Building the brain (1): Evolutionary insights
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- Emery Parsons
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1 Building the brain (1): Evolutionary insights Historical considerations! Initial insight into the general role of the brain in human behaviour was already attained in antiquity and formulated by Hippocrates in the 5 th century BC.! Due to alternative views of the brain s function, such as that of Aristotle ( BC), who considered that the brain served to cool the blood, little progress was made in understanding the brain for over a millennium.! During the renaissance, important groundwork was laid for a basic understanding of the brain in anatomical terms. The Fabrica of Vesalius, the first human anatomy (published 1543), played an important role in this.! In the following decades and centuries, some slow progress was made towards a more detailed understanding of neuroanatomy. However, neither the fine structure of nor the origins of the brain were understood.! With the advent of evolutionary theory due to Darwin s work in 1859, the stage was set for comparative neuroanatomical studies in different animals. Shortly thereafter, with the extension of cell theory to the nervous system by Cajal around 1900, the current era of neuroscience began.! This rapidly led to the emergence of modern comparative neuroanatomy, which coupled with molecular, developmental and functional studies, provided insight into the evolution of vertebrate brains. Origins of the vertebrate brain
2 ! Currently, it is clear that all vertebrate brains contain homologous structures (i.e. cerebellum, hindbrain, etc.) and, thus, have a common evolutionary origin in an ancestral chordate/vertebrate brain.! This does not mean that the brain of any one group of living vertebrates derived from a more primitive brain of another living vertebrate group; the mammalian brain did not derive from a brain of a living reptile.! However, until recently, there was no evidence that the brains of vertebrates and invertebrates might be evolutionarily related. Moreover, at the overt anatomical level there is no evidence for possibly homologous brain structures in the two animal groups.! Thus, given the large gross anatomical and histological differences between vertebrate and invertebrate brains, these two types of brains were considered to have separate evolutionary origins.! Indeed, classically, the evolutionary origins of the vertebrate brain were generally placed near the base of the chordate phylum implicating ancestral forms similar to extant protochordates and hemichordates.! Currently, a different view of brain evolution is emerging based on a covert level of neuroanatomy revealed by comparative studies of the expression and action of control genes that play key roles in brain development.! These studies indicate that the same developmental control genes act in brain development of invertebrates such as insects and vertebrates such as mammals. This in turn suggests that all brains of bilaterian animals might derive from an ancestral brain in the last common bilaterian ancestor. Urbilateria
3 ! To estimate the level of complexity that this ancestral brain might have had, a consideration of the probable body plan complexity of the last bilaterian common ancestor is useful. Urbilaterian body plans! Fossil evidence suggests that the last common bilaterian ancestor, Urbilateria, lived around Mya. Classical notions about the morphology of Urbilateria postulate a very simple body plan comparable to living acoelomate flatworms or cnidarian planula larva.! Contrasting with this proposed simple morphology, is the fact that both complex arthropods and complex chordates were already present Mya. Thus, animal body plan complexity and diversity (i.e. arthropod vs. chordate) would have evolved from simple forms in very short geological time.! An alternative explanation for this high level of body plan complexity and diversity early in the fossil record is the notion that Urbilateria itself was in fact not a simple bilateral bag of cells but already quite complex in morphology.! This hypothesis is supported by comparative developmental genetics which indicate that similar genes control the development of the nervous system, circulatory system, digestive system, sensory organs, etc. in all extant bilaterians, suggesting that these genes and the complex structures they control might also have been present in the last bilaterian common ancestor. Carroll et al, 2001.! Accordingly, an explanation for the high level of body plan diversity early in the fossil record is the dorsoventral inversion hypothesis (St. Hilaire, 1830),
4 which postulates that an invertebrate type of body plan would easily give rise to a vertebrate type of body plan following a simple dorsoventral inversion.! This hypothesis has recently gained strong support from molecular genetic studies of early dorsoventral patterning mechanisms which show that the signalling molecules that set up dorsoventral polarity (dpp/bmp4; sog/chordin) are conserved, but inverted topologically in insects vs. vertebrates.! Thus, if Urbilateria was indeed a relatively complex animal, it might have had a complex brain, from which the brains of all extant animals could have evolved.
