The Claustrum: Structural, Functional, and Clinical Neuroscience

By John R. Smythies and Vilayanur S. Ramachandran

The present day is witnessing an explosion of our understanding of how the brain works at all levels, in which complexity is piled on complexity, and mechanisms of astonishing elegance are being continually discovered. This process is most developed in the major areas of the brain, such as the cortex, thalamus, and striatum. The Claustrum instead focuses on a small, remote, and, until recently, relatively unknown area of the brain. In recent years, researchers have come to believe that the claustrum is concerned with consciousness, a bold hypothesis supported by the claustrum’s two-way connections with nearly every other region of the brain and its seeming involvement with multisensory integrations—the hallmark of consciousness. The claustrum, previously in a humble position at the back of the stage, might in fact be the conductor of the brain’s orchestra.

The Claustrum brings together leading experts on the claustrum from the varied disciplines of neuroscience, providing a state-of-the-art presentation of what is currently known about the claustrum, promising lines of current research (including epigenetics), and projections of new lines of investigation on the horizon.

• Develops a unifying hypothesis about the claustrum’s role in consciousness, as well as the integration of sensory information and other higher brain functions
• Discusses the involvement of the claustrum with autism, schizophrenia, epilepsy, Alzheimer’s disease, and Parkinson’s disease
• Coverage of all aspects of the claustrum, from its evolution and development to promising new lines of research, including epigenetics, provides a platform and point of reference for future investigative efforts

• Language: English
• Publisher: Academic Press
• Release date: Nov 11, 2013
• ISBN: 9780124047228

Book preview

1

History of the Study and Nomenclature of the Claustrum

John Irwin Johnson and Brian A. Fenske,    Department of Radiology, Division of Human Anatomy, Michigan State University, East Lansing, MI, USA

This account of the progress of research on the claustrum considers it in five consecutive historical eras. The first era, 1780 to 1820 was a time of discovery by Vicq d’Azyr of a particular and curious subdivision of the forebrain, and the initial spread of this knowledge. The second era, 1820 to 1870 saw its naming, by Burdach and others, originally with several terms but ending with agreement to call it the claustrum, and its establishment in the neuroanatomical canon. In the third era, 1870 to 1950, new staining technology introduced by Golgi, Nissl, Weigert, and Marchi, and particularly the employment of the first two, by Ramón y Cajal and by Brodmann, allowed some understanding of its distinctive structure and gross anatomical relationships. In the fourth era, 1950 to 2000, an explosion of new techniques brought information about connections and possible functions, exemplified in the work of LeVay and Sherk, delineating the visual region of the claustrum of the cat, and establishing that region as a satellite of visual regions of cerebral cortex. The fifth era, beginning in the year 2000, sees even more radical technical developments, including proteomics and astrocytic analysis, that promise, at last, significant information about what this mysterious brain structure is and does.

Keywords

claustrum; claustrocortical; endopiriform; neurodiversity; extreme capsule

The First Era: 1780–1820

Something New in the Brain: A Product of Revolutions in Science and Society

The history of the study and nomenclature of the claustrum of the mammalian brain begins with the remarkable and revolutionary career of the Frenchman Félix Vicq d’Azyr (see Parent, 2007, for a fascinating account of this spectacular, tragically brief career, and its lasting imprint on biological science and medical education).

Americans will note with interest that this entry into the scientific literature was published in 1786, three years following the recognition of the United States as an independent nation, and three years before the adoption of the equally revolutionary Constitution of the United States of America, distinctively French in its design and principles.

By 1789 the fame of Vicq d’Azyr, through his work in the foundation of comparative biology as a field of study and his applications of this approach to solve important matters of public health, had led to his appointment as physician to Queen Marie Antoinette. Three years later, both he and the queen were dead, but his influence was profound and lives on in many ways, including in our continued attention to the structure we now know as the claustrum.

This young and superbly talented medical student was one of the early enthusiasts who pursued the anatomical study of animals as well as humans, attending lectures on the anatomy of both. He won fame by a series of lectures, on the same topics, which he initiated when he was only 25 years old. Based on these he was awarded his medical degree, and in recognition of their merit was elected to the Academy of Sciences.

