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DonnaL.Gruol· NoriyukiKoibuchi· MarioManto·
MarcoMolinari· JeremyD. Schmahmann·
YingShenEditors
Essentials
ofCerebellum and
Cerebellar Disorders
APrimer For Graduate Students
SecondEdition
Essentials of Cerebellum and Cerebellar Disorders
Donna L. Gruol • Noriyuki Koibuchi
Mario Manto • Marco Molinari
Jeremy D. Schmahmann • Ying Shen
Editors
Essentials of Cerebellum and
Cerebellar Disorders
A Primer ForGraduate Students
Second Edition
Editors
Donna L. Gruol
Neuroscience Department
The Scripps Research Institute
La Jolla, CA, USA
Noriyuki Koibuchi
Department of Integrative Physiology
Gunma University Graduate School of Medicine
Maebashi, Gunma, Japan
Mario Manto
Service de Neurologie
CHU-Charleroi
Charleroi, Belgium
Jeremy D. Schmahmann
Ataxia Center, Cognitive Behavioral
Neurology Unit, Laboratory for Neuroanatomy
and Cerebellar Neurobiology, Department
of Neurology
Massachusetts General Hospital, Harvard
Medical School
Boston, MA, USA
Marco Molinari
Clinical Translational Research
Santa Lucia Foundation
Rome, Italy
Ying Shen
Department of Physiology
Zhejiang University School of Medicine
Hangzho, China
ISBN 978-3-031-15069-2 ISBN 978-3-031-15070-8 (eBook)
https://doi.org/10.1007/978-3-031-15070-8
© The Editor(s) (if applicable) and The Author(s), under exclusive license to Springer Nature Switzerland AG 2016,
2023
This work is subject to copyright. All rights are solely and exclusively licensed by the Publisher, whether the whole or
part of the material is concerned, specically the rights of translation, reprinting, reuse of illustrations, recitation,
broadcasting, reproduction on microlms or in any other physical way, and transmission or information storage and
retrieval, electronic adaptation, computer software, or by similar or dissimilar methodology now known or hereafter
developed.
The use of general descriptive names, registered names, trademarks, service marks, etc. in this publication does not
imply, even in the absence of a specic statement, that such names are exempt from the relevant protective laws and
regulations and therefore free for general use.
The publisher, the authors, and the editors are safe to assume that the advice and information in this book are believed
to be true and accurate at the date of publication. Neither the publisher nor the authors or the editors give a warranty,
expressed or implied, with respect to the material contained herein or for any errors or omissions that may have been
made. The publisher remains neutral with regard to jurisdictional claims in published maps and institutional afliations.
This Springer imprint is published by the registered company Springer Nature Switzerland AG
The registered company address is: Gewerbestrasse 11, 6330 Cham, Switzerland
Contents
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1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1
Donna L. Gruol, Noriyuki Koibuchi, Mario Manto, Marco Molinari,
Jeremy D. Schmahmann, and Ying Shen
Part I Brief Historical Note
2 A Brief History of the Cerebellum. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5
Jeremy D. Schmahmann
3 Pivotal Insights: The Contributions of Gordon Holmes (1876–1965)
and Olof Larsell (1886–1964) to Our Understanding
of Cerebellar Function and Structure . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 15
Duane E. Haines
Part II Anatomy and Histology of the Cerebellum
4 Gross Anatomy of the Cerebellum . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 23
Jan Voogd and Enrico Marani
5 Vascular Supply and Territories of the Cerebellum . . . . . . . . . . . . . . . . . . . . . . . . 29
Qiaoshu Wang and Louis R. Caplan
6 The Olivocerebellar Tract . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 41
Yuanjun Luo and Izumi Sugihara
7 Precerebellar Nuclei: Embryological Principles . . . . . . . . . . . . . . . . . . . . . . . . . . . 47
Mayumi Yamada and Mikio Hoshino
8 Vestibular Nuclei and Their Cerebellar Connections . . . . . . . . . . . . . . . . . . . . . . . 51
Neal H. Barmack
9 Spinocerebellar and Cerebellospinal Pathways . . . . . . . . . . . . . . . . . . . . . . . . . . . . 61
Tom J. H. Ruigrok
10 Visual Circuits . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 69
Manuel Jan Roth, Axel Lindner, and Peter Thier
