Thoughts on the development, structure and evolution of the mammalian and avian telencephalic pallium

Various lines of evidence suggest that the development and evolution of the mammalian isocortex cannot be easily explained without an understanding of correlative changes in surrounding areas of the telencephalic pallium and subpallium. These are close neighbours in a common morphogenetic field and are postulated as sources of some cortical neuron types (and even of whole cortical areas). There is equal need to explain relevant developmental evolutionary changes in the dorsal thalamus, the major source of afferent inputs to the telencephalon (to both the pallium and subpallium). The mammalian isocortex evolved within an initially small dorsal part of the pallium of vertebrates, surrounded by other pallial parts, including some with a non-cortical, nuclear structure. Nuclear pallial elements are markedly voluminous in reptiles and birds, where they build the dorsal ventricular ridge, or hypopallium, which has been recently divided molecularly and structurally into a lateral pallium and a ventral pallium. Afferent pallial connections are often simplified as consisting of thalamic fibres that project either to focal cell aggregates in the ventral pallium (predominant in reptiles and birds) or to corticoid areas in the dorsal pallium (predominant in mammals). Karten's hypothesis, put forward in 1969, on the formation of some isocortical areas postulates an embryonic translocation into the nascent isocortex of the ventropallial thalamorecipient foci and respective downstream ventropallial target populations, as specific layer IV, layers II- III, or layers V-VI neuron populations. This view is considered critically in the light of various recent data, contrasting with the alternative possibility of a parallel, separate evolution of the different pallial parts. The new scenario reveals as well a separately evolving tiered structure of the dorsal thalamus, some of whose parts receive input from midbrain sensory centres (collothalamic nuclei), whereas other parts receive oligosynaptic 'lemniscal' connections bypassing the midbrain (lemnothalamic nuclei). An ampler look into known hodological patterns from this viewpoint suggests that ancient collothalamic pathways, which target ventropallial foci, are largely conserved in mammals, while some emergent cortical connections can be established by means of new collaterals in some of these pathways. The lemnothalamic pathways, which typically target ancestrally the dorsopallial isocortex, show parallel increments of relative size and structural diversification of both the thalamic cell populations and the cortical recipient areas. The evolving lemnothalamic pathways may interact developmentally with collothalamic corticopetal collaterals in the modality-specific invasion of the emergent new areas of isocortex.     

Cytoarchitecture and connectivity of the amphibian medial pallium.

We investigated the cytoarchitecture and connectivity of the medial pallium of amphibians by intracellular recording and biocytin labeling. The experiments were carried out in a whole-brain in vitro preparation in the painted frog, Discoglossus pictus. Four types of neurons with specific axonal projection patterns and position in the medial pallium are distinguished, three types with extratelencephalic and one type with only intratelencephalic projections. Our findings corroborate the assumption that the anuran medial pallium is homologous to the subiculum and Ammon's horn of the mammalian hippocampus at a gross level, while the specific axonal projection patterns differ. Due to the absence of hippocampal neurons with only intrinsic projections, there seems to be no portion homologous to the dentate gyrus.     

Development and evolution of the subpallium

Among vertebrates, the ventral part of the telencephalon called the subpallium presents common basic developmental, hodological, neurochemical and functional features. It is genetically specified by expression of Dlx genes; its progenitor zones contribute a huge variety of neuronal cell types throughout the telencephalon; it is the origin and substrate of multiple and complex migration and navigation pathways during embryogenesis; and its derivatives, i.e. the basal ganglia and the amygdaloid complex, are highly conserved through evolution. Comparative developmental studies point to a largely common basic plan to generate the subpallium in vertebrates, including comparable progenitor domains and similar migratory cellular movements. In the course of telencephalic evolution however, slight variations have occurred, and the subpallium has probably represented a source for significant novelties and diversification in vertebrate forebrain anatomy and physiology.     

Development and evolution

Unlike many other animals whose sex ratios have been studied, parasitic wasps are able to determine the sex of their offspring. It is known that parasitic wasps sometimes produce different offspring sex ratios on different sized hosts. A model is constructed which includes the choice of accepting or rejecting a host as well as the choice of sex of offspring. The best reproductive strategy satisfies MacArthur's “product rule” for sex ratios and Charnov's “marginal value theorem” for optimal foraging. The model can be used to show that optimal sex ratio may vary with host density and size distribution.     

Development and evolution of the human neocortex

The size and surface area of the mammalian brain are thought to be critical determinants of intellectual ability. Recent studies show that development of the gyrated human neocortex involves a lineage of neural stem and transit-amplifying cells that forms the outer subventricular zone (OSVZ), a proliferative region outside the ventricular epithelium. We discuss how proliferation of cells within the OSVZ expands the neocortex by increasing neuron number and modifying the trajectory of migrating neurons. Relating these features to other mammalian species and known molecular regulators of the mouse neocortex suggests how this developmental process could have emerged in evolution.     