He discovered that, by hardening internal tissues in a special fixative, he was able to take thin sections without disrupting the organization of the cells. From these superb sections he proceeded to make exquisite pictures of the internal organs of animals and humans with hitherto unattainably detailed and accurate macroscopic and microscopic views. His depiction of the claustrum showing extended points of it protruding outward into the white matter of the overlying insular gyri can still be viewed today, online, courtesy of the Bibliothèque Interuniversitaire de Santé (see below).

This is prime evidence of the care and accuracy in observation that was employed in the creation of these illustrations. This feature was rarely, if ever, seen in illustrations of claustrum in the subsequent 230 years, but is present in the brains of humans, dolphins, and other large-brained mammals. It has figured in recent speculations about how claustrum achieves its distinctive morphology in different mammalian species (Buchanan and Johnson, 2011).

Even in photographs (Figure 1.1) of sections through llama, dolphin and human brains, it takes careful observation of several adjacent sections to determine the extent and configuration of these gyral core invasions. Their appearance in the illustration by Vicq d’Azyr is much clearer, paradoxically, than in photographs of stained sections. This is a reminder that his illustrations are in fact paintings, although exquisitely accurate paintings. Generations of contemporary medical students know well the advantage of learning from paintings of tissue rather than from photographs or the viewing of actual specimens. The painting isolates and clarifies the spatial relationships through the intrusion of the mind of the painter; however, rather than distorting reality it actually gives a better depiction than the more direct illustrations. Even photographic evidence has lost its advantages now that photo editing can effectively change the depiction of the reality to conform to the abstractions, or many other purposes, of transmitting such views.

Figure 1.1 Invasion of white matter of insular gyri by claustral tissue, as seen in sections through brains of: llama, Lama glama (top); bottlenose dolphin, Tursiops truncatus (center); and human, Homo sapiens (bottom). This feature was depicted in a section of human brain by Vicq d’Azyr (1786) in the first publication that mentioned the existence of the claustrum. The llama section was stained using thionine in the Nissl method to show cell bodies; the dolphin section was stained using iron hematoxylin in the Loyez version of the Weigert method to show myelinated fibers; the human section was stained using cresyl violet in the Nissl method. Llama section is from the Welker Wisconsin Collection; dolphin and human sections are from the Yakovlev-Haleem Collection, all now at the National Library of Health and Medicine, Silver Spring, Md.

At the age of 38, Vicq d’Azyr gathered his superb pictures into a grand compendium, the Traité d’anatomie et de physiologie avec des planches coloriées représentant au naturel les divers organes de l’homme et des animaux [Treatise on anatomy and physiology with plates in color representing, in their natural condition, the diverse organs of men and animals], (Vicq d’Azyr, 1786).

This was the first major reference book in the field that was thereby brought into published existence: comparative biology. The key to the lasting importance of this work is indicated by the term au naturel in the title. Great care was taken in the figures to reproduce what was actually seen in the sections, rather than what might be believed should be in the sections. Such concern was paramount in Vicq d’Azyr’s recommendations, 5 years later, for reforming French medical education so as to base it on data rather than on theory. Although his recommendations were dismissed by the embattled authorities at that turbulent time, they remained available in the form of his published report, and eventually did shape the reform of French medical education into a system that was a world leader for a generation.

Thus it was with the Treatise on anatomy and physiology – its reliance on actual pictures of structures has proved of lasting value. Virtually all contributors to the rest of the history of research on the claustrum, and of many other topics as well, make reference to these illustrations as the first authoritative accounts.

This work contains five remarkable pictures that clearly depict the claustrum and constitute its earliest appearance in the scientific literature. Thanks to the generosity of the Bibliothèque numérique Medic of the Bibliothèque Interuniversitaire de Santé in Paris, readers can view these pictures from one of the few surviving copies. Accessing Volume 2 of the Traité via http://bit.ly/10NIEI8 brings up Plate IX. The illustration has numerical labels; there is no reference to the name claustrum nor to any other name. The structure we now know as the claustrum is labeled ‘28’ on this and subsequent plates.

There are explanatory texts in Volume 1 of the Traité, and the text for Plate IX can be accessed at http://bit.ly/ZqQ7Mz. Paging down from there leads to an explanation for the structure labeled ‘28’, which is identified as follows :

28, 28, 28, ces chiffres indiquent de chaque coté une trace légère de substance corticale placée longitudinalement entre la portion supérieure et externe des stries 26, 26, 27, et le bord interne 6,6,5, des circonvolutions cérébrales qui composent la division postérieure de la scissure de Sylvius. (on page 27)

[28, 28, 28, these figures indicate on each side a light trace of cortical substance placed longitudinally between the superior external portion of the striatum 26, 26, 27, and the internal edge 6, 6, 5, of the cerebral convolutions that make up the posterior division of the fissure of Sylvius.]

