The Chick Brain in Stereotaxic Coordinates and Alternate Stains: Featuring Neuromeric Divisions and Mammalian Homologies

By Luis Puelles, Margaret Martinez-de-la-Torre, Salvador Martinez and 2 more

This atlas – and its accompanying text - is the most comprehensive work on avian neuroanatomy available so far. It identifies more than 900 hundred structures (versus ca. 250 in previous avian atlases), 180 of them for the first time. It correlates avian and mammalian neuroanatomy on the basis of homologies and applies mammalian terms to homologous avian structures. This is the first atlas that represents the fundamental histogenetic domains of the vertebrate neuroaxis on the basis of sound fate-mapping and gene expression data. This results in a substantial increase in accuracy of delineations. Developmental molecular biologists will find it easier to extrapolate early neural tube patterns into mature structures. The modern trend to shift avian neuroanatomical nomenclature toward mammalian terminology by reference to postulated homologies has been expanded to the entire brain, but is not yet complete. This creates a new standard for comparative cross-reference, which can also be applied to reptilian-mammalian comparisons.

• Color photographs and matching diagrams of 65 coronal, 23 sagittal and 9 horizontal 140 micron-thick sections reacted histochemically for acetylcholinesterase (AChE).
• Thoroughly revised drawings. Updated view of the pallium, including the new concept of homology between the lateral pallium and the mammalian claustro-insular complex.
• Extensive introductory text and bibliography, presenting the background information, methodology and justification of delineations.
• For the first time in any species, this atlas depicts the fate-mapped natural embryonic boundaries in the postnatal brain. For the first time, we present color images of all the 6 histological stains (AChE, Nissl, TH, calbindin, calretinin and parvalbumin) on which delineations are based (accompanying Expert Consult eBook).
• Includes the Expert Consult eBook version, compatible with PC, Mac, and most mobile devices and eReaders, which allows readers to browse, search, and interact with content.
• The eBook also contains annotatable AI files of diagrams for use by researchers.

• Language: English
• Publisher: Academic Press
• Release date: Nov 30, 2018
• ISBN: 9780128160411

Luis Puelles

Dr. Puelles has held various positions teaching human anatomy and conducting research in neuroembryology and comparative neuroanatomy at the Universities of Granada, Sevilla, Badajoz, Cadiz and Murcia in Spain. Since 1983 he has been Full professor of Neuroanatomy at the University of Murcia. He is author of ~230 works, notably the first edition of Chick Brain in Stereotaxic Coordinates, and co-editor of Elsevier’s The Mouse Nervous System.

Book preview

The Chick Brain in Stereotaxic Coordinates and Alternate Stains

Featuring Neuromeric Divisions and Mammalian Homologies

Second Edition

Luis Puelles

Dept. Human Anatomy & Psychobiology, School of Medicine, Univ. of Murcia, Murcia, Spain, [e-mail]

Margaret Martinez-de-la-Torre

Dept. Human Anatomy & Psychobiology, School of Medicine, Univ. of Murcia, Murcia, Spain, [e-mail]

Salvador Martínez

Instituto de Neurociencias de Alicante, School of Medicine, University Miguel Hernández, San Juan (Alicante), Spain, [e-mail]

Charles Watson

The University of Western Australia, Perth, Australia, [e-mail]

George Paxinos

Neuroscience Research Australia and The University of New South Wales, Sydney, Australia, [e-mail]

Table of Contents

Cover image

Title page

Copyright

Dedication

Acknowledgments

Preface to the second edition

New features in the second edition

Key features of both editions

A). Generalities, procedures and background information

B). Rationale for names applied in the atlas

C). Literature cited

D). List of abbreviations

E). Brain structures classified topographically by region

Figures

Coronal sections of the brain

Sagittal sections of the brain

Horizontal sections of the brain

Copyright

Academic Press is an imprint of Elsevier

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First edition 2007

Second edition 2019

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Cover design by Yvette Paxinos

Book design by Lewis Tsalis

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A catalog record for this book is available from the Library of Congress

ISBN: 978-0-12-816040-4

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Dedication

Dedicated to Bengt Källén, R. Glenn Northcutt and Rudolf Nieuwenhuys, bearers of the torch.