5 Building the brain (2): Modular construction principles Modular patterning of the developing brain! Modularity of information processing systems is a useful organisational principle for generating ordered complexity. Modularity also facilitates the analysis of such systems.! At the overt anatomical level, the modularity of most types of brains is not generally apparent, thus, making their analysis difficult.! In contrast, at the deeper covert anatomical level of developmental control gene expression and function, modularity is readily apparent reflecting a basic metameric organization. Thus, at this level, analysis is facilitated.! Importantly, at this deeper level of developmental control gene action, remarkable similarities in brain plans in animals as diverse as insects and mammals are apparent arguing for a common evolutionary origin of all brains.! Four sets of developmental control genes that are expressed in a modular manner in early embryonic development and pattern the brains of insects and vertebrates in a comparable manner can be considered. Hox genes act in posterior brain development! The first gene set are is the homeotic or Hox genes, first discovered and analysed in Drosophila, which are expressed in the same linear order along the chromosome and along the developing anteroposterior body axis. Hox genes encode homeodomain transcription factors.! Homologous groups of Hox genes were also found in vertebrates (and later in all bilaterians) and a similar colinearity of chromosomal arrangement and body expression was observed. In general, Hox genes are responsible for the regional identity of their modular expression domains along the body axis.! In the embryonic brain of Drosophila, Hox genes are expressed in the posterior parts of the brain and nerve cord in an anteroposterior order which is very similar to the colinear expression pattern seen in the embryonic body.! In the embryonic brain of the mouse, Hox genes are also expressed in the posterior parts of the brain and spinal cord and their order of expression is highly similar to that seen in the CNS of Drosophila. Thus, the anteroposterior order of Hox gene expression is conserved in insects and vertebrates! In terms of function in brain development, the Hox genes that have been investigated in detail all have a very similar role in flies and mammals. For example, loss of the labial/hox1 group of Hox genes results in a comparable loss of neuronal identity in the mutant cells in both Drosophila and mouse.
6 Carroll, 1996 Otx genes act in anterior brain development! The second gene set is the cephalic gap genes which were also originally discovered in Drosophila. These genes are members of the segmentation gene hierarchy which subdivides the developing embryo into smaller and smaller modular domains during embryogenesis.! Examples of the cephalic gap genes are the otd/otx gene family, which also encode homeodomain transcription factors. In Drosophila, the otd gene is expressed in the anterior parts of the embryonic brain and gene mutation results in the complete absence of these anterior brain structures.! In the mouse, the homologous Otx genes (Otx1, Otx2) are also expressed in anterior parts of the embryonic brain (telencephalon, diencephalon, mesencephalon) and gene mutation also results in the complete absence of these anterior brain structures.! Indeed, the similarity in expression and action of fly otd and mouse Otx genes is such that cross-phylum rescue experiments can be carried out. Thus, a Drosophila otd-transgene can rescue a mouse Otx2 mutant so that an appropriate embryonic mouse brain is generated in the mouse mutant strain.
7 ! This interchangeability of developmental control genes is remarkable given the fact that the fly and mouse otd/otx genes have been separated by over 500 million years of evolution; it strongly finding supports the notion that the brains of insects and vertebrates are evolutionarily related. Pax genes and the development of an intermediate boundary zone! In vertebrates, an intermediate modular domain is found between the anterior and posterior parts of the brain at the midbrain-hindbrain boundary (MHB). This MHB plays an important role as an organizer center during embryonic brain development and is characterized by the expression of specific control genes including the Pax 2,5,8 genes.! The homologs of the Pax 2,5,8 genes and the other MHB control genes are present in Drosophila and are also expressed in a regionalized manner during embryonic fly brain development.! In Drosophila, all of these genes are expressed at a specific brain boundary between the anterior and posterior parts of the insect brain, just as in vertebrates. Moreover the genetic interactions among these genes are very similar in insect and vertebrate brains.! Thus, analysis of developmental control gene expression reveals a similar set of anteroposterior compartments in the embryonic brains of insects and vertebrates. Anterior compartments are specified by otd/otx genes, posterior compartments are specified by Hox genes and an intermediate compartment is specified by Pax 2,5,8 genes. Drosophil Mous T B D V en tr al N er ve B B S S S S pi n al M R h o m b Otd/Otx2 Otx1 lab/hoxb1 pb/hoxb2 Hoxb3 Dfd/Hoxb4 Scr/Hoxb5 Antp/Hoxb6 Ubx/Hoxb7 abd-a/hoxb8 Abd-B/Hoxb9
8 Columnar genes act in development of dorsoventral brain compartments! Remarkably similar dorsoventral compartments are found in the embryonic CNS of insects and vertebrates; these are set up by the same conserved set of signalling molecules that initially generate the (inverted) dorsoventral polarity of these animals (dpp/bmp4; sog/chordin).! The sog/chordin signals determine where the neuroectoderm, which gives rise to the CNS, will form along the dorsoventral axis and they also activate the expression of three columnar genes, which subdivide the neuroectoderm into three dorsoventral modular domains.! In Drosophila, the three columnar genes are vnd, ind, and msh; in the mouse the three homologous columnar genes are Nkx2, Gsh and Msx. All encode homeodomain transcription factors and their expression in the modular domains along the dorsoventral axis is very similar in insects and vertebrates ! Mutations of columnar genes in Drosophila and mouse result in very similar brain phenotypes. In flies and vertebrates, adjacent columnar genes extend their area of expression into the mutant domain, and neural progenitors as well as neurons are reprogrammed or lost in the mutant domain. A monophyletic origin of all brains! Thus, both along the anteroposterior axis and the dorsoventral axis of the developing brain, conserved compartments characterized by modular
9 expression and function of homologous developmental control genes are found in insects and vertebrates.! The remarkable similarity of developmental control gene action in modular embryonic brain development in invertebrates and vertebrates strongly implies that these nervous systems are built according to a common ground plan.! This modular ground plan was likely to have been present in the last urbilaterian common ancestor of these living groups and, therefore suggests a monophyletic origin for all brains.