11 The Cerebrocerebellar System . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 77
Jeremy D. Schmahmann
12 Cerebello-Cerebral Feedback Projections . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 87
Kim van Dun, Mario Manto, and Peter Mariën
Part III Embryology and Development of the Cerebellum
13 Cerebellar Neurogenesis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 93
Richard Hawkes and G. Giacomo Consalez
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14 Zones and Stripes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 99
Carol Armstrong and Richard Hawkes
15 Specification of Cerebellar Neurons . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 107
Satoshi Miyashita and Mikio Hoshino
16 Cerebellar Nucleus Development. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 111
Hong-Ting Kwok and Richard J. T. Wingate
17 Development of Glutamatergic and GABAergic Synapses . . . . . . . . . . . . . . . . . . . 115
Marco Sassoè-Pognetto
18 Synaptogenesis and Synapse Elimination in Developing Cerebellum . . . . . . . . . . 121
Kouichi Hashimoto, Masahiko Watanabe, and Masanobu Kano
19 Cerebellar Epigenetics: Transcription of microRNAs in Purkinje
Neurons as an Approach to Neuronal Plasticity . . . . . . . . . . . . . . . . . . . . . . . . . . . . 127
Neal H. Barmack
20 The Genetic Programs Behind Cerebellar Development . . . . . . . . . . . . . . . . . . . . 137
Kathleen J. Millen
Part IV Cerebellar Circuits: Biochemistry, Neurotransmitters
and Neuromodulation
Contents
21 Granule Cells and Parallel Fibers . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 149
Egidio D’Angelo
22 Purkinje Cells . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 155
Théo Rossi and Philippe Isope
23 Stellate Cells . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 163
Siqiong June Liu and Christophe J. Dubois
24 Basket Cells . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 169
Masahiko Watanabe
25 Golgi Neurons . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 173
Stéphane Dieudonné
26 Lugaro Cells. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 177
Moritoshi Hirono
27 Unipolar Brush Cells . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 181
Marco Martina and Gabriella Sekerková
28 Glial Cells . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 187
Katharine L. Dobson and Tomas C. Bellamy
29 GABA Pathways and Receptors . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 191
Tomoo Hirano and Shin-ya Kawaguchi
30 Glutamatergic Pathways and Receptors . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 197
Susumu Tomita
31 Norepinephrine in the Cerebellum . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 201
Haven K. Predale, Daniel J. Chandler, and Barry D. Waterhouse
32 Serotonin in the Cerebellum . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 209
Johannes A. van Hooft and Marlies Oostland
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33 Nitric Oxide . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 215
Sho Kakizawa
34 Cannabinoids . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 221
Gary J. Stephens
35 Purinergic Signaling in the Cerebellum . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 225
Mark J. Wall
36 Neuropeptides in the Cerebellum . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 231
Georgia A. Bishop and James S. King
37 Neuroactive Steroids . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 237
C. Fernando Valenzuela and Samantha Varela
38 Role of Unipolar Brush Cells in the Vestibulocerebellum . . . . . . . . . . . . . . . . . . . . 243
Rachel N. Koops, Cathrin B. Canto, Bin Wu, Martijn Schonewille,
Beerend H. J. Winkelman, and Chris I. De Zeeuw
39 Distributed Plasticity in the Cerebellar Circuit . . . . . . . . . . . . . . . . . . . . . . . . . . . .259
Egidio D’Angelo
Part V Basic Physiology
40 Simple Spikes and Complex Spikes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 265
Thomas S. Otis
41 Rebound Depolarizations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 269
Steven Dykstra and Ray W. Turner
42 Cerebellar Nuclei. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 275
Dieter Jaeger and Huo Lu
43 Plasticity of the Cerebellum . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .281
Xin-Tai Wang and Ying Shen