Acknowledgments

An uninterrupted series of research grants from the Spanish Ministry of Education and Science to L.P. and S.M. supported since 1980 the comparative embryological and anatomical work that served as a basis for developing this atlas. L.P., and M.M.T. are presently emeritus professors at the University of Murcia and IMIB (Murcia Institute of Biomedical Research). S.M. is professor of Anatomy at the Miguel Hernández School of Medicine and director of the Alicante Institute of Neuroscience. Work on rhombomeres and hindbrain homologies reported herein was supported by an Australian Research Council grant to Paxinos, Watson and Puelles, and an NHMRC grant to Paxinos. We thank Natalie Farra of Elsevier for her strong support of this project.

Preface to the second edition

The decade since the publication of the first edition has benefitted from the harmonization of brain nomenclature of birds and mammals, has seen a significant increase of publications on the avian brain based on molecular markers, and the prosomeric model on which the first edition of this atlas was based has been updated in various aspects touching the regionalization of pallium, subpallium, hypothalamus, pretectum, midbrain, and hindbrain (Ferran et al., 2009; Puelles et al., 2012; Puelles, 2013; Puelles et al., 2013; Puelles, 2014; Puelles and Rubenstein, 2015; Puelles et al., 2016a-c; Puelles et al., 2017; Puelles, 2016, 2017a; Watson et al., 2017). This alone justifies our present offer of a second updated edition with all available color histological material.

New features in the second edition

• Fully revised delineations of the coronal, sagittal and horizontal diagrams and color AChE-stained atlas plates throughout.

• All diagrams and colour TIFF files of all Nissl, AChE, TH, CB, CR, and PV stained material used for the atlas available at the online website (first time).

• Definition by shading of the two hypothalamic prosomeres and indication of the boundary between mesomeres 1 and 2, as well as the hypothalamo-diencephalic and mes-rhombencephalic boundaries.

• Fully revised text includes updates to the prosomeric, pallium, subpallium, hypothalamus, pretectum, midbrain and hindbrain models and literature, including recently discovered avian claustroinsular complex.

Key features of both editions

• 65 coronal sections (diagrams and photographs)

• 23 sagittal sections (diagrams and photographs)

• 9 horizontal sections (diagrams and photographs)

• over 900 structures identified (more than 180 of them new entities, detected on the basis of cross-checked chemoarchitectonic material)

• explicit developmental rationale for morphological classification of items

• tracings of neuromeric forebrain and hindbrain subdivisions

• identification of pallial territories sharing common early molecular determinants in all vertebrates, and particularly in birds and mammals

• adaptation of terminology in many cases to mammalian-homolog names

A)

Generalities, procedures and background information

1. Why this atlas

Avian neuroanatomy has progressed considerably in the last 40 years. This is a result of the advances made possible by a variety of experimental tract-tracing methods (particularly techniques using anterograde or retrograde axonal transport), coupled to stereotaxy, and combined with various histochemical, immunocytochemical, autoradiographic and in situ mRNA hybridization mapping results. There have also been parallel breakthroughs in developmental and physiological knowledge. This overall progress indeed surpasses the level of conceptual analysis and anatomical detail provided in the avian brain atlases used during the last 60 years. The atlases of Van Tienhoven and Juhász (1962), Karten and Hodos (1967), Jungherr (1969), Zweers (1971) and Künzel and Masson (1988) were largely inspired in the classic treatise of Kappers, Huber and Crosby (1936), apart from other important influences (e.g., Edinger, 1898, 1908; Edinger and Wallenberg, 1899; Edinger et al., 1903; Rose, 1914; Craigie, 1935, 1939, 1940; Källén, 1953, 1962; Kuhlenbeck, 1936, 1938, 1939, 1973, 1977; Stingelin, 1958). There is a handful of other less ambitious avian atlases. The recent dove brain atlas of den Boer-Visser, Brittijn and Dubbeldam (2004) offers little morphological update over Karten and Hodos (1967) and Künzel and Masson (1988), though it usefully incorporates some updated terminological aspects.

