Of Horse-Caterpillars and Homologies: Evolution of the Hippocampus and Its Name.

The hippocampus was first named in mammals based on the appearance of its gross morphological features, one end of it being fancied to resemble the head of a horse and the rest of it a silkworm, or caterpillar. A hippocampus, occupying the most medial part of the telencephalic pallium, has subsequently been identified in diverse nonmammalian taxa, but in which the "horse-caterpillar" morphology is lacking. While some strikingly similar functional similarities have been identified, questions of its homology ("sameness") across these taxa and about the very fundamental relationship of structure to function in central nervous system structures remain open. The hippocampal formation of amniotes participates in allocentric (external landmark) spatial navigation, memory, and attention to novel stimuli, and these functions generally are shared across amniotes despite variation in its morphological features. Substantially greater deviation in its morphology occurs in anamniotes, including amphibians and ray-finned fishes (actinopterygians), but its functions of allocentric spatial navigation and/or memory have been found to be preserved by studies in these taxa. Its shared functional roles cannot be used as evidence of structural homology, but given that other criteria indicate homology of the medial pallial derivative across these clades, the similar functions themselves may be regarded as homologous functions if they are based on the same cellular mechanisms and connections. The question arises as to whether the similar functions are performed by as yet undiscovered, shared morphological features or by different features that accomplish the same results via different mechanisms of neural function.

Hallmarks of consciousness.

Consciousness, ranging from the primary, or perceptual, level to high levels that include a sense of self, can be identified in various organisms by a set of hallmarks that include behavioral, neural and phenomenal and/or informational. Behavioral hallmarks include those that indicate high cognitive abilities, such behavioral flexibility, verbal abilities, episodic memories, theory of mind, object constancy, transitive inference and multistability, all of which have been demonstrated in birds as well as in primates. Neural hallmarks include the thalamocortical model for mammals and similar circuitry in some nonmammalian taxa. Informational hallmarks include sensorimotor awareness, as provided by somatosensory and/or lateral line systems, which may form the basis for the sense of self and distinguishing self from nonself, as well as other sensory information, such as the richness and quantity of color and form information obtained by the visual system. The comparative method reveals a correlation of these different types of hallmarks with each other in their degree of development, which thus may be indicative of the level of consciousness present in a particular species.

Evolution of the amniote pallium and the origins of mammalian neocortex.

Karten's neocortex hypothesis holds that many component cell populations of the sauropsid dorsal ventricular ridge (DVR) are homologous to particular cell populations in layers of auditory and visual tectofugal-recipient neocortex of mammals (i.e., temporal neocortex), as well as to some amygdaloid populations. The claustroamygdalar hypothesis, based on gene expression domains, proposes that mammalian homologues of DVR are found in the claustrum, endopiriform nuclei, and/or pallial amygdala. Because hypotheses of homology need to account for the totality of the evidence, the available data on multiple forebrain features of sauropsids and mammals are reviewed here. While some genetic data are compatible with the claustroamygdalar hypothesis, and developmental (epigenetic) data are indecisive, hodological, morphological, and topographical data favor the neocortex hypothesis and are inconsistent with the claustroamygdalar hypothesis. Detailed studies of gene signaling cascades that establish neuronal cell-type identity in DVR, tectofugal-recipient neocortex, and claustroamygdala will be needed to resolve this debate about the evolution of neocortex.

Evolution of brains, cognition, and consciousness.

