 133:3552–3563
Behrens TE, Johansen-Berg H, Woolrich MW, Smith SM, Wheeler-Kingshott CA, Boulby PA, Barker GJ, Sillery EL, Sheehan K, Ciccarelli O, Thompson AJ, Brady JM, Matthews PM (2003) Non-invasive mapping of connections between human thalamus and cortex using diffusion imaging. Nat Neurosci 6:750–757
Bense S, Stephan T, Yousry TA, Brandt T, Dieterich M (2001) Multisensory cortical signal increases and decreases during vestibular galvanic stimulation (fMRI). J Neurophysiol 85:886–899
Brandt T, Dieterich M (1994) Vestibular syndromes in the roll plane: topographic diagnosis from brainstem to cortex. Ann Neurol 36:337–347
Büttner U, Henn V (1976) Thalamic unit activity in the alert monkey during natural vestibular stimulation. Brain Res 103:127–132
Ceballos-Baumann AO, Boecker H, Fogel W, Alesch F, Bartenstein P, Conrad B, Diederich N, von Falkenhayn I, Moringlane JR, Schwaiger M, Tronnier VM (2001) Thalamic stimulation for essential tremor activates motor and deactivates vestibular cortex. Neurology 56:1347–1354
Conrad J, Baier B, Dieterich M (2014) The role of the thalamus in the human subcortical vestibular system. J Vest Res 24:375–385
Dieterich M, Brandt T (1993) Thalamic infarctions: differential effects on vestibular function in the roll plane (35 patients). Neurology 43:1732–1740
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
Gauthier L, Dehaut F, Joanette Y (1989) The bells test: a quantitative and qualitative test for visual neglect. Int J Clin Neuropsychol 11:49–54
Hawrylyshyn PA, Rubin AM, Tasker RR, Organ LW, Fredrickson M (1978) Vestibulothalamic projections in man—a sixth primary sensory pathway. J Neurophysiol 41:394–401
Hyam JA, Owen SL, Kringelbach ML, Jenkinson N, Stein JF, Green AL, Aziz TZ (2012) Contrasting connectivity of the ventralis intermedius and ventralis oralis posterior nuclei of the motor thalamus demonstrated by probabilistic tractography. Neurosurgery 70:162–169
Karnath HO, Johannsen L, Broetz D, Küker W (2005) Posteriorthalamic hemorrhage induces ‘‘pusher syndrome’’. Neurology 64:1014–1019
Kirsch V, Keeser D, Hergenroeder T, Erat O, Ertl-Wagner B, Brandt T, Dieterich M (2015) Structural and functional connectivity mapping of the vestibular circuitry from human brainstem to cortex. Brain Struct Funct (Epub ahead of print)
Lopez C, Blanke O (2011) The thalamocortical vestibular system in animals and humans. Brain Res Rev 67:119–146
Marlinski V, McCrea RA (2008) Activity of ventroposterior thalamus neurons during rotation and translation in the horizontal plane in the alert squirrel monkey. J Neurophysiol 99:2533–2545
Meng H, May PJ, Dickman JD, Angelaki DE (2007) Vestibular signals in primate thalamus: properties and origins. J Neurosci 27:13590–13602
Mike A, Balas I, Varga D, Janszky J, Nagy F, Kovacs N (2009) Subjective visual vertical may be altered by bilateral subthalamic deep brain stimulation. Mov Disord 24:1556–1557
Pérennou DA, Mazibrada G, Chauvineau V, Greenwood R, Rothwell J, Gresty MA, Bronstein AM (2008) Lateropulsion, pushing and verticality perception in hemisphere stroke: a causal relationship? Brain 131:2401–2413
Saiki S, Yoshioka A, Yamaha Y et al (2000) Two cases of thalamic infarction presenting with “thalamic astasia”. Rinsho Shinkeigaku 40:383–387
Shiroyama T, Kayahara T, Yasui Y, Nomura J, Nakano K (1999) Projections of the vestibular nuclei to the thalamus in the rat: a Phaseolus vulgaris leucoagglutinin study. J Comp Neurol 407:318–332
Spiegelmann R, Nissim O, Daniels D, Ocherashvilli A, Mardor Y (2006) Stereotactic targeting of the ventrointermediate nucleus of the thalamus by direct visualization with high-field MRI. Stereotact Funct Neurosurg 84:19–23
Tarnutzer AA, Bockisch C, Straumann D, Olasagasti I (2009) Gravity dependence of subjective visual vertical variability. J Neurophysiol 102:1657–1671
Telford R, Vattoth S (2014) MR anatomy of deep brain nuclei with special reference to specific diseases and deep brain stimulation localization. Neuroradiol J 27:29–43
Yardley L (1990) Contribution of somatosensory information to perception of the visual vertical with body tilt and rotating visual field. Percept Psychophys 48:131–134
Acknowledgments
This work was supported by the Deutsche Forschungsgemeinschaft (BA 4097/1-1 to BB) and the BMBF (IFB code 01 EO 0901 to MD).
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B. Baier and T. Vogt contributed equally to the study.
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Baier, B., Vogt, T., Rohde, F. et al. Deep brain stimulation of the nucleus ventralis intermedius: a thalamic site of graviceptive modulation. Brain Struct Funct 222, 645–650 (2017). https://doi.org/10.1007/s00429-015-1157-x
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DOI: https://doi.org/10.1007/s00429-015-1157-x