In the majority of these atlases, the information is offered as interpreted drawings, without corresponding photographs (Karten and Hodos [1967] show photographs, but from a different specimen). This procedure tends to emphasize known aspects over unknown ones. As a consequence, perusal of these atlases seeking straightforward resolution of a new morphological problem - e.g., what lies between this and that? - often leads to dissatisfaction, suspicion of error, or simply lack of data (a blank space in the atlas). One cannot expect an atlas to resolve every question, since knowledge is always imperfect, but we need at least a synthesis of the present state of knowledge and conceptual analysis, in order to serve properly the various demands of the scientific community for a period of time. From this viewpoint, it seemed clear to us that we presently need an updated avian brain atlas based on high quality histological microphotographs.

As regards conceptual background, there are two interacting fields to consider: brain evolution (i.e., comparative neuroanatomy) and development. These domains of research have also progressed significantly during recent decades, as reflected in recent published works covering the field (Nieuwenhuys et al., 1998; Striedter, 2005; Butler and Hodos, 2005; Kaas, 2007; Nieuwenhuys and Puelles, 2016). The Nieuwenhuys et al. (1998) treatise is now the obligatory reference for any novel comparative atlas, as was the treatise of Kappers et al. (1936) for the previous efforts. In this work new ways of thinking are highlighted that still need to be explored thoroughly (see Nieuwenhuys and Puelles, 2016).

In full accordance with these authors, we believe that brain developmental patterns studied comparatively – essentially molecular neural regionalization and brain histogenesis - provide the essential cues for setting anatomical analysis of any vertebrate brain into proper evolutionary perspective; that is, for identifying and qualifying homologies, analogies (homoplasies and parallelisms) and those evolutionary novelties that accompany novel emergent functions.

Chemoarchitecture and hodology represent essential complementary approaches in this task, but we need to remember that they explore tertiary differentiated phenomena in the causal chain under study (1: patterning, 2: histogenesis, 3: differentiation, 4: function), and their importance comes from the link they provide with the quaternary physiological data. Homology relates instead strongly with patterning and histogenetic pattern. Functional analysis, which frequently comes first in our neurobiological curiosity, is clearly several steps removed from the evolutionary and molecular causes of either morphostasis or morphological variation, and should come last into consideration from a morphological perspective (and should never be construed as a basis of morphological analysis, as happened in the past –e.g., Herrick, 1910).

It is now widely accepted that organic evolution essentially progresses via accumulated variation and subsequent selection at the level of animal populations (fitness selection) of changes in the genetically controlled morphogenetic pattern (with occasional intervention of epigenesis). Early neuromorphogenesis, the process by which the fundamental organization of brain structure is established, occurs independently of, and earlier than, axonal navigation, synaptogenesis and any neural function. Consequently, when one asks in what measure avian brains resemble structurally the brains of reptiles or mammals, and, in contrast, what aspects of brain organization are restricted to birds or sauropsids (issues that turn up when deciding on homology and selecting convenient names for these entities), the crucial questions and answers inescapably will have to be couched in developmental rather than hodological or functional terms.