44 Long-Term Depression at Parallel Fiber–Purkinje Cell Synapses . . . . . . . . . . . . . 287
Michisuke Yuzaki
45 Regulation of Calcium in the Cerebellum. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 293
Donna L. Gruol
46 Neurotrophic Factors in Cerebellar Development and Function . . . . . . . . . . . . . . 299
Juan Pablo Zanin and Wilma J. Friedman
47 The Cerebellar Neuroimmune System . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 305
Donna L. Gruol
48 Restoring a Loss of Mossy Fiber Plasticity in a Model
of Fragile X Syndrome . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 313
Xiaoqin Zhan and Ray W. Turner
Part VI Neuroimaging of the Cerebellum
49 Cerebellar Closed Loops . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 321
Christophe Habas
50 MRI Aspects: Conventional, SWI, and DTI . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 325
Thomas M. Ernst, Andreas Deistung, Marc Schlamann,
and Dagmar Timmann
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51 SPECT and PET . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 333
Martina Minnerop
52 MR Spectroscopy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 339
Vladimír Mlynárik
53 Functional Topography of the Human Cerebellum . . . . . . . . . . . . . . . . . . . . . . . . . 343
Catherine J. Stoodley and Jeremy D. Schmahmann
54 fMRI-Based Anatomy: Mapping the Cerebellum . . . . . . . . . . . . . . . . . . . . . . . . . . 351
Xavier Guell and Jeremy D. Schmahmann
Part VII Functional Properties of the Cerebellum
55 Cerebro-Cerebellar Networks . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 359
Iolanda Pisotta and Marco Molinari
56 Clinical Functional Topography in Cognition . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 363
Maria Leggio
57 Sequencing . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 371
Marco Molinari
58 Speech and Language . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 375
Peter Mariën and Kim van Dun
Contents
59 Theory of Mind and Cerebellum . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 379
Giusy Olivito, Libera Siciliano, and Maria Leggio
60 Cerebellum and Decision-Making . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 387
Ben Deverett and Marlies Oostland
Part VIII Cellular and Animal Models of Cerebellar Disorders
61 The Zebrafish Cerebellum . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 393
Jan Kaslin and Michael Brand
62 The Teleost Fish . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 399
Takanori Ikenaga
63 Lurcher Mouse . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 403
Jan Cendelin, Jan Tuma, and Zdenka Purkartova
64 The Tottering Mouse . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 409
Russell E. Carter and Timothy J. Ebner
65 The Rolling Nagoya Mouse . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 413
Jaap J. Plomp, Arn M. J. M. van den Maagdenberg, and Else A. Tolner
66 Lesions of the Cerebellum . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 419
Maria Teresa Viscomi and Marco Molinari
67 The Staggerer Mouse: RORα Deficiency Induces
Cerebellar Neurodegeneration . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 425
Natalie Morellini, Ann M. Lohof, Jean Mariani, and Rachel M. Sherrard
68 Alcohol and the Cerebellum . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 431
David J. Rossi
69 Moonwalker Mouse . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 441
Mohamed F. Ibrahim and Esther B. E. Becker
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Part IX Human Cerebellar Symptoms: From Movement to Cognition
70 Cerebellum and Oculomotor Deficits . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 451
Olwen Murphy and Amir Kheradmand
71 Speech Disorders . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 457
Maria Caterina Silveri
72 Deficits of Limbs Movements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 463
Giuliana Grimaldi
73 The Three Cornerstones of the Cerebellar Syndrome . . . . . . . . . . . . . . . . . . . . . . . 469
Pierre Cabaraux and Mario Manto
74 Lesion-Symptom Mapping . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 479
Dagmar Timmann, Thomas M. Ernst, Winfried Ilg, and Opher Donchin
75 The Cerebellar Cognitive Affective Syndrome
and the Neuropsychiatry of the Cerebellum . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 485
