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The Role of the Thalamus in the Human Subcortical Vestibular System

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The Role of the Thalamus in the Human Subcortical Vestibular System Journal of Vestibular Research 24 (2014) 375–385 375 DOI 10.3233/VES-140534 IOS Press The role of the thalamus in the human subcortical vestibular system Vestibular pathways of the human brainstem to the thalamic nuclei and their functional relevance: Evidence from human lesion- and functional imaging studies Julian Conrada,1,∗, Bernhard Baierb,1 and Marianne Dietericha,c aDepartment of Neurology, German Center for Vertigo and Balance Disorders-IFBLMU , LMU Munich, Germany bDepartment of Neurology, Medical Centre of the Johannes Gutenberg University, Mainz, Germany cMunich Cluster for Systems Neurology, Munich, Germany Received 31 December 2013 Accepted 27 June 2014 Abstract. Most of our knowledge concerning central vestibular pathways is derived from animal studies while evidence of the functional importance and localization of these pathways in humans is less well defined. The termination of these pathways at the thalamic level in humans is even less known. In this review we summarize the findings concerning the central subcortical vestibular pathways in humans and the role of these structures in the central vestibular system with regard to anatomical local- ization and function. Also, we review the role of the thalamus in the pathogenesis of higher order sensory deficits such as spatial neglect, pusher syndrome or thalamic astasia and the correlation of these phenomena with findings of a vestibular tone imbalance at the thalamic level. By highlighting thalamic structures involved in vestibular signal processing and relating the different nomenclatures we hope to provide a base for future studies on thalamic sensory signal processing. Keywords: Medial longitudinal fascicle, ascending tract of Deiters, brachium conjunctivum, ipsilateral vestibulothalamic tract, crossed ventral tegmental tract, vestibular, thalamus, neglect, pusher, astasia Glossary IPL Inferior parietal lobule IVTT Ipsilateral vestibulothalamic tract ATD Ascending tract of Deiters ML Medial lemniscus BC Brachium conjunctivum MLF Medial longitudinal fascicle BOLD Blood oxygen level dependent MRI Magnetic resonance imaging CVTT Crossed ventral tegmental tract MTG Middle temporal gyrus DBS Deep brain stimulation MVN Medial vestibular nucleus FDG-PET Fluordesoxyglucose-Positron- OTR Ocular tilt reaction Emission-Tomography oVemp Ocular vestibular evoked myogenic IFG Inferior frontal gyrus potentials INC Interstitial nucleus of Cajal PCA Posterior cerebral artery INO Internuclear ophthalmoplegia rCBF regional cerebral blood flow rCGM regional cerebral glucose metabolism riMLF Rostral interstitial nucleus of the 1The two first authors contributed equally to the study. medial longitudinal fascicle ∗ Corresponding author: Julian Conrad, Department of Neurology, SCC Semicircular canal Ludwig-Maximilians-University, Marchioninistr. 15, 81377 Mu- nich, Germany. Tel.: +49 4400 77825; Fax: +49 4400 74801; E-mail: SCP Superior cerebellar peduncle [email protected]. SHV Subjective haptic vertical SLF Superior longitudinal fascicle SPV Subjective postural vertical ISSN 0957-4271/14/$27.50 c 2014 – IOS Press and the authors. All rights reserved 376 J. Conrad et al. / The role of the thalamus in the human subcortical vestibular system SVN Superior vestibular nucleus cose metabolism (rCGM) signal and thus correlation of SVV Subjective visual vertical activation/deactivation patterns with anatomical struc- VLBM Voxel based lesion behavior mapping tures in the brainstem and thalamus lacks statistical VN Vestibular nerve power. Furthermore, functional imaging studies reveal For abbreviations of the thalamic nuclei see Fig. 2 all areas that are activated during a task relative to a certain baseline (i.e. correlation) but do not reveal areas that are necessary for a task (i.e. causality) [41,45]. 1. Introduction The role of the thalamus in central vestibular pro- 2. Ascending pathways cessing and the target structures of vestibulothala- mic connections are poorly understood in humans. Five pathways carrying otolith and/or semicircu- Thus, we would like to present an overview of human lar canal signals have been described in animal stud- lesion- and functional imaging studies concerning cen- ies [44,53]. The medial longitudinal fascicle (MLF), tral vestibular processing in the brainstem and specific the ascending tract of Deiters (ATD), the crossed ven- thalamic “vestibular” nuclei and point out implications tral tegmental tract (CVTT), the brachium conjunc- for future research. tivum (BC; superior cerebellar peduncle, SCP) and Most of our knowledge regarding vestibular pro- the ipsilateral vestibulothalamic tract (IVTT). For re- cessing in the brainstem and thalamus is derived