Most current hypotheses about the neural basis for consciousness, including higher-level consciousness, are based on mammalian neural features, particularly focusing on thalamocortical circuitry. It is postulated here that since higher-level consciousness is correlated with higher-level cognitive abilities in humans and other mammals, this correlation also holds for nonmammalian taxa; that the level of cognitive ability may be proportional to the level of consciousness; and that the neural basis for both is either the same or highly overlapping. Recent studies, ingeniously designed to be species-sensitive, have revealed a host of highly cognitive abilities in birds, including manifestations of working memory (delayed match-to-sample, episodic memory, transitive inference, and multistability) and category formation, language and numerical comprehension, tool manufacture and cultural transmission of tool design, theory of mind, and Piagetian object permanence to a high level. Comparisons of the neural circuitry reveal extensive similarity in thalamic nuclei and ascending systems to the pallium. However, the avian pallium lacks the laminar architecture and therefore cortical columns of mammals, and avian pallial projection neurons are multipolar rather than specifically pyramidal as in mammals. Neural features common to both mammals and birds, which thus may be crucially involved in the generation of both higher-level cognitive abilities and higher-level consciousness, include large, multipolar, glutamatergic neurons with extensive and densely spiny dendrites, with extensive interconnectedness as well as inter-regional connections, GABAergic inputs from local interneurons, and connections with thalamic nuclei that are regulated by the thalamic reticular nucleus as well as basal ganglia loops.

Mammalian and avian neuroanatomy and the question of consciousness in birds.

Some birds display behavior reminiscent of the sophisticated cognition and higher levels of consciousness usually associated with mammals, including the ability to fashion tools and to learn vocal sequences. It is thus important to ask what neuroanatomical attributes these taxonomic classes have in common and whether there are nevertheless significant differences. While the underlying brain structures of birds and mammals are remarkably similar in many respects, including high brain-body ratios and many aspects of brain circuitry, the architectural arrangements of neurons, particularly in the pallium, show marked dissimilarity. The neural substrate for complex cognitive functions that are associated with higher-level consciousness in mammals and birds alike may thus be based on patterns of circuitry rather than on local architectural constraints. In contrast, the corresponding circuits in reptiles are substantially less elaborated, with some components actually lacking, and in amphibian brains, the major thalamopallial circuits involving sensory relay nuclei are conspicuously absent. On the basis of these criteria, the potential for higher-level consciousness in these taxa appears to be lower than in birds and mammals.

The serial transformation hypothesis of vertebrate origins: comment on "The new head hypothesis revisited".

In "The New Head Hypothesis Revisited," R.G. Northcutt (2005. J Exp Zool (Mol Dev Evol) 304B:274-297) evaluates the original postulates of this hypothesis (Northcutt and Gans, 1983. Quart Rev Biol 58:1-28). One of these postulates is that the brain-particularly the forebrain-evolved at essentially the same time as many neural crest and neurogenic placode derivatives-including sensory ganglia, dermal skeleton and sensory capsules of the head, and branchial arches. Northcutt's subsequent paper in 1996 concluded with the idea that transitional forms might not have occurred at the origin of vertebrates. Butler proposed a "Serial Transformation" hypothesis in 2000, which disputed the latter idea in that paired eyes and an enlarged brain (but lacking telencephalon) were envisioned to have been gained before elaboration of most neural crest and neurogenic placodal derivatives. In 2003, J. Mallatt and J.-Y. Chen analyzed fossils of the Cambrian animal Haikouella, which strongly support its affinity to craniates and aspects of several hypotheses, including Butler's transformational model, because although branchial bars are present, most other neural crest and placodal derivatives are absent, while paired eyes and an enlarged brain (but probably without telencephalon) are present. A more complete picture of vertebrate origins can be realized when the various hypotheses are constructively reconciled.

Evolution of the neural basis of consciousness: a bird-mammal comparison.

The main objective of this essay is to validate some of the principal, currently competing, mammalian consciousness-brain theories by comparing these theories with data on both cognitive abilities and brain organization in birds. Our argument is that, given that multiple complex cognitive functions are correlated with presumed consciousness in mammals, this correlation holds for birds as well. Thus, the neuroanatomical features of the forebrain common to both birds and mammals may be those that are crucial to the generation of both complex cognition and consciousness. The general conclusion is that most of the consciousness-brain theories appear to be valid for the avian brain. Even though some specific homologies are unresolved, most of the critical structures presumed necessary for consciousness in mammalian brains have clear homologues in avian brains. Furthermore, considering the fact that the reptile-bird brain transition shows more structural continuity than the stem amniote-mammalian transition, the line drawn at the origin of mammals for consciousness by several of the theorists seems questionable. An equally important point is that consciousness cannot be ruled out in the absence of complex cognition; it may in fact be the case that consciousness is a necessary prerequisite for complex cognition.