10 Building the brain (3): Simple rules for complex circuitry Massively parallel connectivity! Massively parallel interconnections among numerous information processing units characterizes both modern supercomputers and biological brains. In the case of supercomputers, the underlying construction principles are known because we can build these computers.! In the case of the brains, the construction principles are poorly understood, in part due to the enormous numbers of neurons and the daunting complexity of the circuitry involved. The complex mammalian visual system exemplifies the challenge for understanding brain connectivity matrices.! While it seems unlikely that we can understand the entire complex interconnectivity of the brain, it might be possible to understand the rules by which this circuitry is generated during development. These rules may turn out to be simple.! To investigate this, invertebrate model systems such as Drosophila are useful. Insect brains are simpler than mammalian brains, nevertheless they remain complex and are composed of hundreds of thousands of neurons interconnected in sophisticated information processing circuitry. Drosophila Mouse Rules for generating neural stem cells! Given that all brains derive from the neuroectoderm, a first step in building a brain is to pattern the neuroectoderm into defined modules. This is important since unpatterned proliferation leading to masses of neurons results in the large problem of subsequently correctly interconnecting these neurons.! Patterning of the neuroectoderm is mediated directly or indirectly by the same developmental control genes that pattern the rest of the embryo. Since the
11 neuroectoderm is part of the embryonic ectoderm, ectodermal patterning genes extend their expression domains into and specify the neuroectoderm.! The resulting specified domains of gene expression regionalize the cephalic neuroectoderm from which the brain derives in a similar manner in insects and vertebrates. Each domain is characterized by specific combinations of control gene expression.! In a second step, individual neural stem cells delaminate from the regionalized gene expression domains of the neuroectoderm. In doing so the neural stem cells retain specific combinations of developmental control gene expression which serve as a molecular identity code for each of these neural progenitors.! Following their delamination, neural stem cells proliferate through selfrenewing stem cell divisions which give rise to intermediate progenitors and subsequently to neural progeny. The neural stem cells are multipotent and generate all of the neurons and glia in the brain. (from Doe) Rules for generating neuroanatomical complexity! The neural stem cells which give rise to the brain can be individually identified, based on their specific molecular identity code and on their position in the neurogenic array. Surprisingly, the tens of thousand of neurons in each brain hemisphere are generated by only 100 identified neural stem cells.! This occurs through proliferation whereby each molecularly specified neural stem cell gives rise to a clonal lineage of neural progeny. Remarkably, the anatomical features of most of the neurons in a given lineage are very similar; most of the neurons in each lineage are anatomical clones.
12 (from Urbach and Technau)! The clonal anatomy of different neural stem cell lineages is generally quite different. The entire brain can be considered to be a polyclonal composite of 100 different subunits of anatomy that are neural stem cell-derived lineages.! Given that the fundamental unit of brain anatomy in Drosophila is the clonal lineage, a simple, yet powerful rule for the formation complex connectivity in the brain is that neurons of one lineage make ordered synaptic connections to neurons of a different lineage. Clones connect to clones: the olfactory system! One of the best understood information processing system in Drosophila is the olfactory system. Olfactory sensory neurons send their axons to the glomeruli of the antennal lobe where they connect with the dendrites of specific projection neurons. The projection neurons relay olfactory information via their axons to higher brain centers, the mushroom bodies and lateral horn.! The projection neurons are clonal; most derive from two neural stem cells. Their connectivity targets, the Kenyon cells of the mushroom body are also clonal; they derive from four (identical) neural stem cells. Thus, in the olfactory system, clones connect to clones in a massively parallel connectivity matrix.! What influences the neuroanatomy and connectivity of the projection neurons? Surprisingly, the same developmental control genes, which regionalize the ectoderm and subsequently specify the identity of the neural stem cells, also control the connectivity of clonal lineages of neurons in the olfactory system.
