Textbook on MRI Mapping of the Human Deep Brain

Jean-Jacques LEMAIRE

Description

The full access to the 3D volumetric description of the human deep brain greatly eases the mastering of this complex region. For the first time, the reader has a unique description of numerous structures extracted from high resolution MRI ground-truth, belonging to the thalamus, the hypothalamus, the subthalamus and the telencephalon including the amygdalo-hippocampal complex. The real rendition will matter particularly for all those dealing with the volumetric architecture. A triplanar MRI atlas is included. Several international terminologies allow to seek highly specialized data, making the link between pioneering and seminal works, and current modern usages. The textbook addresses basically the students in neuroscience, whether in biology, medicine, psychology, and in biomedical sciences. Faculties and tenured persons, as well as staffs of industry sectors, should find useful reminders and insights. Those who would like to individualize the analysis of the deep brain will find key elements. Definitively, the textbook is intended to share the knowledge toward inter and trans disciplinary approaches.

Sujets

• Médecine
• Spécialités médicales
• Médecine Générale
• MÉDECINE
• PHARMACIE
• PARAMÉDICAL
• MÉDECINE VÉTÉRINAIRE

Informations

• Publié par: EDP Sciences
• Date de parution: 23 septembre 2021
• Nombre de lectures: 0
• EAN13: 9782759825769
• Langue: Français
• Poids de l'ouvrage: 47 Mo

Extrait

Current Natural Sciences

JeanJacques LEMAIRE

Textbook on MRI Mapping

of the Human Deep Brain

Maps and Extended 3D Analysis

M E D I C I N E

M E D I C I N E

ISBN : 978-2-7598-2575-2

9 782759 825752

Current Natural Sciences

Textbook on MRI Mapping of the Human Deep Brain Maps and Extended 3D Analysis

JeanJacques LEMAIRE

The full access to the 3D volumetric description of the human deep brain greatly eases the mastering of this complex region. For the first time, the reader has a unique description of numerous structures extracted from high resolution MRI groundtruth, belonging to the thalamus, the hypothalamus, the subthalamus and the telencephalon including the amygdalohippocampal complex. The real rendition will matter particularly for all those dealing with the volumetric architecture. A triplanar MRI atlas is included. Several international terminologies allow to seek highly specialized data, making the link between pioneering and seminal works, and current modern usages. The textbook addresses basically the students in neuroscience, whether in biology, medicine, psychology, and in biomedical sciences. Faculties and tenured persons, as well as staffs of industry sectors, should find useful reminders and insights. Those who would like to individualize the analysis of the deep brain will find key elements. Definitively, the textbook is intended to share the knowledge toward inter and trans disciplinary approaches.

JeanJacques LEMAIREPhD), professor of neurosurgery, (MD, is a researcher on Image Guided Therapy at the Institut Pascal (Université Clermont Auvergne, CHU, CNRS, INPClermont, France) upon his return of stays in Boston and Los Angeles. He has advanced experience on MRI brain mapping and image guided procedures, and is one of the pioneers on direct clinical MRI mapping of the deep brain.

www.edpsciences.org

Current Natural Sciences

JeanJacques LEMAIRE

Textbook on MRI Mapping of the Human Deep Brain

Maps and Extended 3D Analysis

All IllustrationsJeanJacques Lemaire

Printed in France

EDP Sciences–ISBN(print): 9782759825752–ISBN(ebook): 9782759825769 DOI: 10.1051/9782759825752

All rights relative to translation, adaptation and reproduction by any means whatsoever are reserved, worldwide. In accordance with the terms of paragraphs 2 and 3 of Article 41 of the French Act dated March 11, 1957,“copies or reproductions reserved strictly for private use and not intended for collective use”and, on the other hand, analyses and short quotations for example or illustrative purposes, are allowed. Otherwise,“any representation or reproduction–whether in full or in part–without the consent of the author or of his successors or assigns, is unlawful”(Article 40, paragraph 1). Any representation or reproduction, by any means whatsoever, will therefore be deemed an infringement of copyright punishable under Articles 425 and following of the French Penal Code.