A modern avian brain atlas (in fact, any modern brain atlas), therefore, should illustrate the major natural brain developmental units currently thought to operate within the brain Bauplan of all vertebrates. This should be linked to a consistent terminology which facilitates developmental comparison of relative positions within the Bauplan of brain primordia and corresponding derivatives across vertebrate species. In so doing, there emerges a wholly new emphasis on relative topological position along the dorsoventral and anteroposterior axes of the neural primordium; in other words, an emphasis on topologically characterized natural histogenetic complexes. These encompass the sets of derivatives of any positionally and molecularly well-defined portion of the neuroepithelium, some of which become arranged (stratified) strictly radially in the local neural wall, whereas others eventually may migrate tangentially away. This histogenetic approach supersedes the old habit of identifying adult nuclei as isolated entities among neighboring anatomical elements, or defined relative to arbitrary landmarks (e.g., nucleus x appears at caudal levels through nucleus y) , as if there was no orderly causal pattern in their respective topographic relationships (as potatoes in a potato sack). There is still a large task ahead in comparative neuroanatomy in reformulating the old topographic descriptions into topologic developmental ones, in order to emphasize both the invariant aspects and any essential variance in the structure. Systematic conceptual reference to neuroepithelial origins in an atlas allows correlation with relevant molecular, proliferative and neurogenetic patterns. These patterns guide not only differential appearance of reticular, nuclear and cortical histogenetic patterns, but also the highly specific processes of neuronal migration, axonal navigation and patterned synaptogenesis.

Available developmental knowledge, and in particular the quite advanced recent results of fate mapping studies in the chicken brain (see references below), have clarified much previous uncertainty. Lack of such data was usually the reason adduced earlier for not employing developmental results more intensely in comparative neuroanatomy. This argument may still hold in other vertebrates, but does no longer apply to birds and mammals. Now we know with reasonable precision which are the adult derivatives of most parts of the early avian or mammalian neural tube, and, indeed, there have been major surprises when comparing such conclusions with the classical descriptive expectations. We regard these as landmark results that force a reinterpretation of neuroanatomy. Every neurobiologist should be aware of them.

The vast majority of neural histogenetic areas produce clearly delimited and compact derived domains in the mantle layer, which extend radially from the ventricle to the pial surface. Stratification of derivatives into distinct periventricular, intermediate and superficial strata occurs often. Pronuclei (immature cell masses that later segregate into two or more definitive nuclei) and individual nuclei or specific dispersed neuronal populations reproducibly differentiate at typical locations within these mantle domains, each originated from differentially specified sets of neuroepithelial progenitors and migrating in a stereotyped way to a characteristic position in the neural wall.

These nuclear primordia or cell populations and the related sets of proliferative progenitors are subjected during development to tridimensional morphogenetic deformation, whose varying extent and heterochronous relationships in different vertebrate lineages are part of the intermediate sources of evolutionary diversity and, therefore, need to be known and compared appropriately. Some regions expand in volume considerably, whereas other become compressed. Such morphogenetic events variously lead to the appearance of bulges, constrictions, fissures, fossae and sulci typical of the adult form. The scenario is rendered even more complex by the discovery of an increasing number of cases where neuronal derivatives of one neuroepithelial locus migrate tangentially to adjacent or distant histogenetic domains. This gives rise to the contrast between autoctonous cell populations (which are generated and differentiate locally) and migrated cell populations, which eventually interact functionally with local elements found within the invaded brain centers. Some of these translocations are still poorly investigated, and we do not know how many remain unknown. Present data suggest we can suspect this phenomenon any time the typological diversity within a centre is large and/or includes both excitatory and inhibitory neurons, since such differences apparently require spatially separate specialization of the progenitors. Understanding primary brain structure in terms of radial histogenetic domains and autoctonous cell populations is an obvious prerequisite for the meaningful exploration of tangential neuronal migrations and their eventual integration into local functional circuitry. Radial and tangential migrations also represent a potentially important source of neural evolutionary variation that requires appropriate comparative analysis.