Avian brains and a new understanding of vertebrate brain evolution.

We believe that names have a powerful influence on the experiments we do and the way in which we think. For this reason, and in the light of new evidence about the function and evolution of the vertebrate brain, an international consortium of neuroscientists has reconsidered the traditional, 100-year-old terminology that is used to describe the avian cerebrum. Our current understanding of the avian brain - in particular the neocortex-like cognitive functions of the avian pallium - requires a new terminology that better reflects these functions and the homologies between avian and mammalian brains.

Revised nomenclature for avian telencephalon and some related brainstem nuclei.

The standard nomenclature that has been used for many telencephalic and related brainstem structures in birds is based on flawed assumptions of homology to mammals. In particular, the outdated terminology implies that most of the avian telencephalon is a hypertrophied basal ganglia, when it is now clear that most of the avian telencephalon is neurochemically, hodologically, and functionally comparable to the mammalian neocortex, claustrum, and pallial amygdala (all of which derive from the pallial sector of the developing telencephalon). Recognizing that this promotes misunderstanding of the functional organization of avian brains and their evolutionary relationship to mammalian brains, avian brain specialists began discussions to rectify this problem, culminating in the Avian Brain Nomenclature Forum held at Duke University in July 2002, which approved a new terminology for avian telencephalon and some allied brainstem cell groups. Details of this new terminology are presented here, as is a rationale for each name change and evidence for any homologies implied by the new names. Revisions for the brainstem focused on vocal control, catecholaminergic, cholinergic, and basal ganglia-related nuclei. For example, the Forum recognized that the hypoglossal nucleus had been incorrectly identified as the nucleus intermedius in the Karten and Hodos (1967) pigeon brain atlas, and what was identified as the hypoglossal nucleus in that atlas should instead be called the supraspinal nucleus. The locus ceruleus of this and other avian atlases was noted to consist of a caudal noradrenergic part homologous to the mammalian locus coeruleus and a rostral region corresponding to the mammalian A8 dopaminergic cell group. The midbrain dopaminergic cell group in birds known as the nucleus tegmenti pedunculopontinus pars compacta was recognized as homologous to the mammalian substantia nigra pars compacta and was renamed accordingly; a group of gamma-aminobutyric acid (GABA)ergic neurons at the lateral edge of this region was identified as homologous to the mammalian substantia nigra pars reticulata and was also renamed accordingly. A field of cholinergic neurons in the rostral avian hindbrain was named the nucleus pedunculopontinus tegmenti, whereas the anterior nucleus of the ansa lenticularis in the avian diencephalon was renamed the subthalamic nucleus, both for their evident mammalian homologues. For the basal (i.e., subpallial) telencephalon, the actual parts of the basal ganglia were given names reflecting their now evident homologues. For example, the lobus parolfactorius and paleostriatum augmentatum were acknowledged to make up the dorsal subdivision of the striatal part of the basal ganglia and were renamed as the medial and lateral striatum. The paleostriatum primitivum was recognized as homologous to the mammalian globus pallidus and renamed as such. Additionally, the rostroventral part of what was called the lobus parolfactorius was acknowledged as comparable to the mammalian nucleus accumbens, which, together with the olfactory tubercle, was noted to be part of the ventral striatum in birds. A ventral pallidum, a basal cholinergic cell group, and medial and lateral bed nuclei of the stria terminalis were also recognized. The dorsal (i.e., pallial) telencephalic regions that had been erroneously named to reflect presumed homology to striatal parts of mammalian basal ganglia were renamed as part of the pallium, using prefixes that retain most established abbreviations, to maintain continuity with the outdated nomenclature. We concluded, however, that one-to-one (i.e., discrete) homologies with mammals are still uncertain for most of the telencephalic pallium in birds and thus the new pallial terminology is largely devoid of assumptions of one-to-one homologies with mammals. The sectors of the hyperstriatum composing the Wulst (i.e., the hyperstriatum accessorium intermedium, and dorsale), the hyperstriatum ventrale, the neostriatum, and the archistriatum have been renamed (respectively) the hyperpallium (hypertrophied pallium), the mesopallium (middle pallium), the nidopallium (nest pallium), and the arcopallium (arched pallium). The posterior part of the archistriatum has been renamed the posterior pallial amygdala, the nucleus taeniae recognized as part of the avian amygdala, and a region inferior to the posterior paleostriatum primitivum included as a subpallial part of the avian amygdala. The names of some of the laminae and fiber tracts were also changed to reflect current understanding of the location of pallial and subpallial sectors of the avian telencephalon. Notably, the lamina medularis dorsalis has been renamed the pallial-subpallial lamina. We urge all to use this new terminology, because we believe it will promote better communication among neuroscientists. Further information is available at http://avianbrain.org

