This monograph on the subthalamic nucleus accentuates in Part I the gap between experimental animal and human information concerning subthalamic development, cytology, topography and connections. The light and electron microscopical cytology concerns the open nucleus concept and the neuronal types present in the STN. The cytochemistry encompasses: enzymes, NO, GRAP, calcium binding proteins, and receptors (dopamine, cannabinoid, piod, glutamate, GABA, serotonin, cholinergic, and calcium channels). The ontogeny of the subthalamic cell cord is reviewed. The topography concerns the rat, cat, baboon and human STN. The descriptions of the connections are also given from a historial point of view. Recent tracer studies on the rat nigro-subthalamic connection revealed contralateral projections

Heida, Tjitske

Lakke, Egbert A.J.F.

Marani, Enrico

Usunoff, Kamen G.

English

Part I. Development, cytology, topography and connections. This monograph on the subthalamic nucleus accentuates in Part I the gap between experimental animal and human information concerning subthalamic development, cytology, topography and connections. The light and electron microscopical cytology concerns the open nucleus concept and the neuronal types present in the STN. The cytochemistry encompasses: enzymes, NO, GRAP, calcium binding proteins, and receptors (dopamine, cannabinoid, piod, glutamate, GABA, serotonin, cholinergic, and calcium channels). The ontogeny of the subthalamic cell cord is reviewed. The topography concerns the rat, cat, baboon and human STN. The descriptions of the connections are also given from a historial point of view. Recent tracer studies on the rat nigro-subthalamic connection revealed contralateral projections