Number ‘28’ was as far as Vicq d’Azyr appears to have gone in pursuing the naming of this structure that was new both to science and to the understanding of brain architecture.

With the stabilization of society, after the years of turmoil and disruption stemming from the Revolution, many additional papers by Vicq d’Azyr were collected from their scattered refuges, and several were published at later dates.

Moreau (1805) published a compendium of the writings of Vicq d’Azyr, at least part of which is now generally available as an online publication. In a 2012 reprinting, there is only a brief text followed by 500 pages of explanations of the plates and the incorporated ‘Figures’. No graphic pictures are included. In the explanations, those of Plates IX, X, and XI from the 1786 volumes are included, but are represented as explanations of Plates VII, VIII, and IX. The texts of these explanations are identical to those published in 1786, including the description of the structure labeled ‘28’, which corresponds to the structure now known as the claustrum. There is mention of neither a nucleus taeniaeformis nor any other name, just the description of a trace of cortical substance lying between the striatum and the insular cortical convolutions.

Hippolyte Cloquet organized a series of works, published as jointly authored by Vicq d’Azyr and Cloquet, or vice versa, and finally by Cloquet alone. Four of these have been reprinted in whole or in part, all with the same title, but each with different content, by Nabu press. The third volume in a series entitled Système Anatomique et de Physiologie was apparently started by Vicq d’Azyr but completed by Cloquet (Vicq d’Azyr, 1813a). In addition, A book with the title Traité de l’anatomie du cerveau, and claiming the long-deceased Vicq d’Azyr as sole author, was also published in 1813 (Vicq d’Azyr, 1813b) and was available in an online sale in 2013. The circumstances of its content and publication are obscure. One of these two books may be the source of the date 1813 in many historical timelines for the discovery of the claustrum by Vicq d’Azyr.

Sorting out and analyzing the contents of all of these posthumous publications will entail a major, and worthwhile, effort, but are beyond the scope of this review.

The Second Era: 1820–1870

Naming the Claustrum: And Initiating it into the Canon of the Components of Cerebral Neuroanatomy

The German physiologist Karl Burdach published another grand compendium, this one restricted to the structure and function of the brain. The book appeared in two volumes, published 3 years apart (Burdach, 1819/2012, 1822/2012). This work included copious acknowledgments to the work of Vicq d’Azyr, as well as to that of Reil, Gall, and others. There was a separate section on the claustrum in volume II, which is the earliest text devoted specifically to this structure that the authors have been able to find in current generally available resources, and this text is presented below.

Vormauern

An der äussern Fläche der äussern Capsel, und an Der inner Fläche der Belegungs masse, welche als die Seitenfläche des Stammlappens oder als Insel erscheint, liegt die Vormauer (claustrum)* als eine Shicht grauer Substanz, welche dem Linsenkerne parallel sich erstreckt. Sie ist nämlich 1 Zoll 6 Linien lang; ihre Lage entspricht der Länge nach den Linsenkerne, und sie ist ihm entsprechend in die Länge etwas gekrümt, nach aussen gewölbt, nach innen ausgehölt; so ist sie auch ziemlich von gleicher Höhe mit demsselben. Oben schärft sie sich, wie derselbe, zu; unten breitet sie sich in eine a bis 3 Linien breite Basis auf; so dass sie auf dem senkrechten Querdurchshnitte wie ein aufrecht stehendes Dreyeck erscheint. Hier beugt sie sich aber auch an einer Stelle nach innen um, oder ihre Grundfläche verlängert sich in einen inner Arm, welcher unter dem Linsenkerne, an dem wagerechten Markblatte der äussern Capsul nach innen sich erstreckt. Sie scheint eine zur äussern Capsel gehörige Ganglienmasse zu seyn.

