CORE Metadata, citation and similar papers at core.ac.uk Provided by Springer - Publisher Connector Brain Struct Funct (2008) 212:443–463 DOI 10.1007/s00429-007-0170-0 ORIGINAL ARTICLE Human pallidothalamic and cerebellothalamic tracts: anatomical basis for functional stereotactic neurosurgery Marc N. Gallay Æ Daniel Jeanmonod Æ Jian Liu Æ Anne Morel Received: 7 September 2007 / Accepted: 20 December 2007 / Published online: 10 January 2008 Ó The Author(s) 2008 Abstract Anatomical knowledge of the structures to be two tracts in the subthalamic region, (3) the possibility to targeted and of the circuitry involved is crucial in stereo- discriminate between different subthalamic fibre tracts on tactic functional neurosurgery. The present study was the basis of immunohistochemical stainings, (4) correla- undertaken in the context of surgical treatment of motor tions of histologically identified fibre tracts with high- disorders such as essential tremor (ET) and Parkinson’s resolution MRI, and (5) evaluation of the interindividual disease (PD) to precisely determine the course and three- variability of the fibre systems in the subthalamic region. dimensional stereotactic localisation of the cerebellotha- This study should provide an important basis for accurate lamic and pallidothalamic tracts in the human brain. The stereotactic neurosurgical targeting of the subthalamic course of the fibre tracts to the thalamus was traced in the region in motor disorders such as PD and ET. subthalamic region using multiple staining procedures and their entrance into the thalamus determined according to Keywords Basal ganglia Á Thalamus Á Motor disorders Á our atlas of the human thalamus and basal ganglia [Morel Essential tremor Á Parkinson’s disease (2007) Stereotactic atlas of the human thalamus and basal ganglia. Informa Healthcare Inc., New York]. Stereotactic Abbreviations three-dimensional coordinates were determined by sec- ac Anterior commissure tioning thalamic and basal ganglia blocks parallel to al Ansa lenticularis stereotactic planes and, in two cases, by correlation with Acb Accumbens nucleus magnetic resonance images (MRI) from the same brains AChE Acethylcholinesterase prior to sectioning. The major contributions of this study Amg Amygdala are to provide: (1) evidence that the bulks of the cerebel- ap Ansa peduncularis lothalamic and pallidothalamic tracts are clearly separated AV Anteroventral nucleus up to their thalamic entrance, (2) stereotactic maps of the B Basal nucleus of Meynert bic Brachium of the inferior colliculus CaBP Calcium-binding proteins Cd Caudate nucleus M. N. Gallay Á D. Jeanmonod Á J. Liu Á A. Morel (&) CeM Central medial nucleus Laboratory for Functional Neurosurgery, Neurosurgery Clinic, CB Calbindin D-28K University Hospital Zu¨rich, CR Calretinin Sternwartstrasse 6, 8091 Zurich, Switzerland e-mail: [email protected] CL Central lateral nucleus Cl Claustrum Present Address: CM Centre me´dian nucleus J. Liu (or centromedian) Department of Physiology and Pathophysiology, School of Medicine, Xi’an Jiaotong University, 710061 Xian, CTT Cerebellothalamic tractotomy People’s Republic of China fct Fasciculus cerebello-thalamicus 123 444 Brain Struct Funct (2008) 212:443–463 fl Fasciculus lenticularis VLp (d, v, pl) Ventral lateral posterior nucleus (dorsal, frf Fasciculus retroflexus ventral, and paralamellar divisions) ft Fasciculus thalamicus VM Ventral medial nucleus fx Fornix VPI Ventral posterior inferior nucleus GPi Globus pallidus, internal segment VPL (p) Ventral posterior lateral nucleus GPe Globus pallidus, external segment (posterior division) Hip Hippocampus VPM Ventral posterior medial nucleus Hyp Hypothalamus VPMpc Ventral posterior medial nucleus, ic Internal capsule parvocellular division IC Inferior colliculus ZI Zona incerta iml Internal medullary lamina LD Lateral dorsal nucleus LGN Lateral geniculate nucleus Li Limitans nucleus Introduction LP Lateral posterior nucleus M1 Primary motor cortex The surgical treatment of motor disorders such as Parkin- MB Mammillary body son’s disease (PD) and essential tremor (ES) has evolved MD (pc, mc, pl) Mediodorsal nucleus (parvocellular, over the years, targeting alternatively the motor thalamus, magnocellular, and paralamellar the basal ganglia, and more rarely, subthalamic area. The divisions) different approaches are based on extensive knowledge of MGN Medial geniculate nucleus the motor circuitry and of the pathophysiology known from ml Medial lemniscus animal models, such as the MPTP monkey (DeLong 1990; mtt Mammillothalamic tract Obeso et al. 2000; Wichmann and DeLong 2003), and MV Medioventral nucleus peroperative recordings in patients undergoing surgery ot Optic tract (Lenz et al. 1994; Jeanmonod et al. 1996; Lozano et al. PAG Peri-aqueductal