The Avian Brain Nomenclature Forum: Terminology for a New Century in Comparative Neuroanatomy.

Many of the assumptions of homology on which the standard nomenclature for the cell groups and fiber tracts of avian brains have been based are in error, and as a result that terminology promotes misunderstanding of the functional organization of avian brains and their evolutionary relationship to mammalian brains. Recognizing this problem, a number of avian brain researchers began an effort to revise the terminology, which culminated in the Avian Brain Nomenclature Forum, held at Duke University from July 18 to 20, 2002. In the new terminology approved at this Forum, the flawed conception that the telencephalon of birds consists nearly entirely of a hypertrophied basal ganglia has been purged from the telencephalic terminology, and the actual parts of the basal ganglia and its brainstem afferent cell groups have been given names reflecting their now evident homologies. The telencephalic regions that were erroneously named to reflect presumed homology to mammalian basal ganglia were renamed as parts of the pallium, using prefixes that retained most established abbreviations (to maintain continuity with the replaced nomenclature). Details of this meeting and its major conclusions are presented in this paper, and the details of the new terminology and its basis are presented in a longer companion paper. We urge all to use this new terminology, because we believe it will promote better communication among neuroscientists.

Clustered phylogenetic distribution of nucleus rostrolateralis among ray-finned fishes.

Nucleus rostrolateralis, which was named for its location in the rostrolateral part of the diencephalon of neopterygian fishes, has been identified in a variety of species based on position, cytoarchitecture, hodology, and/or histochemistry. The phylogenetic distribution of the nucleus is highly sporadic, however. Due to this distribution, nucleus rostrolateralis cannot be regarded as phylogenetically homologous, but it might be an example of syngeny, or generative homology, which applies to characters that have the same genetic and/or developmental basis inherited from a common ancestor, whether or not the character itself has a phylogenetic distribution congruent with a monophyletic taxon--i.e., in general terms, an example of either phylogenetic homology or parallelism. To test whether the nucleus occurs in closely related taxonomic clusters, as might be expected for a character with a shared generative basis, a number of species of cyprinids and atherinomorphs (both teleost taxa) were examined for its presence. Many of the species examined appear to lack the nucleus, but a clustered occurrence of it was found within both taxa. Within cyprinids, nucleus rostrolateralis occurs in all three members examined of the Subfamily Rasborinae. Within atherinomorphs, it occurs in both members examined of the Tribe Poeciliini (of the Subfamily Poeciliinae, Family Poeciliidae) and in the one member examined of the Family Anablepidae. The clustered occurrence of nucleus rostrolateralis supports the hypothesis that it is an example of syngeny. Its postulated shared generative basis appears to derive from the common ancestor of the entire neopterygian radiation despite the rare occurrence of the character itself.

Apparent absence of claustrum in monotremes: implications for forebrain evolution in amniotes.

The claustrum, which comprises the claustrum proper and the endopiriform nucleus, is generally thought to be present in all mammals. Some previous reports of its possible absence in monotremes have appeared in the literature, but the question of its presence or absence in this clade has not been formally addressed. Whether monotremes have a claustrum is of some importance for formulating and evaluating hypotheses relating to the evolution of the structures in the lateral sector of the pallium across amniotes. Archival sets of sections through the brains of the platypus and the short-beaked echidna were examined and included material stained for seven different histochemical and immunohistochemical protocols. No cytoarchitectonically distinct claustrum could be identified in this material for either monotreme. We thus conclude that if monotremes have any cell population that is homolgous to the claustrum of therian mammals, it is entirely cryptic. A claustrum might have been present in ancestral mammals and lost in the monotreme clade, or it might have been gained at the origin of therian mammals. Nonetheless, its absence as a cytoarchitectonically discrete and identifiable structure in monotremes fails to support homology of the claustrum of therian mammals with any single part of the sauropsid pallium.

