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Evolutionary origins of the nervous system

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THE human brain is a true marvel of nature. This jelly-like 1.5kg mass inside our skulls, containing hundreds of billions of cells which between them form something like a quadrillion connections, is responsible for our every action, emotion and thought. How did this remarkable and extraordinarily complex structure evolve? This question poses a huge challenge to researchers; brain evolution surely involved thousands of discrete, incremental steps, which occurred in the mists of deep time across hundreds of millions of years, and which we are unlikely to ever fully understand. Nevertheless, a number of studies published in recent years have begun to shed some light on the evolutionary origins of the nervous system, and provide clues to some of the earliest stages in the evolution of the human brain. These clues come from the most unexpected of places – from sea sponges, which lack nervous systems altogether, and from the extant descendents of a primitive worm which lived some 600 million years ago. Despite their differences, vertebrates, worms and insects are all believed to be descended from a common ancestor – a worm-like organism, named Urbilateria, which lived some 600 million years ago. Urbilateria displayed bilateral symmetry – its body was symmetrical along its longitudinal axis – and this body plan was inherited by the diverse array of organisms descended from it. But, according to new research, published in 2007 in the journal Cell, it wasn’t just bilateral symmetry that the descendants of Urbilateria inherited: at the earliest stages of their evolution, vertebrates – including humans – may have inherited the organization of their nervous systems from it as well. The simplest nervous systems lack a brain, and instead consist of diffuse networks of nerves. The nervous systems of vertebrates and annelid worms, however, are organized in another way, with nerve fibres arranged in centralized cords, and large groups of nerve cells (called ganglia, singular ganglion). The major differences between them are, of course, the level of complexity, and the positioning – the nerve cord of invertebrates is located ventrally (toward the belly), whereas the vertebrate spinal cord is located dorsally (toward the back). In 1875, Anton Dohrn proposed the annelid theory, according to which, the vertebrate central nervous system arose after a proto-vertebrate inverted itself along the dorsal-ventral axis. This conflicts with the view that the vertebrate and invertebrate nervous systems evolved separately, on the dorsal and ventral sides of the body, respectively. During vertebrate development, different types of neurons are generated in a specific pattern across the dorso-ventral (D-V, or back-to-stomach) axis, as well as along the anteriorposterior (A-P, or longitudinal) axis, of the neural tube (the early developing nervous system).

one combination of signals generates motor neurons near the ventral midline. another generates sensory neurons near the dorsal midline. has evidence that suggests . just like that of the zebrafish and other vertebrates. There are. But Platynereis is considered to be a “living fossil”. and. this inhibited expression of the chemical signals that would normally be found in the targeted domain. the chemical signals in the ragworm were found to be sensitive to the same regulatory factors that are involved in patterning the D-V axis of the neural tube of the zebra fish and other vertebrates. Pax6 and Msx) were determined in worm larvae. The expression patterns of genes encoding the annelid versions of three proteins known to be involved in dorso-ventral patterning of the vertebrate nervous system (Nk2. worms and insects all inherited their central nervous system from their common ancestor. and a third generates interneurons in between. Thus. In this way. each of which is characterized by the same molecular fingerprint as its counterpart in the zebrafish. Platynereis dumerilii (above). The study by Arendt’s group therefore supports Dohrn’s annelid theory by providing evidence that vertebrates. changing the fingerprint of the cells in that domain and the pattern of cell types across the D-V axis.This pattern is brought about by the differential expression of genes encoding diffusible chemical signals. Confocal microscopy. They locally increased the concentration of a member of the BMP family. This drives the differentiation of the cell along a particular pathway. Chris Lowe. of the European Molecular Biology Laboratory in Germany. and compared them with the patterns found in development of the zebrafish. It was found that the developing nervous system of the ragworm. Furthermore. The concentration of a signal in a given location specifies a spatial domain within which a particular type of neuron will be generated. sensory neurons are generated in the dorsal half of the neural tube. in the ragworm. an assistant professor in the University of Chicago’s Department of Organismal Biology and Anatomy. is thought to resemble the common ancestor more closely than most other extant organisms. Urbilateria. and motor neurons are generated more ventrally. no Urbilateria fossils in which these gene expression patterns can be investigated. by in situ hybridization and antibody staining. However. Each domain contains undifferentiated cells that express a unique combination of these chemical signals. of course. as such. The combination of signals in a domain constitutes a “molecular fingerprint” that determines the differentiation pathway of cells within that domain. which is a vertebrate. determined the patterns of these developmental signals in the marine ragworm.2. as in vertebrates. Detlev Arendt and his colleagues. is subdivided into discrete domains. Each signal is a transcription factor – it binds to DNA and switches a specific gene or set of genes on or off (and each is itself regulated by a diffusible signalling factor belonging to the BMP protein family).