gray 1997; Hutchison et al. 1998; Vitek et al. 1998; Magnin pc Posterior commissure et al. 2000, 2001a; Zonenshayn et al. 2000; Garonzik et al. Pf Parafascicular nucleus 2002; Kobayashi et al. 2003). The two major motor path- PF Prefrontal cortex ways involved in PD and ET are illustrated schematically PMc Premotor cortex, caudal part in Fig. 1. Their principal access to the thalamus and thal- PMr Premotor cortex, rostral part amocortical network is through the pallidothalamic and Po Posterior nucleus cerebellothalamic tracts, respectively. The pallidothalamic pre-SMA Pre-supplementary motor area tract is composed of the ansa lenticularis (al) and of the PTT Pallidothalamic tractotomy fasciculus lenticularis (fl, coursing through field H2 of PuA Anterior pulvinar Forel), both take their origin in the internal part of the PuM Medial pulvinar pallidum (GPi). The two fibre tracts merge into the fas- PuT Putamen ciculus thalamicus (ft) (or field H1 of Forel) before PV Parvalbumin entering the thalamus. The cerebellothalamic tract connects R Reticular thalamic nucleus the deep cerebellar nuclei (dentate, interposed, and fastigial RN Red nucleus nuclei) with the thalamus and courses through the superior SC Superior colliculus cerebellar peduncle, decussates, and passes through and SG Suprageniculate nucleus anterior to the red nucleus before reaching the thalamus. sm Stria medullaris The current knowledge on the pallidothalamic and SMA-proper Supplementary motor area cerebellothalamic connections is dominantly derived from SNc Substantia nigra, pars compacta data in monkeys. Degeneration studies and the use of SNr Substantia nigra, pars reticulata modern tracing techniques with multiple anterograde and sPf Subparafascicular nucleus retrograde tracers provided much information about the STh Subthalamic nucleus origin of these fibre tracts and their projections to the stt Spinothalamic tract thalamus and thalamocortical circuits (Nauta and Mehler VA (pc, mc) Ventral anterior nucleus (parvocellular 1966; Carpenter et al. 1976; Asanuma et al. 1983a, b; and magnocellular divisions) Parent and De Bellefeuille 1983; Ilinsky et al. 1985; Per- VLa Ventral lateral anterior nucleus cheron et al. 1993, 1996; Rouiller et al. 1994; Inase and 123 Brain Struct Funct (2008) 212:443–463 445 M1 PMc SMA-proper pre-SMA PMr PFC Cortex VLp VLa VApc Thalamus V.im+D.im VM V.o.(p,a) L.po V.o.m Pontine Nuclei fct ft fl Striatum GPi GPe Cerebellum Cerebellar Cerebellar STh Basal Ganglia cortex nuclei al SNc Fig. 1 Simplified diagram of the cortico-cerebello-thalamocortical primarily to the VLa, VApc, and VM nuclei, with only minor and cortico-basal ganglia-thalamocortical circuitry based on data projections to the VLp (projections to the intralaminar nuclei are not derived from tracing studies in monkeys. The cerebellar nuclei project shown). Equivalent Hassler’s nomenclature (Hassler 1982) for to the motor thalamus via the fasciculus cerebellothalamicus (fct), thalamic nuclei is also indicated. Connections to the thalamus and with primary target in the VLp, but also in VLa and VM (projections cortex are represented with different thicknesses according to their to medial thalamic nuclei are not included in the schema). Efferent relative density and by different gradients in the thalamus. The two connections of the GPi to the thalamus course through the ansa major motor pathways are also represented by different colors for lenticularis (al) and the fasciculus lenticularis (fl), and the two fibre clarity. See list of abbreviations bulks merge to form the fasciculus thalamicus (ft) which projects Tanji 1995; Parent and Hazrati 1995a; Matelli and Luppino thalamocortical system (thalamocortical dysrhythmia, TCD) 1996; Sakai et al. 1996, 2000; Shink et al. 1997; Sidibe following thalamic cells deactivation, in case of ET, or cell et al. 1997; Middleton and Strick 2000; Baron et al. 2001, overinhibition, in case of PD (Magnin et al. 2001a, 2001b; 2006; Francois et al. 2002; Haber 2003; Parent and Parent Aufenberg et al. 2005). This pre-thalamic approach maxi- 2004; Calzavara et al. 2005). Thus, more is known about mizes the disinhibition of the thalamus with a lesion of the the origin and terminations than the exact pathway of those pallidothalamic fibers, that is, at least three times smaller fibres, particularly in the subthalamic region. In the human than the size of a pallidal lesion that would include the sen- brain, the course of the pallidothalamic and cerebellotha- sorimotor and the associative territories (Francois et al. 1994; lamic fibre tracts is still unclear. Indeed the description of Parent and Hazrati 1995a; Gross et al. 1999; Karachi et al. the subthalamic fibre pathways in the human brain dates 2002; Morel et al. 2002). The relevance of the