(Burdach, 1822/2012, §. 181)

[On the outer face of the external capsule, and on the inner side of the occupancy mass which appears as the lateral face of the stem or insula, lies the front wall (claustrum)* as a layer of gray substance that stretches along the length of the lentiform nucleus. It is 1 inch and 6 lines [about one-and-a-half-inches] long; its extent equals that of the lentiform nucleus and in that extent it is correspondingly somewhat curved, convex on the outside, concave on the inside; so they are about the same height. At the top it is sharpened; below it widens into a base 3 lines [about a quarter of an inch] wide, such that in coronal section it appears as an upright triangle. But here at one point it is bent inwardly, or its base is extended in an inner arm, which under the lentiform nucleus is extended inward in the horizontal margins of the external capsule. It appears to be a ganglion mass belonging to the external capsule].

The asterisk in Burdach’s text refers to a footnote listing the pictures in Vicq d’Azyr’s, 1786Traité wherein lie each occurrence of the structure numbered 28, indicating that this was indeed the structure he was naming Vormauern and claustrum. So although, as can be seen, Burdach referred to the structure as Vormauern, but included the word claustrum in parentheses and italics, although only on this one occasion. It is possible that this is the introduction of the term claustrum reported by later historians. The Dejerines (Dejerine and Dejerine-Klumpke, 1895) were of the opinion that in this work Burdach was introducing Vormauern as a synonym for claustrum. It seems strange that such an introduction or coinage of two completely new terms would include no mention of the reasons for use of such new terms, nor from whence they came.

The Dejerines also said that Reil (1809) described the gray matter of the forebrain separated by the internal, external, and extreme capsules as caudatus, nucleus lentiformis, and nucleus taeniaeformis. Our reading of this article by Reil found the description of the three capsules but no mention of the word taeniaeformis.

Meanwhile the term Vormauern continued to be in use into the 20th century. Avant-mur is the equivalent term used in French literature, including by the Dejerines in their 1895 great French compendium of neuroanatomy, and its usage has continued in medical school courses in France into the 21st century. The Italian counterpart, antimuro, appears in the Italian literature at least through 1922.

According to previous histories (Edelstein and Denaro, 2004; Meyer, 1971; Olry and Haines, 2001; Rae, 1954), Vicq d’Azyr himself named the structure nucleus taeniaeformis. This may have been done in one or another of his posthumous publications, but we did not find the source containing that information. It was not in the self-published 1786 Traité.

In 1820 Cloquet published a compendium of the works by himself and with Vicq d’Azyr, constituting a major anatomical resource for its age. This attracted admiration and respect such that it was soon translated into English and published, by the redoubtable Robert Knox, in several editions. The edition available to us (Knox, 1831) contains a description of the external and internal anatomy of the cerebrum, with several references to the nomenclature of Vicq d’Azyr on pp. 412 to 426, but it makes no mention of a nucleus taeniaeformis, nor of the claustrum under any other name.

In 1838, one of the many volumes on anatomy published during the 1830s by Friedrich Arnold, the Tabula Anatomica, in Latin, served later authors as a source of official terms. The names are accompanied by anatomical illustrations of the referents for the names. Here we find the designation in the list and in the illustration, N. taeniaeformis s. claustrum. We can see this today thanks to the library of the University of Heidelberg, who, like their counterparts in Paris, have placed online the entire book. These offerings show the wonderful illustrations along with the texts and can be viewed at http://bit.ly/13jCKOT.

The earliest mention of the claustrum that we could find, in a published scientific investigation rather than an anatomical text, was in a review of cerebral morphology by Turner (1866), which was presented at their invitation to the Royal Medical Society in London. His reference was incidental to his main subject, the cerebral convolutions, and he called our subject Arnold’s N. taeniaeformis, indicating that that name was, to some degree, in general use at that time.

The full range of neuroanatomical designations, including N. taeniaeformis, Vormauern, and claustrum is listed in German textbooks through at least 1904 (e.g. Broesike, 1904; Wundt, 1904). The years 1889 through 1895 saw recommendations from the following societies that "claustrum" be the preferred term over all of the synonyms:

 1889 – Report of the Committee of the Association of American Anatomists, adopted unanimously at Philadelphia, December 28.

 1895 – Report of the Committee of the Anatomische Gesellschaft, adopted at Basle.

 1896 – American Neurological Association at Philadelphia, June 5.

(From: Scientific Notes and News, Science, N. S. Vol. IV, No. 81, July 17, 1896)

Meanwhile the next era of research on the claustrum was underway.