Science Press, EDP Sciences, 2021

Foreword

We are settling our neuronal nodal network knowledge learned from the visualiza tion of the human brain connectivity. However, the understanding of the integration of deep cerebral structures is still lacking. The visualization of these nodal con nections and hubs of neurons, represent a major challenge for specialized physicians and neuroscientists alike. It is challenging to unveil the less complex networks, such as motor, sensory, auditive and visual. More so to understand the discrete connec tions, we still do not realize the existence, for example, the ones responsible for human cognition. Recognition in the living brain of relays learned during years of exhaustive anatomic dissections, using from the most basic to the most complex laboratory techniques of brain fixation and dissection, is the mission of this textbook. We still have not correlated with the necessary detail what we are having the privilege to seein vivowith images of the living brain. Now, we can see and confirm these relays with exquisite details. These need to be cataloged to be available, not only for the understanding of the brain structure and function but also, most importantly, for guiding neuroscientists and physicians to develop novel strategies to treat neurological diseases, minimizing human suffering. While the cerebral cortex is better mapped during awake surgery, we learned recently that plasticity can modify areas of cortical function. This challenges well established neuroscientists’and physicians’anatomical knowledge. We are realizing, comparing the findings in open surgery, functional images and the old established maps of the cerebral cortex that functional sites are changing dynamically in the brain of an individual. While we are realizing these cortical dynamisms, we know little about these changes in the depth of the brain. Indeed, understanding the deep cluster of cells’functions and their cortical connections still limits what physicians offer to abate patients’suffering and cure diseases. Atlases devised for this purpose exist; however, the correlation of the dis played structures with the most targeted deep brain functional relays to alleviate

DOI: 10.1051/9782759825752.c901 © Science Press, EDP Sciences, 2021

IV

Foreword

symptoms is still being unveiled. Now with tractography, functional imaging and spectroscopy offered by magnetic resonance imaging (MRI), these mysteries of the brain function are at hand to realize. Aided by molecular imaging and optogenetics, our understanding of the human brain function promises to be fertile grounds for years of study. This understanding depends, however, on detailed anatomical knowledge. This Textbook, hinged on exquisite MRI analyses and painstaking segmentation of structures, brings further knowledge of what is necessary to explore the universe of the functionality of deep brain therapeutic targets. Several of which already alleviating symptoms of diseases for which medicine still do not have the cure. Understanding the anatomical boundaries of a cluster of cells, their connections, and their correlation to the established clinical knowledge is the base for the develop ment of novel therapies. Structures related to motor function, easily correlated to symptoms during surgery, are taken as the main indicators of functionality of certain deep brain cluster of cells. The motor relays of the thalamus, pallidum and subthalamus are explored by Professor Lemaire in this compendium, confirming their boundaries, shapes and correlation with the classic ventricular landmarks, which guided the functional neurosurgeon to approach the brain during the last century. They allowed the transfer of the knowledge acquired in the last century to the live images and probabilistic atlases being developed in the two decades of the past century and now. This became possible, thanks to the advent of the computerized images: computed tomography, magnetic resonance imaging and positron emission tomography, all valued Nobel Prizes. The exquisite threedimensional compilation presented by Professor Lemaire in various views enhance the knowledge necessary for interpre tation of the surgical anatomy, indispensable for our interventions based on images for stereotactic surgery, surgical navigation and guided ultrasound surgery. Beyond the motor targets in the depth of the brain, already applicable to the therapy of several motor cerebral disorders, the reader is greeted with the same detailed definition of structures involved in mysteries of endocrine function, cogni tion and behavior, including the hippocampus and the hypothalamus. This gift to science presented in this Atlas represents years of dedication of Prof. Lemaire, which I had the privilege to witness for over a decade, correlating settled knowledge of brain anatomy with the detailed visualization offered by images obtained with high tesla MRI technology, always bringing to the anatomical interpretation his exquisite knowledge of functional neurosurgery, acquired during a lifetime experience treating patients with genetic and neurodegenerative diseases of the brain. This Atlas becomes a classic of human brain anatomy.

Antonio De Salles Professor Emeritus of Neurosurgery and Radiation Oncology University of California Los Angeles, USA Director of NeuroSapiens, São Paulo, Brazil

Preamble

After more than fifteen years of pure direct targeting of the deep brain in stereo tactic functional neurosurgery,i.e.the direct mapping, identification (label and boundary) and targeting of anatomical structures, and considering the amount of knowledge gathered, and the kind requests from students, I have taken the decision to provide this advanced knowledge to all those who are interested in deciphering the architecture of the human brain. i From the first report of pure direct targeting in 1999 , this new path was charted progressively, with the conviction that the basic principle of direct identification of the deep brain architecture would be a significant step in advancing neuroscience and medical applications. Clinical MRI was being developed at the same time as the technique of deep brain stimulation was introduced, with the result that they crossfertilized the concept of direct targeting in my mind. This made it apparent that an atlas of the 3D MRI anatomy of the deep brain would be necessary, allowing the analysis of structural information (i.e.neuroanatomy). Using a high field (4.7 T) MRI research machine, it was possible to obtain high resolutionex vivoimages of the ii deep brain . The inherent challenge was to fix labels and determine boundaries to structures on the basis of patchy anatomic evidence and using nondedicated tools. Finally, it took more than ten years to create an atlas usable for clinical practice, research and teaching, and fully MRI based. It was baptized MDBA, for MRI Deep Brain Atlas. The clinical approach to the atlas creation process required a meticulous checking of anatomic and topographic information, structure by structure, bearing in mind