The present atlas consequently aims to identify adult avian brain structures within the radial histogenetic framework that can be deduced from avian neural tube fate-mapping data. These reduce the adult positions and boundaries (the topography) to theoretically invariant (topologic) developmental neurogenetic and cell migration phenomena. This topological analysis still requires cautious extrapolation or reserve in cases where these processes still need to be investigated further (particularly when possible tangential migrations are involved). Our mappings of early histogenetic boundaries in the chick brain are based on fate-mapping experimental data, supplemented with recent chemo- or genoarchitectonic characterization using molecular markers (in good part data obtained in the laboratories of L.P. and S.M.). They should allow the readers to trace the radially related ventricular zone and pial surface for most mature structures across the three planes of section illustrated. This clarifies the stratigraphic neighbourhood relationships within any radial domain, irrespective of the morphogenetic deformations which may have occurred. Adjacent radial domains can then be compared fruitfully (e.g., the periventricular stratum can be compared along a series of adjacent histogenetic domains, noting similarities and differences depending on the spatial dimension explored), or the homologous (the same) radial domain can be cross-examined in another species which displays differential morphogenetic deformations. The radial histogenetic domains postulated here are held to be field homologous one-to-one across most vertebrates, with possible significant exceptions only in Agnatha (Puelles, 1995, 2001a,b; see discussion of field homology in Puelles and Medina, 2002 and Nieuwenhuys and Puelles, 2016). In this way, each cell population identified acquires implicitly a putative developmental context, a feature which should help considerably in comparative analysis. Developmental histogenetic topology was previously investigated by tridimensional or graphic reconstruction (e.g., His, 1893a,b, 1904; Bergquist and Källén, 1954; Kallen, 1951, 1962), as well as by radial-projection analysis of brainstem nuclei maps in various vertebrates, as performed in the nineteen sixties and seventies by R. Nieuwenhuys and colleagues (review in Nieuwenhuys and Puelles, 2016).

Concurrent advances in comparative neurobiology have changed considerably our views on how vertebrate brains relate to one another. These advances have considerably enlarged the list of homologies, and have done away with the need to retain neuroanatomical names assigned in older times to avian brain structures whose homologies were wrongly interpreted, or seem now non-existent. The idea that the avian brain has many fundamental aspects in common with mammalian brains, irrespective of its apparently variant anatomic configuration, is much stronger nowadays than 100 years back. A number of the old names have become very cumbersome, since they clearly imply false homologies, or do not point to the true homologies that have been discovered in the meantime. On the whole, present fate-mapping knowledge confirms that birds have essentially the same pattern of histogenetic parts (natural units) observed in mammals. Although some issues are still under discussion, they evidently have the same brain Bauplan, with one-to-one corresponding radial histogenetic units. This fundamental conclusion logically drives us to search actively among tetrapods and anamniotes for those homologies which are not yet apparent, with concurrent analysis of any apparent species-specific variations. However, it is also quite clear now that some conserved radial histogenetic units have evolved in quite divergent ways in birds and mammals, so that field homologies, rather than point to point homologies, must be defined between sets of particular derivatives, and sometimes we see little similarity between the homologous domains. The telencephalic isocortex, and the claustro-insular and amygdaloid pallial complexes represent the major fields of current debate.

Increasing dissatisfaction with the old nomenclature led shortly before the first version of this atlas came out in 2007 to a proposal of new terms for the avian telencephalon by an international Forum of specialists (Reiner et al., 2004). The aims were to eliminate historic conceptual errors and propose a nomenclature that would come closer to the mammalian one, via updated considerations of homology. However, the latter objective was achieved only in part (only for the basal ganglia), due to persisting disagreements between experts on homology hypotheses and associated research paradigms contemplating the telencephalic pallium. A decades-old developmental conclusion (Smith, 1918/1919; Holmgren, 1925, Kappers, 1947, Kallen, 1962) about the true extent of the sauropsidian pallium was accepted in the new pallial nomenclature. Unfortunately, the convened specialists were divided in an inconciliable way about the relative weight that should be given respectively to hodological and chemoarchitectonic data versus developmental molecular specification data and fate mapping with regard to postulating homology for particular pallial subdivisions. It seems that in order to make coherent these two major lines of recent advance, an important conjecture on the formation of the mammalian cortex and its correspondence with avian pallial primordia that is currently favoured among some avian specialists (e.g., the conception espoused by Karten, 1969; 1997; 2013, 2015) would have to be abandoned. The Forum shied away from what would have been for some a stressful conclusion.