13 Glomeruli Projection Neurons Kenyon Cells (from Heisenberg)! For example, the cepahlic gap gene ems, which is regionally expressed in the neuroectoderm and later in a subset of neural stem cells, acts in the developing projection neurons to determine the correct number of neurons in each lineage and to specify the precise synaptic interactions of the projection neuron dendrites with incoming olfactory sensory neuron axons.! Despite the obvious difference between the olfactory sense organs in insects (antenna) and in vertebrates (nasal epithelium), the general organization of the central circuitry in the olfactory system is remarkably similar in both cases.! This similarity also extends to the level of developmental control gene action. Thus, the ems gene homolog in vertebrates, Emx2, also acts at the level of the olfactory projection neurons and is required there for the correct number and connectivity of these neurons in the vertebrate brain.! Moreover, the ems/emx2 genes are required for the development of the olfactory sensory neurons in the antenna of insects as well as in the olfactory epithelium of vertebrates. Thus, at the deep level of developmental control gene action, the olfactory systems of vertebrates and invertebrates may be built by similar, evolutionarily conserved mechanisms.
14 Building the brain (4): Making more Duplication of proliferative modules! In designing increasingly powerful information processing systems, increasing quantities of memory, processors and circuitry are needed. In computer technology this generally involves duplication of modular integrated circuits. How is this achieved in biological information processing systems?! Increased neuroantomical complexity can be achieved in a simple yet highly ordered manner through the duplication of lineage-based architectural modules of the brain by duplicating individual neural stem cells.! In the fly brain, this principle of duplication of proliferative modules is used to generate a key center for learning and memory, the mushroom bodies, which are four-fold clonal structures generated by four identical neural stem cells.! Similar processes are used in the developing vertebrate cortex, where extensive neural stem cell expansion is achieved by repeated duplication of individual stem cells through symmetric proliferative divisions; these are followed by asymmetric neurogenic divisions to make neural progeny. Amplification by transient intermediate progenitors! Inherent limitations of the number of neural stem cells that can be generated through repetitive duplication are due to constraints in developmental time and space. For further amplification of neuronal circuit elements, neural stem cells must alter their proliferative properties so as to generate intermediate progenitors instead of postmitotic neural cells as their progeny.
15 ! Amplification of proliferation through transient intermediate progenitors leads to a multiplicative increase in the number of clonal progeny generated by a single neural stem cell. This amplification of proliferation by intermediate progenitors has been studied in the developing mammalian cortex and in the Drosophila brain.! In Drosophila, the molecular mechanisms of this amplification involve the asymmetrically segregation of cell fate determinants from the dividing neural stem cell to its daughter cells. In classical neural stem cells, this asymmetric segregation is such that one daughter cell becomes the self-renewing neural stem cell while the other daughter gives rise to differentiated neural progeny.! In amplifying neural stem cells, the segregation of cell fate determinants is altered such that both daughter cells retain neural stem cell features; the larger daughter remains a self-renewing neural stem cell and the smaller daughter gives rise to a transient amplifying intermediate progenitor. The Prospero gene is critical in controlled and uncontrolled amplification! A key element that differentiates classical from amplifying neural stem cells is the transcription factor Prospero. In classical neural stem cell lineages, Prospero acts as a binary molecular switch between stem cell renewal and neural differentiation of progeny. During neural stem cell division, Prospero is asymmetrically segregated to the smaller daughter cell, translocates to the nucleus and affects gene expression so as to initiate neural differentiation.! In amplifying neural stem cells, Prospero is not expressed and, thus, cannot be segregated to the smaller daughter cell. In consequence, this smaller daughter does not undergo neural differentiation and continues to divide repeatedly in a (classical) stem cell-like mode as an intermediate progenitor.!"#!"#! Importantly, and in contrast to its parent neural stem cell, the intermediate progenitor does express Prospero and also asymmetrically segregates this cell fate determinant to one of its daughter cells, which subsequently initiates neural differentiation.
16 ! Given its key role in controlling the amplification of neural stem cell proliferation, complete mutational loss of the Prospero gene and the ensuing loss of proliferation control have deleterious consequences. Absence of Prospero in intermediate progenitors leads to the repeated and expanding duplication of these proliferative cells in each of their divisions. Normal Prospero Mutant! As a result, uncontrolled exponential growth in the number of intermediate progenitor cells occurs in each of the amplifying neural stem cell clones; differentiating postmitotic neural progeny are never produced. This in turn leads to massive tumorigenesis in the brain with each amplifying neural stem cell essentially acting as a tumor stem cell.
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