from view see Zwergal, A. and co-workers [53] and Pierrot- animal studies in different species. Based on these Deseilligny and colleauges [44]. studies otolith and semicircular canal (SCC) signals As mentioned above most functional imaging stud- are transferred from the inner ear hair cells to the ies focus on cortical vestibular processing due to the vestibular nuclei and enter the medullary brainstem to- lack of high resolution of functional MRI in the brain- gether with the cochlear and facial nerves. Saccular stem. That means that functional imaging which pro- and posterior SCC signals are transmitted via the in- vides information of functionally connected brain ar- ferior branch of the vestibular nerve (VN), and signals eas (i.e. tracts) unfortunately cannot be applied to dif- from the utricle, the anterior and horizontal SCC pass ferentiate the brainstem tracts involved in vestibular by the superior branch of the VN. Usually otolith sig- signal processing. In functional imaging it has been nal encoding neurons have a sensitivity to both angular shown that the thalamus is an integral part of vestibu- acceleration and tilt (i.e. semicircular canal and otolith lar processing but again the exact anatomic location signals) [22] and signals converge in the vestibular nu- of the nuclei involved cannot be investigated with this clei [2]. The nerve fibers divide in an ascending branch method. Thus, most information on the brainstem path- to the superior vestibular nucleus [15] (SVN) and a de- ways in humans to date stems from clinical observa- scending branch to the medial and inferior vestibular tions and lesion studies. nuclei. The different vestibular nuclei are heavily inter- connected. Output of the vestibular nuclei reaches cer- 2.1. Medial longitudinal fascicle (MLF) in humans vical, cerebellar, ocular-motor and eye-head coordina- tion centers or higher order sensory integration struc- The medial longitudinal fascicle is a bilaterally de- tures (for review see Büttner-Ennever et al. [15]). The veloped pathway that interconnects the ocular motor main sources of output are the magnocellular regions nuclei and is well known to transmit vestibular infor- of the medial and superior vestibular nucleus and adja- mation from the vestibular nuclei (mainly MVN and cent dorsal Y group. SVN) to ocular motor nuclei and the midbrain integra- There are several ascending vestibular pathways tion centers (INC, riMLF) to provide eye-head coordi- that have been described in animal studies whereas nation in roll. In a descriptive lesion study Brandt and studies on human vestibulothalamic processing are Dieterich [14] found that lesions of the caudal part of scarce [36]. Only a few lesion and functional imag- the MLF and the VN lead to ipsiversive ocular tilt reac- ing studies concerning this matter are available. While tion (i.e., head tilt, ocular torsion, skew deviation and most lesion studies are descriptive in nature, analy- deviation of the subjective visual vertical (SVV); ipsi- sis of functional imaging data in most cases is lim- lateral eye undermost), while lesions of the rostral pons ited to the poor spatial resolution of the blood oxy- and midbrain (at the site of the oculomotor nuclei, the gen level dependent (BOLD-)/regional cerebral glu- riMLF and the interstitial nucleus of Cajal (INC)) lead J. Conrad et al. / The role of the thalamus in the human subcortical vestibular system 377 to contraversive OTR. Their hypothesis was that this nerve nucleus, the Centre Médian (Ce/CM) nucleus graviceptive pathway is the MLF whose fibers cross in and the Ventrolateral nuclear complex (Vim, Voi/VL) the pontomedullary brainstem. In 36% of their cases, (see Table 1 below for the different nomenclatures of patients exhibited internuclear ophthalmoplegia (INO) thalamic nuclei) of the ipsilateral thalamus. The reason in addition to OTR supporting their hypothesis [14]. In why the contribution of ATD lesions has not been ap- 2008 Zwergal and co-workers examined 120 patients preciated to contribute to vestibular dysfunction in hu- with hemorrhagic or ischemic brainstem stroke [52]. mans might be due to its close proximity to the MLF They found that 98% of the patients with INO due which makes differentiation difficult. to brainstem stroke also had at least one component of contraversive OTR, mostly deviation of SVV but 2.3. Crossed ventral tegmental tract (CVTT) in also skew deviation and ocular torsion in more than humans 50% of the cases. They also observed OTR in patients with “one-and-a-half-syndrome”. Therefore they fig- Evidence of vestibular signals in human CVTT is ured that vestibular (mainly otolith) fibers must be in- rare and restricted to case reports and assumptions cluded in or adjacent to the MLF. It is noteworthy that but no systematic clinical studies have been carried this assumption stems from the clinical
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