The new list of avian telencephalic names finally offered by the Forum (Reiner et al., 2004) serves the field by eliminating a number of well-known errors in the older names, notably the terms giving the incorrect suffix -striatum to many parts of the pallium, and by approximating the names of avian subpallial components to those of mammalian basal ganglia. However, the impasse reached on alternative homology hypotheses for pallial sectors led to proposal of novel avian-specific supposedly neutral terms for the various parts of the pallium (essentially with meanings reduced to adult topographic position or crude appearance –e.g., the novel terms apical hyperpallium, nidopallium, arcopallium). Such terms were also chosen trying to depart as little as possible from the abbreviations of the old set of names, while indicating the correct ascription to the pallium (e.g., the new term nidopallium was argued to be convenient because it refers vaguely to nested domains characteristic of this area, and it starts with an "n, like the substituted previous term neostriatum"). This feature may be helpful for avian neurobiologists, who are used to the old names and abbreviations, but certainly will not be appreciated by neurobiologists using mainly mammalian terms. The latter would prefer resolved homology questions and consequent application to birds of names inspired in the corresponding mammalian homologues. The Forum new terminology may thus worsen the estrangement of the field of avian neuroanatomy from mammalian neuroanatomy. Moreover, it may mislead naïve readers to believe that the new names represent advances in neuroanatomical knowledge, or even conceptual breakthroughs in avian neuroscience, which is not the case.

We would have preferred homology-based or development-based terms, moderated by caveats where appropriate. Just as the field suffered a delay of 80 years in accepting in its present modified terminology weighty developmental evidence on the definition of what is pallium, there is a risk that we may now have to wait more decades before the present developmental evidence on pallial subdivisions is accepted, thus handicapping scientific progress. However, it seems pointless to fight systematically for homology-based mammalian pallial terms, in the context of a bird-oriented scientific community that has made explicit its current ‘officially undecided’ conceptual status (which just barely hides its support of a suspect conjecture dating to Karten, 1969). Accordingly, we have limited ourselves to brief discussions of problematic issues in the text of the atlas, accompanied by a graphical representation of the pallial and neuromeric developmental units which we think are field-homologous with corresponding mammalian ones on the basis of accumulated developmental evidence. Otherwise we used in the atlas the pallial and subpallial nomenclature of the Forum (Reiner et al., 2004), but adapted it here and there to our needs (sometimes we contemplate more subdivisions than the Forum; details below). In a few cases we proposed alternative terms and abbreviations, in which we emphasized, for instance, the functional character of the relevant structures (e.g., somatosensory, visual, auditory, motor, amygdaloid, etc.), or some developmental characteristic not found in mammals (e.g., ectopic pallidum, referring specifically to a strictly homologous cell population that migrates to a non-radially-corresponding locus inside the avian striatum). At some points we departed from what we considered to be errors of interpretation in the description or classification of structures reported by the Forum (e.g., amygdala). In the second edition we have added current salient ideas about the verifiable existence of a claustro-insular pallial complex in the avian brain. Leaving aside considerations of homology, we thought that readers interested in a bridge with mammalian terms would appreciate this sort of help. In the text below we explain more fully our rationale for names given for each brain part.

Our general position relative to avian and mammalian terms is that whenever there are strong grounds to think that structures are homologous (even if not similar in every aspect), they should be given the mammalian name and abbreviation (attending to avian peculiarities as seems appropriate). This is the approach we have taken for the entire brain, expanding the work already done by the Forum on the avian subpallium and isolated brainstem centers (Reiner et al., 2004). Rarely, cases turned up where one wishes that the avian term (or a reptilian term) be used in mammalian brains, superseding historic mammalian terms that have intrinsic wrong connotations. For example, the mammalian posterior pretectal nucleus turns out not to be pretectal at all, and is developmentally and hodologically comparable to the mesencephalic tectal gray component found just rostral to the optic tectum in all tetrapods. Here we disregarded giving the mammalian name posterior pretectal nucleus to the corresponding avian structure and retained the term tectal gray, which is commonly used in birds, reptiles and amphibia. Tectal gray has recently been introduced in the atlases of the marmoset (Paxinos et al, 2012), rat (Paxinos and Watson, 2014) and mouse (Paxinos and Franklin, in press).