The Third Era: 1870–1950

The Chromatic Epiphany: New Stains Show Distinctions Among Major Regions of Brain Tissues, a Major Step Towards Productive Investigations

Our third era commences with the development, in rapid succession, of four new staining methods, around 1873 and 1885. Three of these rapidly became the standard techniques, still in use today, and they bear the names of their inventors. The metallic deposition method of Camillo Golgi was able to show an entire neuronal cell with all of its processes (Golgi, 1873). Thus the morphology of the entire cell could be seen, including the size and shape of the dendrites, and of course the branching pattern of the axon.

Next, Franz Nissl devised a chemical reaction that colored nucleoli and perikarya through reactions with, it was learned much later, RNA molecules clustered in ribosomes. In this way total numbers and densities of cell bodies could be viewed. While the Nissl method was discovered in 1884 and widely used, his first publication of the method did not appear until a decade later (Nissl, 1894).

Carl Weigert, who was working his method during the same time period and at the same location as Nissl, the Städtische Irrenanstalt in Frankfurt-am-Main, published his method of attaching chelated iron to myelin sheaths throughout their cellular extent, allowing views of the extent, length, and grouping of myelinated fibers (Weigert, 1885).

In combination these methods revealed most of what we now know about the fine structure and connectivity of the brain and spinal cord.

Separately each of them reveals a quite different set of features than do the other two, as can be seen in the famous and oft-repeated depiction of layers of cerebral cortex, which can be identified in very different images. Examples can be seen on many websites, including:

 www.benbest.com/science/anatmind/anatmd5.html

 en.wikibooks.org/wiki/Consciousness_Studies/Neuroscience_1

 www.humanneurophysiology.com/cerebralcortex.htm

 www.cixip.com/index.php/page/content/id/1180

(all accessible in June 2013).

Golgi Stain

Golgi stains allow a view of only occasional cells, and the selection process is still unknown. But the cells that are selected are shown in their entirety, including all of the dendrites and often the axon, as well as the cell body. Taking full advantage of these properties, Ramón y Cajal produced an informative, classical series of studies of the architectural arrangement, with beautiful pictures of the shapes of neurons, and much of their connectivity, in most parts of the brain.

One of these stained regions was the claustrum (Ramón y Cajal, 1900, p. 178–183). Meynert (1885, p. 71–75) had asserted that claustrum was the deepest layer of cerebral cortex in the region of the insula, although he recognized that it was not coterminous with the insula, areas of claustrum extending into opercular cortices and even on to the external surface of the hemisphere. These features can be seen in the section of the dolphin brain in our Figure 1.1.

Ramón y Cajal concluded that the claustrum was a not a detached portion of cortex, nor of the corpus striatum, since the size, shape and arrangement of nearly all the neurons in the claustrum were quite distinct from the corresponding features in the neighboring structures: corpus striatum internally and insular cortex externally (Figure 1.2).

Figure 1.2 Depictions of the cell types seen in human cerebral cortex, claustrum, and corpus striatum, revealed by the Golgi stain (in Spanish). Source: Ramón y Cajal (1900). Made available in the public domain in the USA by the Hathi Trust Digital Library.

Striatum and claustrum have, as their majority constituents, sizeable neurons with radiating dendrites thickly covered with dendritic spines, and axons that project out of the nucleus; but the striatum has, in addition, numerous small cells, some with either bushy dendrites or short axons that do not leave the nucleus (or with both). These cells are spaced fairly evenly with no apparent pattern to their arrangement. In cerebral cortex, in sharp distinction, the majority of cells are pyramidal with a single apical dendrite stretching some distance radially from internal to more external levels in the cortex, along with bushes of basal dendrites very close to the cell bodies, all reaching in tangential directions at right angles to the path of the apical dendrites. Furthermore these fields of apical dendrites and cell bodies are arranged in consistent and distinctive laminas, such that the outstanding feature of cortical cytoarchitecture is its pronounced layering.

Nissl Stain

Nissl stains have the advantage that they can be magnified many times to reveal details of cellular organization in gray matter, since all cell bodies are stained. In particular the regular layers of cortex are revealed when considering large populations of cell bodies. For over a decade, Brodmann extensively and carefully studied Nissl stained sections from an amazing variety of mammalian brains, from the collections at the Vogt Institute for Brain Research. From these he produced his system of classification of cortical regions, based on the variations in sizes, shapes, and arrangements of layers of cell bodies in the different regions of cortex (Brodmann, 1909/2006).