i Lemaire J.J., Durif F., Boire J.Y., Debilly B., Irthum B., Chazal J. (1999) Direct stereotactic MRI location in the globus pallidus for chronic stimulation in Parkinson’s diseaseActa Neurochir.141, 759.https://doi.org/10.1007/s007010050372. ii Lemaire J.J., Caire F., Bonny J.M., Kemeny J.L., Villéger A., Chazal J. (2004) Contribution of 4.7T MRI in the analysis of MRI anatomy of the human subthalamic area,Acta Neurochir.146, 906 (Abst.).https://doi.org/10.1007/s0070100403019.

DOI: 10.1051/9782759825752.c902 © Science Press, EDP Sciences, 2021

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the potential clinical implications. This work was punctuated by the publication of articles. Finally, deep brain mapping provides an advanced atlas gathering historical data and modern imaging. Obviously, the atlas is composed of maps that can be used for the direct identification of the structures, which is what it was designed for. However, it can also be used by those performing indirect identification of struc tures, as it is also a stereotactic atlas. Neuroscientists should be interested in such data, which are infrequent, and particularly since they are based on clinical practice. This textbook is intended for a wide audience of students and professionals. While compiling it, I noted that known structures are sometimes not so known as thought, talked about or reported. Despite this, it was possible to merge sources, sometimes in oblivion, in an effort to mix several points of view, to clarify the information without oversimplification. Doing so, I pointed to still littleknown areas to suggest new maps of certain regions. Today, recent advances in artificial intelligence have revealed that the automatic identification of brain structures, including the deep brain, may be achievable in the next few decades, and advances will be achieved all the more quickly as the ground truth will be available for learning the machine. Therefore, precise and extended databases, linking several terminologies must be built, and the MDBA could par ticipate in this exciting challenge. In summary, the textbook of MRI mapping of the human deep brain gathers advanced clinical knowledge in neuroanatomy, and historical and pioneering anatomical data which were made available to map the deep brain. Mapping was performed by meticulous manual contouring of more than one hundred structures revealed by high geometric resolution, sub millimetric voxels, using MRI images. The MDBA facilitates the direct identification of structures on MRI and enables 3D understanding of the deep brain architecture. Finally, a specific section of the textbook shows examples of real clinical cases of manual contouring of deep brain structures targeted in functional stereotactic neurosurgery. The textbook provides the means to identify anatomic structures of the deep brain on MRI, both in territories studied anatomically since the first pioneering works, some of which going back to the 19th century, and others still not well studied/explored. Indeed, recognizing the structures that make up the human deep brain is difficult. This is true in medicine and research, even with the most recent MRI machine and computing methods. It should be noted at the outset that the term deep brain is somewhat imprecise. It is an attempt to define a region composed of subcortical, deeply seated, structures, white matter territories and gray nuclei. In practice, the deep brain includes, not exclusively, the thalamus, the prethalamus, the hypothalamus, the lenticular and sub lenticular regions, capsules and lamina, and the mesencephalon, socalled“macrostructures”. Most structures making up these macro structures are little known from clinical and anatomical points of view, first and foremost because they are deeply located and imbricated in a complex manner, hence many are merely ignored, incompletely studied, or unexplored. The following structures are examples among the most wellknown: the subthalamic nucleus, the zona incerta, the ventrocaudal nucleus of the thalamus, the ventromedial nucleus of the hypothalamus, the thalamic fascicle, the brachium conjunctivum, the ansa

Preamble

VII

lenticularis, the substantia innominate, the central tegmental tract and the area of Wernicke. Clinicians or researchers who want to identify structures on MRI must look for fragmented data in books and publications, as well as in free webbased atlases. They must address the difficulty of mastering different sources in a comprehensive and integrated manner. Moreover, reference books are not easy to read because they require advanced knowledge, and some are simply not available in libraries. Fur thermore, there are several nouns that refer to the same, or almost the same, structure,e.g.the thalamic fascicle is also called the thalamic fasciculus, the Forel H1 field, H1, the area tegmentalis H, and Forel’s field H. The same fascicle is also called: area subthalamica tegmentalis and pars dorsomedialis (Neuronames); fasci culus thalamicus and nucleus campi dorsalis [H1] (terminologica anatomica and neuroanatomica); field h1 and the nucleus of the dorsal field of the subthalamus (Foundational Model of Anatomy). On the other hand, free web atlases, which are quite easy to download, are often simplified and sometimes include approximations, notably for structures which have not been frequently and recently studied. Finally, there is no precise and detailed MRI atlas of the deep brain. These difficulties are also hurdles for master’s students in search of a synthetic and comprehensive description of the deep brain, facilitating the analysis of MRI anatomy, while giving links to several nomenclatures. More specifically, the textbook addresses three tricky points regarding the structures of the deep brain.