Jeremy D. Schmahmann
76 Ataxia Scales for the Clinical Evaluation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 493
Katrin Bürk
77 The Ataxic Gait . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 501
Pierre Cabaraux and Mario Manto
78 The Social Cerebellum and Human Interactions . . . . . . . . . . . . . . . . . . . . . . . . . . . 511
Elien Heleven and Frank Van Overwalle
Part X Human Cerebellar Disorders: From Prenatal Period to Elderly
79 Genetics and Differential Diagnosis of Cerebellar Ataxias . . . . . . . . . . . . . . . . . . . 521
Francesc Palau and Javier Arpa
80 Overview of Ataxia in Childhood . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 531
Eugen Boltshauser
81 Cerebellar Pathology in Autism . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 537
S. Hossein Fatemi and Justin W. Aman
82 Cerebellar Pathology in Schizophrenia, Bipolar Disorder,
and Major Depression . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .541
S. Hossein Fatemi and Justin W. Aman
83 Autosomal Recessive Ataxias . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 547
Marie Beaudin, Ikhlass Haj Salem, and Nicolas Dupré
84 X-Linked Ataxias . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 555
Josef Finsterer
85 Imaging of Malformations of the Hindbrain and Craniocervical Junction . . . . . 561
Christian Herweh
86 Cerebellar Stroke . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 567
Keun-Hwa Jung and Jae-Kyu Roh
87 Immune-Mediated Cerebellar Ataxias . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 575
Marios Hadjivassiliou and Hiroshi Mitoma
88 Paraneoplastic Cerebellar Syndrome . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 583
Raffaele Iorio and Lucia Campetella
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89 Essential Tremor . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 595
Elan D. Louis
90 Toxic Agents . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 599
Alexandra Bakolas and Mario Manto
91 Endocrine Disorders . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 607
Mario Manto and Christiane S. Hampe
92 Friedreich Ataxia. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 617
Mario Manto
93 Ataxia Telangiectasia . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 621
Rob A. Dineen and William P. Whitehouse
94 Neuroimmune Mechanisms of Cerebellar Ataxias . . . . . . . . . . . . . . . . . . . . . . . . .631
Hiroshi Mitoma and Mario Manto
95 Primary Autoimmune Cerebellar Ataxia (PACA) . . . . . . . . . . . . . . . . . . . . . . . . . . 641
Marios Hadjivassiliou and Hiroshi Mitoma
96 Gluten Ataxia . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 645
Marios Hadjivassiliou
97 Cerebrotendinous Xanthomatosis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 649
Evelien Hendriks, Bianca M. L. Stelten, and Aad Verrips
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98 Cerebellar Variant of Multiple System Atrophy (MSA-C) . . . . . . . . . . . . . . . . . . . 655
Marios Hadjivassiliou
99 Cerebellar Tumors . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 659
Thomas Beez
100 Post-traumatic Cerebellar Syndromes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 665
Jordi Gandini and Mario Manto
101 Superficial Siderosis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 671
Hiroyuki Katoh and Masahiko Watanabe
102 Ataxia in Multiple Sclerosis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 679
Giacomo Koch and Danny Adrian Spampinato
103 CANVAS . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 685
Mario Manto and Joao Lemos
104 Spastic Paraplegia Type 7 (SPG7) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 691
Gorka Fernández-Eulate, Aurora Pujol, and Adolfo López de Munain
Part XI Therapies of Cerebellar Ataxias
105 Drugs in Selected Ataxias . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .699
Dagmar Timmann and Winfried Ilg
106 Cerebellar Stimulation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 705
Giuliana Grimaldi
107 Motor Rehabilitation of Cerebellar Disorders . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 709
Winfried Ilg and Dagmar Timmann
108 Editing the Genome . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 715
Jordi Gandini and Mario Manto
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