Neuronal changes during forebrain evolution in amniotes: an evolutionary developmental perspective.

Embryology is the interface of genetic inheritance and phenotypic expression in adult forms, and as such is uniquely positioned to illuminate both. Embryonic cell migration pattern, transient connectivity, axonal growth kinetics and fasciculation patterns can clearly be substantially impacted at the striatocortical junction, which appears to be critical for telencephalic development. Similarly, the big questions concerning pallial evolution in amniotes all involve the pivotal region at the pallial-subpallial boundary, an area where complex developmental cross-currents may be involved in the specification of multiple structures that are thus related to each other. We review some of the positions based on recent genetic data and/or hodology, then suggest that comparative studies of intervening, embryological events may resolve some of the apparent conflicts and illuminate the evolutionary scenario. We propose a new hypothesis, the collopallial field hypothesis, which specifies that the anterior dorsal ventricular ridge of sauropsids and a set of structures in mammals--the lateral neocortex, basolateral amygdalar complex, and claustrum-endopiriform nucleus formation--are homologous to each other as derivatives of a common embryonic field. We propose that in mammals the laterally lying collopallium splits, or differentiates, into deep (claustroamygdalar) and superficial (neocortical) components, whereas in sauropsids, this split does not occur.

The corticostriatal junction: a crucial region for forebrain development and evolution.

Most parts of the brain are conserved across reptiles and birds (sauropsids) and mammals. Two major qualitative differences occur in the upper part, or pallium, of the telencephalon, the most rostral part of the brain. Mammals have a six-layered neocortex and also exhibit a different morphological organization in the lateral half, or sector, of their pallium than do sauropsids. These differences of lateral pallial construction may derive from small but crucial differences in migration patterns of neuronal precursors generated at or above the corner of the lateral ventricle, the corticostriatal junction (CS). Sauropsids have a large structure, the dorsal ventricular ridge, that is proliferated from this region, and its anterior part (ADVR) receives ascending projections from the dorsal thalamus. Mammals have multiple structures in this same region-the lateral part of neocortex, amygdala, and claustrum-endopiriform formation. We propose here that, as the degree of development of structures that form the deeper tier of the pallium varies across the stages of embryology and across phylogeny, mutations may have occurred during evolution at the origin of mammals that had profound consequences for the fate of neural populations generated in the region of the CS and its neighboring pallial germinal zone.

Development and evolution of the collopallium in amniotes: a new hypothesis of field homology.

Embryological development is uniquely positioned to illuminate both hodology in adult brains and its inherited genetic bases. The lateral corner of the lateral ventricle in mammals is a particularly crucial region where cell migration patterns, transiently formed connections, axonal growth kinetics, and fasciculation patterns are complex and interactive. Based on hodology, the sauropsid anterior dorsal ventricular ridge (ADVR) has been proposed as the homologue on a one-to-one basis of the mammalian lateral neocortex (LNC), the basolateral amygdalar complex (BLA), or the claustrum-endopiriform nucleus (CE). Data on gene expression patterns during development have indicated ADVR homology with parts of the latter two structures rather than with LNC. Collothalamic nuclei (the set of dorsal thalamic nuclei that receive their predominant input from the midbrain roof) project to part of BLA and to LNC. Recent findings demonstrate a complex pattern of mutually overlapping but noncongruent gene expression territories and collothalamic projections, which suggests a new, collopallial field hypothesis that the ADVR is homologous as a field to all three structures LNC, BLA, and CE. This hypothesis accounts for current hodological and developmental data as well as for lack of a CE in monotremes and for an abnormal subcortical lamina of gray matter that results from a genetic abnormality in humans.