The density is an extremely complex and highly dynamic network – in humans it contains perhaps several hundred different types of protein – which organizes the molecular machinery needed for a neuron to detect and respond to the chemical signals sent to it by . Neurons are specialized to communicate with one another. so that the belly became the back. with just four different types of cells making up partially differentiated tissues in a simply organized body.otherwise. and vice versa. and other members of Arendt’s lab. For him. Arendt suggests another possibility – that Urbilateria went from being a burrowing worm that spent much of its life partially buried in the seabed to a free-swimming one. the PLoS One study shows that at least one species of sea sponge.and post-synaptic nerve cell membranes. and therefore lack. He points out that this animal uses the same signals as vertebrates for patterning the anterior-posterior axes. and this communication takes place at a structure called the synapse. On both sides of the synapse (at the presynaptic and postsynaptic membranes) the signalling components are organized by a scaffold of proteins called the pre. the pioneer of the vertebrate lineage would have been surrounded by water in all directions. the question is: how did the inversion from ventral to dorsal take place? According to Dohrn. calledAmphimedon queenslandica.” says co-author Gáspár Jékely. These surprising findings provide clues about how the first neurons may have evolved in the most ancient of animals. These structures are a specialization of the cytoskeleton found just beneath the pre. sea sponges do not need. “Such a complex arrangement could not have been invented twice throughout evolution. central nervous system development and axis patterning could well have been separate mechanisms that evolved independently. However. after which gill slits nearest the front of the body formed a mouth. For the signalling to be effective. it is crucial that all the proteins involved are organized correctly. So. in Urbilateria. a worm whose nervous system consists of a diffuse network of cells (unlike vertebrates and Platynereis. With this adaptive change in lifestyle. It must be the same system.and postsynaptic densities. Because of the lifestyle they lead. Lowe works with another descendant of Urbilateria. They are the most primitive of all multicellular animals. nerve cells. in which the nervous system is centralized). synthesizes many of the proteins that are essential for the cell-to-cell communication that takes place within nervous systems. which was published in the open access journal PLoS One at around the same time. and the body would have been fixed in a new belly-up orientation. the ventral-to-dorsal relocation of the central nervous system was simply the result of an inversion of the entire body. even though its nervous system is organized in a different way. More insight into the evolutionary origins of the nervous system come from a study of sea sponges. a miniscule gap of about 40 nanometres found at the junction between adjacent cells. muscle cells and internal organs of any kind. Sea sponges are sedentary organisms that attach themselves to the sea bed and filter nutrients from the water that they force through their porous bodies with flagella.

. which express them in its simple nervous system. Using a technique called proteomics. It is. So. whereby a pre-existing structure is modified slightly to perform a new function. Flask cells with post-synaptic densities may predate the first neurons. and mediates the movements of the machinery within the membrane in response to neuronal activity. fruit flies. In the PLoS One study. The protein product of that gene contains a number of regions that form the protein-protein bonds that hold the scaffold together. encodes a crucial component of the post-synaptic density scaffold.adjacent cells. (These genes are. and found that it contains 36 families of genes known to encode proteins of the post-synaptic density. the analysis performed by Grant’s suggests that this is not necessarily the case – it shows that brain complexity. present in cnidarians. also possible that flask cells evolved from simple neurons that lost some of their synaptic components. only a few of the human postsynaptic density genes are missing from the sea sponge’s genome – those encoding ion channel receptors for the neurotransmitter glutamate. Traditionally.) In sponges. A comparison of the DNA sequences from the 36 sea sponge genes with the homologous sequences from humans. even though it has no neurons. they analysed more than 600 postsynaptic proteins in 19 different species. the first synapses may have evolved from postsynaptic densities in a process called exaptation. however. it has usually been assumed that brains grew larger as they evolved. Kenneth Kosic and his colleagues from the University of California at Santa Barbara analyzed the Amphimedon genome. may be the most important factor which determines the behavioural repertoire of an organism. called dlg. however. Drosophila melanogaster (fruit flies) and Nematostella vectensis (a cnidarian with a simple nervous system consisting of a loose network of nerves) revealed striking similarities between the genes in all four species. where they may be involved in sensing chemical cues found in the organism’s environment. This suggests that in the sea sponge these proteins interact in exactly the same way as they do in the human postsynaptic density. If so. However. this sea sponge synthesizes an almost complete set of post-synaptic density proteins. mice and humans. The segment of the dlg gene encoding these binding regions was found to be highly conserved – the DNA sequences in the sea sponge gene were identical to the human sequences. Amphimedon has nearly all the components required to make a post-synaptic density. rather than size. and there has been a long history of linking brain size with intelligence. Seth Grant and his colleagues at the University of Oxford carried out acomparative study of the composition of the postsynaptic density in a wide variety of organisms across animal kingdom. including yeast. More recently. the genes are expressed predominantly in the flask cells of the free-swimming larvae. One gene.