In agreement with Meynert’s (1885) original opinion, Brodmann concluded, and stated consistently and frequently, that the claustrum was a subdivision of the sixth layer, the deepest layer of cerebral cortex, that often became separated from the rest of that layer by the passage through the layer of fibers of the extreme capsule. He classified layer 6 in this region as having three sublayers: 6a, 6b, and 6c. Layer 6c was the claustrum, and this additional sublayer, in his view, was the defining feature of insular cortex. Thus in the Brodmann system, the presence of a claustrum meant that the overlying cortex was classified as insular cortex, and this was regardless of whether or not this region of cortex was covered by folded over operculae of neighboring lobes. This scheme led Brockhaus (1940) to propose renaming the functional region known vaguely as insular cortex as instead, claustrocortex, with precise boundaries.

Thus Brodmann and Ramón y Cajal each undertook a detailed study of claustrum, with dramatically different conclusions as to its origins, structure and function. The difference is due entirely to the different staining method used in the preparation of their material.

Although far from being the only one to take up one or another sides of these conflicting arguments, Landau (1919) rendered a powerful array of data in support of Cajal’s conclusion. The argument has resulted in a persistent flow of data and writings, going on in one form or another up to our own time. Many instances are included in this book, and a particularly pertinent recent study, providing a possible consilience of the two opinions, is the work by Mathur et al. (2009) that we discuss at length in our presentation of the fifth era of this history.

Weigert Stain

Weigert stains color only myelin sheathing, and yield little information about cell size, distribution, and number. But the high degree of contrast of the very black myelinated axons against the pale coloring of other tissue, of the Weigert stain, including its many later variations, gives the clearest definition of what we know as white matter. This can be seen in Figure 1.3, which shows in contrast the results of Nissl and Weigert staining, compared with unstained tissue.

Figure 1.3 Comparison of claustrum in sheep (Ovis aries) brain before and after staining. Top: unstained fixed brain – this is a photograph of the block face as sections were being cut from the brain before staining. This is the type of material that would have been available to Vicq d’Azyr, Burdach, Arnold, etc. Center: a section stained using the Nissl method using thionine, which colors ribosomes and renders cell bodies and their distribution visible. Bottom: a section stained by the Sanides-Woelcke-Heidenhain version of the Weigert iron hematoxylin stain (Axer et al., 2003), which colors myelin black, rendering such structures as the internal and external capsules in vivid contrast. Arrows point to the claustrum in each section. Images are from specimens at Neuroscience Associates, Knoxville, TN and from the Welker Wisconsin collection at the National Museum of Health and Medicine in Silver Spring MD.

With the greater contrast of the Weigert stains, they have been the usual choice in illustrating low magnification levels in much more economical monochrome publications, especially in older works (e.g. Dejerine and Dejerine-Klumpke, 1895; Ariëns Kappers, 1920).

Marchi Stain

The fourth stain, again from those remarkable years 1884 and 1885, was that invented by Vittorio Marchi (1886). In this method, osmium tetroxide is attached preferentially to myelin sheaths in the process of Wallerian degeneration. This was the earliest means of tracking the course of axons to their destination and was widely used for 70 years. Bianchi (1922) reported results of experiments done in 1897, a very early study of experimental tract-tracing. His main finding was evidence for connections between claustrum and distant regions of cerebral cortex. While he regarded this as a very tentative conclusion, it has been amply verified by subsequent studies up until our own time.

Combined Techniques

Nissl stains could also reveal information about projections from degeneration of cell bodies following the separation or destruction of their synapses in target regions. Both Marchi and Nissl methods were used in a long series of studies, all showing apparent connections of cells in the claustrum with cerebral cortex (e.g. Berke, 1960; Bianchi, 1922; Mettler, 1935; Narkiewicz, 1964). None, however, owing to the limitations of these techniques, were able to show definitively which cells of the claustrum projected to which cells of the cortex, and vice versa, nor what effects were produced by the connections between these regions.

Proposed Subdivisions of Claustrum and their Nomenclature

Also in this third era of studying just the anatomy of claustrum, subdivisions of claustrum into dorsal and ventral portions were introduced.

The dorsal portion lies superior to a rhinal sulcus (termed the collateral sulcus in humans), which, in general, separates six-layered neocortex from the alternative laminar patterns of allocortex (including those regions known as paleocortex and archicortex). Intermediate laminar patterns have been called mesocortex, and these are in the close vicinity of the rhinal