Development and evolution of thalamocortical interactions

Thalamocortical projections in mammals must travel through a considerable portion of the newly formed subdivisions of the embryonic forebrain. They descend through the ventral thalamus, advance in the internal capsule amongst cells which already possess dorsal thalamic projections, traverse the striatocortical junction, and then reach the cerebral cortex by associating with subplate cells and their early corticofugal fibers. The interactions of the thalamocortical projections with early generated, largely transient cells of these regions are believed to play a crucial role in their deployment. These ideas are supported by recent work on reeler and other strains of mutant mice. While we are beginning to understand the basic pattern of the cellular and molecular interactions employed in mammalian thalamocortical development, comparative developmental studies hold the promise to reveal the underlying logic of these steps and the evolutionary origin of the mammalian cerebral cortex.     

Development and evolution of chordate cartilage

Deuterostomes are a monophyletic group of animals containing vertebrates, lancelets, tunicates, hemichordates, echinoderms, and xenoturbellids. Four out of these six extant groups-vertebrates, lancelets, tunicates, and hemichordates-have pharyngeal gill slits. All groups of deuterostome animals that have pharyngeal gill slits also have a pharyngeal skeleton supporting the pharyngeal openings, except tunicates. We previously found that pharyngeal cartilage in hemichordates and cephalochordates contains a fibrillar collagen protein similar to vertebrate type II collagen, but unlike vertebrate cartilage, the invertebrate deuterostome cartilages are acellular. We found SoxE and fibrillar collagen expression in the pharyngeal endodermal cells adjacent to where the cartilages form. These same endodermal epithelial cells also express Pax1/9, a marker of pharyngeal endoderm in vertebrates, lancelets, tunicates, and hemichordates. In situ experiments with a cephalochordate fibrillar collagen also showed expression in pharyngeal endoderm, as well as the ectoderm and the mesodermal coelomic pouches lining the gill bars. These results indicate that the pharyngeal endodermal cells are responsible for secretion of the cartilage in hemichordates, whereas in lancelets, all the pharyngeal cells surrounding the gill bars, ectodermal, endodermal, and mesodermal may be responsible for cartilage formation. We propose that endoderm secretion was primarily the ancestral mode of making pharyngeal cartilages in deuterostomes. Later the evolutionary origin of neural crest allowed co-option of the gene network for the secretion of pharyngeal cartilage matrix in the new migratory neural crest cell populations found in vertebrates.     

Development and evolution of adaptive polyphenisms

Phenotypic plasticity is the primitive character state for most if not all traits. Insofar as developmental and physiological processes obey the laws of chemistry and physics, they will be sensitive to such environmental variables as temperature, nutrient supply, ionic environment, and the availability of various macro- and micronutrients. Depending on the effect this phenotypic plasticity has on fitness, evolution may proceed to select either for mechanisms that buffer or canalize the phenotype against relevant environmental variation or for a modified plastic response in which some ranges of the phenotypic variation are adaptive to particular environments. Phenotypic plasticity can be continuous, in which case it is called a reaction norm, or discontinuous, in which case it is called a polyphenism. Although the morphological discontinuity of some polyphenisms is produced by discrete developmental switches, most polyphenisms are due to discontinuities in the environment that induce only portions of what is in reality a continuous reaction norm. In insect polyphenisms, the environmental variable that induces the alternative phenotype is a token stimulus that serves as a predictor of, but is not itself, the environment to which the polyphenism is an adaptation. In all cases studied so far, the environmental stimulus alters the endocrine mechanism of metamorphosis by altering either the pattern of hormone secretion or the pattern of hormone sensitivity in different tissues. Such changes in the patterns of endocrine interactions result in the execution of alternative developmental pathways. The spatial and temporal compartmentalization of endocrine interactions has produced a developmental mechanism that enables substantial localized changes in morphology that remain well integrated into the structure and function of the organism.     

Development and evolution of the muscles of the pelvic fin

Locomotor strategies in terrestrial tetrapods have evolved from the utilisation of sinusoidal contractions of axial musculature, evident in ancestral fish species, to the reliance on powerful and complex limb muscles to provide propulsive force. Within tetrapods, a hindlimb-dominant locomotor strategy predominates, and its evolution is considered critical for the evident success of the tetrapod transition onto land. Here, we determine the developmental mechanisms of pelvic fin muscle formation in living fish species at critical points within the vertebrate phylogeny and reveal a stepwise modification from a primitive to a more derived mode of pelvic fin muscle formation. A distinct process generates pelvic fin muscle in bony fishes that incorporates both primitive and derived characteristics of vertebrate appendicular muscle formation. We propose that the adoption of the fully derived mode of hindlimb muscle formation from this bimodal character state is an evolutionary innovation that was critical to the success of the tetrapod transition.     