There remain nevertheless many structures whose homology is not clear yet, so that bird-specific names still appear in our atlas. Moreover, work on the atlas, comparing with each other 6 different stains, allowed us to identify hitherto unknown structures (some 200 units), which variously did or did not correspond topographically or chemoarchitectonically to elements mapped in mammalian atlases. We selected in each case appropriate descriptive names. In our effort to approximate as much as presently possible our avian neuroanatomical names and name abbreviations to the mammalian terms, we systematically used the naming and abbreviation rules exemplified by mammalian atlases authored or influenced by G.Paxinos and C.Watson. This occasionally led to ruling out some standard avian abbreviations because they already had a specific meaning in mammalian literature; we had to find ad hoc solutions to resolve these conflicts. An auxiliary criterium was to eschew excessively long abbreviations.

2. On homology criteria

Within cladistic methodology various types of data sets are conceivable for sizing up the possibility of homology, including developmental characters, but some developmental characters are more important than others (Fristrup, 2001; Puelles and Medina, 2002). Early patterning and basic histogenetic phenomena in the neural tube (e.g., timed neurogenesis and molecular differentiation of cell types) are strongly conserved features among vertebrates and even draw importantly on widely conserved genetic regulatory mechanisms evolved previously in invertebrates. We accordingly consider that the weightiest practical parameters for establishing neural homologies are: 1) the relative topology of fate-mapped progenitor neuroepithelial cells within the neural tube wall, correlated whenever possible with 2) the corresponding genetic specification code of regional or cellular identities, and 3) the resulting early histogenetic pattern (proliferation pattern, relative neurogenetic timetable, neuronal migration pattern and stratification), as opposed to 4) hodological properties and late (function-driven) neuronal differentiation markers. The latter are known to represent less conserved or pleotropic variables, and in any case depend on several of the previously mentioned types of variables plus epigenetic interactions.

Historically, comparative neuroscience proceeded in inverse order: early studies were done in adults, heavily weighted by functional assumptions; subsequently came descriptive and experimental embryonic studies, while molecular patterning and experimental causal studies started only recently. Classic efforts in the field already stumbled once due to the simplistic assumption that comparable relative topography and shape (structural similarity) were sufficient to safely deduce homologies (this led to misidentifying a part of pallium as subpallium, just because it bulged into the ventricle). Subsequent morphogenetic, hodological and chemoarchitectonic data revealed previous misconceptions and advanced considerably the field, but led to the still alive and equally simplistic general assumption that hodologic and chemoarchitectonic similarity is necessary and sufficient to establish homology, without addressing embryonic pattern. Nowadays, molecular and experimental developmental data are starting to illuminate the points where the previous generation of comparative scientists may have exceeded the interpretive capacity of their methodological paradigm, as we broach the causal fundament of the homologies.

Though most homologous brain structures do show a number of similarities in chemoarchitecture and hodology, revealing a strong conservatism of neural organization, it is not logically required that homologous structures be overtly similar at all, since they may have varied enormously in the course of evolution, without losing their essential homology relationships in terms of common topologic and morphogenetic origin. Moreover, hodological and chemoarchitectonic differentiation properties of neurons typically result from complex epistatic networks of gene functions. It is often possible to have similar analogous characteristics develop through independent or parallel pathways (e.g., the dopaminergic, cholinergic or gabaergic phenotypes achieved in various parts of the brain). A shared neurotransmitter profile does not make distant cell populations homologous. This qualifies enormously the value of such data, particularly when used in absence of an appropriate topological and causal line of developmental reasoning. The misinformed concept of homology that refers exclusively to entities similar in hodological and chemoarchitectonic properties, irrespective of a coherent developmental context, causes much confusion and leads to unfruitful debates in the contemporaneous field of comparative neuroanatomy. Another persistent source of confusion, although all major neuroanatomists have advised against it, is represented by renewed current attempts to assimilate functional analogy with homology.

Functional