➢Topography, topology and neighborhood.The topography and topology of the structures of the deep brain are indubitably one of the most difficult 3D anatomic organizations to master in humans. This atlas offers a unique representation in 2D and 3D of structures that greatly facilitate the understanding of the complexity of the brain’s architecture, depicted in a straightforward way. For example, the main routes penetrating the thalamus are easy to explain as soon as you can see its reliefs. ➢Shape and boundary.It is difficult to explain and imagine the shape of deep brain structures, even for simple ones such as the subthalamic nucleus. The meticulous manual contouring of each structure, with submillimetric voxels, according to MRI contrasts and anatomic features, gives very precise real shapes and envelopes. ➢Terminology. As mentioned above, the terminology of deep brain structures is complex and often confusing. The MDBA offers a large sample of names used in clinical practice and also recommended by anatomical ontologies. Regions not extensively mapped or only partially labelled have been revisited and a new ter minology is proposed that merges historical names when available, such as the subthalamic tegmental field, which was subdivided into anterior, central, dorsal, lateral, medial zones and the Forel H field.

People eager to recognize the architecture of the deep brain, both clinicians and neuroscientists, have two main options: they can use the historical method which relies on stereotactic landmarks, or the indirect method following a proportional and probabilistic approach, or they can use the more recent and straightforward method based on the direct recognition of structures on MRI. They both have strengths and weaknesses. The indirect method relies on quite a long history of works and is

VIII

Preamble

efficient in numerous applications; in fact, you do not need to know the precise architectural features of structures, and some are directly visible on the imagery used. For example, if you want to study the putamen of the lenticular nucleus, atlases can confirm or show its location quite precisely, and also it is identifiable on MRI and PetScan. This technique is also relatively well adapted for studying a series of data of different subjects or patients. However, it is difficult to precisely explore structures, for example, the limits of the ventral putamen at the edges of the putamen, the ventral claustrum, caudolenticular gray bridges and innominate substance are complex. In this case, most common knowledge on the topic and atlases are extremely limited. On the other hand, the direct method relies on advanced knowledge of the architectural features of structures, and on the infor mation provided by the most recent imagery used. It is perfectly adapted for the analysis of“difficult”regions and above all gives a unique chance to study individual data. However, it is timeconsuming and demands much more effort to study a series of data. Briefly, the first, historical“indirect”method, developed in the 19th century, relies on stereotactic atlases (e.g.Schaltenbrand & Bailey, Talairach, etc.) and enables identifying a structure according to coordinates. The link between the morphological (anatomohistological) data of atlases (labeled structures) and sub ject (patients or subjects) imageries (projection or slice imagery) is made through stereotactic coordinates. The most widely used stereotactic coordinate system is based on wellknown anatomic beacons, the anterior (AC) and posterior (PC) white commissure, and related geometry landmarks (ACPC line and planes). This is the most widely used technique in the world. You do not have to master deep brain architecture or recognize structures; you look for the structure of interest in your atlas and select the coordinates to obtain probabilistic information on the location of the structure. This is widely used in neurosurgery, and also by the neuroimaging community (e.g.Talairach’s daemon). As more and more specific MRI sequences allow visualizing details thanks to greater geometrical and contrast resolution, teams combine stereotactic coordinates and direct visualization of the architecture; the subthalamic nucleus is very likely the most emblematic example of this mixed approach. Whatever the case, it is still limited to particular structures because they have been targeted for a long time, such as the globus pallidus and the subthalamic nucleus, or they are easily recognizable on MRI images because they are big, like the thalamus, or strongly contrasted, as in the case of striatal structures like the cau date. One must bear in mind that the greater the weight of the indirect method, the more the topographical information is approximated. The direct method is attracting increasing attention with the advances made in MRI acquisition and machines. However, it is still limited by the difficulty of mas tering the deep brain architecture and making the link between the structures observed in images and corresponding to anatomical structures; hence mixed tech niques are largely used and they rely mainly on the indirect method. The novelty of this textbook is that it associates advanced neuroanatomical nomenclatures connected with several classical terminologies and direct MRI car tography, giving an extensive and realistic overview of the deep brain. It also