University of Twente Research Information

 Reviews and critical articles covering the entire field of normal anatomy (cytology, histology, cyto- and histochemistry, electron microscopy, macroscopy, experimental morphology and embryology and comparative anatomy) are published in Advances in Anatomy, Embryology and Cell Biology. Papers dealing with anthropology and clinical morphology that aim to encourage cooperation between anatomy and related disciplines will also be accepted. Papers are normally commissioned. Original papers and communications may be submitted and will be considered for publication provided they meet the requirements of a review article and thus fit into the scope of “Advances”. English language is preferred.  It is a fundamental condition that submitted manuscripts have not been and will not simultaneously be submitted or published elsewhere. With the acceptance of a manuscript for publication, the publisher acquires full and exclusive copyright for all languages and countries.  Twenty-five copies of each paper are supplied free of charge.  Manuscripts should be addressed to  Prof. Dr. F.  BECK, Howard Florey Institute, University of Melbourne, Parkville, 3000 Melbourne, Victoria, Australia e-mail: fb22@le.ac.uk  Prof. Dr. F.  CLASCÁ, Department of Anatomy, Histology and Neurobiology, Universidad Autónoma de Madrid, Ave. Arzobispo Morcillo s/n, 28029 Madrid, Spain e-mail: francisco.clasca@uam.es  Prof. Dr. M.  FROTSCHER, Institut für Anatomie und Zellbiologie, Abteilung für Neuroanatomie, Albert-Ludwigs-Universität Freiburg, Albertstr. 17, 79001 Freiburg, Germany e-mail: michael.frotscher@anat.uni-freiburg.de  Prof. Dr. D.E.  HAINES, Ph.D., Department of Anatomy, The University of Mississippi Med. Ctr.,2500 North State Street, Jackson, MS 39216–4505, USA e-mail: dhaines@anatomy.umsmed.edu Prof. Dr. N. HIROKAWA, Department of Cell Biology and Anatomy, University of Tokyo, Hongo 7–3–1, 113-0033 Tokyo, Japane-mail: hirokawa@m.u-tokyo.ac.jpDr. Z. KMIEC, Department of Histology and Immunology, Medical University of Gdansk,Debinki 1, 80-211 Gdansk, Polande-mail: zkmiec@amg.gda.pl Prof. Dr. H.-W.  KORF, Zentrum der Morphologie, Universität Frankfurt, Theodor-Stern Kai 7, 60595 Frankfurt/Main, Germany e-mail: korf@em.uni-frankfurt.de  Prof. Dr. E.  MARANI, Department Biomedical Signal and Systems, University Twente, P.O. Box 217, 7500 AE Enschede, The Netherlands e-mail: e.marani@utwente.nl  Prof. Dr. R.  PUTZ, Anatomische Anstalt der Universität München, Lehrstuhl Anatomie I, Pettenkoferstr. 11, 80336 München, Germany e-mail: reinhard.putz@med.uni-muenchen.de  Prof. Dr. Dr. h.c. Y.  SANO, Department of Anatomy, Kyoto Prefectural University of Medicine, Kawaramachi-Hirokoji, 602 Kyoto, Japan  Prof. Dr. Dr. h.c. T.H.  SCHIEBLER, Anatomisches Institut der Universität, Koellikerstraβe 6, 97070 Würzburg, Germany  Prof. Dr. J.-P.  TIMMERMANS, Department of Veterinary Sciences, University of Antwerpen,Groenenborgerlaan 171, 2020 Antwerpen, Belgiume-mail: jean-pierre.timmermans@ua.ac.be  198  Advances in Anatomy,Embryologyand Cell Biology EditorsF. Beck, Melbourne . F. Clascá, MadridM. Frotscher, Freiburg . D.E. Haines, JacksonN. Hirokawa, Tokyo . Z. Kmiec, GdanskH.-W. Korf, Frankfurt . E. Marani, EnschedeR. Putz, München . Y. Sano, KyotoT.H. Schiebler, WürzburgJ.-P. Timmermans, Antwerpen Enrico Marani, Tjitske Heida, Egbert A.J.F. Lakke, and Kamen G. Usunoff  The Subthalamic Nucleus Part I: Development, Cytology, Topography and ConnectionsWith 29 FiguresISSN 0301-5556ISBN 978-3-540-79459-2 e-ISBN 978-3-540-79460-8Library of Congress Control Number: 2008927199© 2008 Springer-Verlag Berlin HeidelbergThis work is subject to copyright. All rights are reserved, whether the whole or part of the  material is concerned, specifically the rights of translation, reprinting, reuse of illustrations, recitation, b roadcasting reproduction on microfilm or in any other way, and storage in data banks. Duplication of this  publication or parts thereof is permitted only under the provisions of the German Copyright Law of September 9, 1965, in its current version, and permission for use must always be obtained from Springer-Verlag. Violations are liable to prosecution under the German Copyright Law.The use of general descriptive names, registered names, trademarks, etc. in this publication does not imply, even in the absence of a specific statement, that such names are exempt form the relevant protecttive laws and regulations and therefore free for general use.Product liability: The publisher cannot guarantee the accuracy of any information about dosage and appli-cation contained in this book. In every individual case the user must check such information by consulting the relevant literature.Printed on acid-free paper9 8 7 6 5 4 3 2 1springer.comEnrico MaraniTjitske HeidaDepartment of Biomedical Signals and Systems,University of Twente,7500 AE EnschedeThe Netherlandse-mail: e.marani@utwente.nle-mail: t.heida@el.utwente.nlEgbert A.J.F. LakkeDepartment of Neurosurgery,Leiden University Medical Centre,2300 RC LeidenThe NetherlandsKamen G. UsunoffDepartment of Anatomy & Histology,Medical University Sofia,1431 SofiaBulgariae-mail: uzunoff@medfac.acad.bgList of Contents1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .  11.1 Hemiballism . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .  11.2 Early Subthalamic Research . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .  21.3 Ballism and the Subthalamic Nucleus . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .  42 Cytology of the Subthalamic Nucleus  . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .  62.1 Neuronal Types Present in the Subthalamic Nucleus . . . . . . . . . . . . . . . . . . . .  82.2  Ultrastructural Features of Subthalamic Nucleus Terminal Boutons  . . . . . .  112.2.1  Flat Type 1 Boutons . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .  112.2.2  Flat Type 2 Boutons . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .  112.2.3  Small Round Boutons . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .  122.2.4  Large Round Type 1 Boutons . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .  132.2.5  Large Round Type 2 Boutons . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .  132.2.6  Dense Core Vesicle Terminals  . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .  142.2.6.1 The Vesicle-Containing Dendrites of the Interneurons  in the Subthalamic Nucleus  . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .  152.3  Cytochemistry of the Subthalamic Nucleus . . . . . . . . . . . . . . . . . . . . . . . . . . . .  162.3.1  Nitric Oxide  . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .  172.3.2  Glial Fibrillary Acidic Protein  . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .  172.3.3  Ca2+ Binding Proteins  . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .  172.3.4  Receptors in the Subthalamic Nucleus . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .  182.3.4.1  Dopamine Receptors . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .  182.3.4.2  Cannabinoid Receptors . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .  192.3.4.3  Opioid Receptors . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .  192.3.4.4  Glutamate Receptors . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .  202.3.4.5  GABA Receptors . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .  212.3.4.6  Serotonin Receptors . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .  222.3.4.7  Cholinergic Receptors . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .  222.3.5  Ca2+ Channels . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .  232.3.6  Purinergic Modulation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .  243 Ontogeny of the Subthalamic Nucleus . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .  243.1  Development of the Subthalamic Cell Cord . . . . . . . . . . . . . . . . . . . . . . . . . . . .  243.2  Early Development of Subthalamic Connections . . . . . . . . . . . . . . . . . . . . . . .  294  Topography of the Rat, Cat, Baboon and Human Subthalamic Nucleus . . . .  304.1  The Rat Subthalamic Nucleus: Cytoarchitecture . . . . . . . . . . . . . . . . . . . . . . . .  304.2  The Cat Subthalamic Nuclear Area: Sagittal Topographic Borders  . . . . . . . .  324.3  The Baboon Subthalamic Area: Nuclei and Tracts . . . . . . . . . . . . . . . . . . . . . .  344.4  The Human Subthalamic Nucleus: Topography . . . . . . . . . . . . . . . . . . . . . . . .  404.4.1 Nissl Sections . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .  404.4.2  Myelin-Stained Sections . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .  474.5  Ageing of the Human STN . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .  475  Connections of the Subthalamic Nucleus  . . . . . . . . . . . . . . . . . . . . . . . . . . . . .  485.1  Overview of the Mature Connections . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .  485.2  Afferent and Efferent Human Connections . . . . . . . . . . . . . . . . . . . . . . . . . . . .  505.2.1  Cortical Connections . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .  505.2.2  Mirrored Somatotopy in the Subthalamic Nucleus . . . . . . . . . . . . . . . . . . . . . .  565.2.3  Subthalamo-Cortical Connections . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .  575.2.4  The Pallido-Subthalamic Connection . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .  585.2.5  The Pedunculopontine-Subthalamic Interconnections . . . . . . . . . . . . . . . . . .  675.2.6  Pedunculopontine Connections in Man . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .  705.3  Raphe Connections to Subthalamic Nucleus . . . . . . . . . . . . . . . . . . . . . . . . . . .  735.4  The Thalamo-Subthalamic Connections . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .  745.5  The Subthalamic–Central Grey Connections  . . . . . . . . . . . . . . . . . . . . . . . . . .  745.6  The Colliculus Superior Connections . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .  755.7  The Nigro-Subthalamic Connections . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .  756  Nigro-Subthalamic Connections in the Rat  . . . . . . . . . . . . . . . . . . . . . . . . . . .  766.1  Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .  766.2  Materials and Methods . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .  766.2.1  Injections. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .  766.2.2  Tracer Histochemistry . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .  776.3 Results . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .  776.3.1  Tracing Results . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .  776.3.1.1 Appearance of Labelling . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .  776.3.1.2  Course and Termination of Nigrosubthalamic Connections  . . . . . . . . . . . . .  786.3.2  Injections into the SNl . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .  826.3.3   Injections into the SNr  . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .  826.3.4 Injections into the SNc  . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .  836.3.5  Control Injections  . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .  836.4  Discussion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .  857  Appendix 1 . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .  877.1  Description of the Human Pathology Cases Used in this Study . . . . . . . . . . .  878  Appendix 2 . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .  888.1  Häggqvist and/or Nauta-Gygax Staining . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .  888.2  Häggqvist and Klüver-Barrera Staining . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .  898.3  Interpretation of the Staining. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .  89References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .  90Index  . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .  115vi List of Contents Abstract  This monograph (Part I of two volumes) on the subthalamic nucleus (STN) accentuatesthe gap between experimental animal and human information concerning subtha-lamic development, cytology, topography and connections. The light and electron microscopical cytology focuses on the open nucleus concept and the neuronal types present in the STN. The cytochemistry encompasses enzymes, NO, glial fibrillary acidic protein (GFAP), calcium binding proteins, and receptors (dopamine, cannabi-noid, opioid, glutamate, γ-aminobutyric acid (GABA), serotonin, cholinergic, and calcium channels). The ontogeny of the subthalamic cell cord is also reviewed. The topography concerns the rat, cat, baboon and human STN. The descriptions of the connections are also given from a historical point of view. Recent tracer studies on the rat nigro-subthalamic connection revealed contralateral projections. Part II of the two volumes (volume 199) on the subthalamic nucleus (STN) starts with a systemic model of the basal ganglia to evaluate the position of the STN in the direct, indirect and hyperdirect pathways. A summary of in vitro studies is given, describing STN spontaneous activity as well as responses to depolarizing and hyperpolarizing inputs and high-frequency stimulation. STN bursting activity and the underlying ionic mechanisms are investigated. Deep brain stimulation used for symptomatic treatment of Parkinson’s disease is discussed in terms of the elements that are influenced and its hypothesized mechanisms. This part of the monograph explores the pedunculopon-tine–subthalamic connections and summarizes attempts to mimic neurotransmitter actions of the pedunculopontine nucleus in cell cultures and high-frequency stimula-tion on cultured dissociated rat subthalamic neurons. STN cell models – single- and multi-compartment models and system-level models are discussed in relation to subthalamic function and dysfunction. Parts I and II are compared. 

The subthalamic nucleus : Part I: Development, cytology, topography and connections

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