Development and evolution of the helicoidal plane of dental occlusion

The helicoidal plane of dental occlusion is a composite feature involving axial inclination of teeth and effects of dental attrition. Recent studies disagree on its distribution and significance in hominoid primates. The distribution, development, and functional basis of the helicoidal plane are investigated here, based on quantitative analysis of dental morphology and attrition in 667 human and 60 chimpanzee dentitions. Helicoidal planes are nearly universal in the human and chimpanzee dentitions studied. Increasing axial inclination of molars from M1 to M3 is primarily responsible for the helicoidal plane, although attrition acts to increase its expression. In hominoids, increased molar axial tilt appears to be associated with facial shortening and dental reduction. Population and species comparisons suggest a functional relationship with cranial structure. Progressive axial tilt of molars producing a helicoidal plane is found consistently in mammals with cheek teeth positioned partly under the cranium, as in hominids, pongids, some cebids, macropodids, ursids, and sciurids. Facial shortening is an important trend in hominid evolution and axial inclination of molars might be expected to show progressive change from Australopithecus afarensis to recent Homo sapiens.     

Development and evolution of cerebellar neural circuits

The cerebellum controls smooth and skillful movements and it is also involved in higher cognitive and emotional functions. The cerebellum is derived from the dorsal part of the anterior hindbrain and contains two groups of cerebellar neurons: glutamatergic and gamma-aminobutyric acid (GABA)ergic neurons. Purkinje cells are GABAergic and granule cells are glutamatergic. Granule and Purkinje cells receive input from outside of the cerebellum from mossy and climbing fibers. Genetic analysis of mice and zebrafish has revealed genetic cascades that control the development of the cerebellum and cerebellar neural circuits. During early neurogenesis, rostrocaudal patterning by intrinsic and extrinsic factors, such as Otx2, Gbx2 and Fgf8, plays an important role in the positioning and formation of the cerebellar primordium. The cerebellar glutamatergic neurons are derived from progenitors in the cerebellar rhombic lip, which express the proneural gene Atoh1. The GABAergic neurons are derived from progenitors in the ventricular zone, which express the proneural gene Ptf1a. The mossy and climbing fiber neurons originate from progenitors in the hindbrain rhombic lip that express Atoh1 or Ptf1a. Purkinje cells exhibit mediolateral compartmentalization determined on the birthdate of Purkinje cells, and linked to the precise neural circuitry formation. Recent studies have shown that anatomy and development of the cerebellum is conserved between mammals and bony fish (teleost species). In this review, we describe the development of cerebellar neurons and neural circuitry, and discuss their evolution by comparing developmental processes of mammalian and teleost cerebellum.     

The temporal sequence of the mammalian neocortical neurogenetic program drives mediolateral pattern in the chick pallium

The six-layered neocortex permits complex information processing in all mammalian species. Because its homologous region (the pallium) in nonmammalian amniotes has a different architecture, the ability of neocortical progenitors to generate an orderly sequence of distinct cell types was thought to have arisen in the mammalian lineage. This study, however, shows that layer-specific neuron subtypes do exist in the chick pallium. Deep- and upper-layer neurons are not layered but are segregated in distinct mediolateral domains in vivo. Surprisingly, cultured chick neural progenitors produce multiple layer-specific neuronal subtypes in the same chronological sequence as seen in mammals. These results suggest that the temporal sequence of the neocortical neurogenetic program was already inherent in the last common ancestor of mammals and birds and that mammals use this conserved program to generate a uniformly layered neocortex, whereas birds impose spatial constraints on the sequence to pattern the pallium.     

Development and evolution of the neural crest: an overview

The neural crest is a multipotent and migratory cell type that forms transiently in the developing vertebrate embryo. These cells emerge from the central nervous system, migrate extensively and give rise to diverse cell lineages including melanocytes, craniofacial cartilage and bone, peripheral and enteric neurons and glia, and smooth muscle. A vertebrate innovation, the gene regulatory network underlying neural crest formation appears to be highly conserved, even to the base of vertebrates. Here, we present an overview of important concepts in the neural crest field dating from its discovery 150 years ago to open questions that will motivate future research.     

Development of symmetry and asymmetry in the early evolution of the echinoderms

Development of pentameral symmetry in echinoderms occurred by coiling and closing up of bilateral asymmetrical trimeral metamery, characteristic of ancestral echinoderms. It originated in the ambulacral system and further developed in other systems under the influence of the original metamery and primary bilateral asymmetry. Stages of the development of pentameral symmetry on the basis of bilateral symmetry are recognized in the morphology of the ambulacral system of the earliest echinoderms.