Scientia Pro Publica #8 Is Up...

Here.

In honor of that, and because after last week's four big posts, I'm going to spend today on research (for future posts), there won't be a big one today.

A question for my readers: Saturday's post got a lot more positive response than any previous, and it was also more pointed towards explaining current understanding than my usual Kuhnian revolutionary efforts. Of course, I always try to provide an explanation of what I'm talking about, but that one was the first that really just pointed at summarizing current research, rather than focusing on places where, IMO, current research has gone astray (with, always, the exception(s) of the paper(s) I'm reviewing). Is this what readers want? Or rather, do you (readers) prefer posts that simply summarize current knowledge rather than pointing out major opportunities for paradigm-breaking research?

I promise to read and consider all your comments.

AK Read more!

The Nature of the Neocortex

The neocortex is a mammalian invention, not present in birds, reptiles, or any other vertebrates.  It's associated with the increases in intelligence seen in mammals since the end of the Cretaceous, especially in primates, and more especially in humans.  While there are dozens (probably hundreds) of discussions of the neocortex available on the Web, I haven't been able to find one that meets my needs (for linking to in detailed discussions), so I'm going to produce my own, in the process discussing a recent paper which reflects on it.

The neocortex develops from a part of the developing neural tube called the telencephalic pallium.^[17] This is the part of the telencephalon that is towards the back (dorsal) and upper side (dorso-lateral), while the part towards the middle of the body (medial) develops into the hippocampus, including the dentate gyrus and some other parts of the brain associated with memory (especially spacial memory) and navigation.  The bottom (ventral) part of the telencephalon develops into the basal nuclei, which "are associated with a variety of functions:  motor control, cognition, emotions, and learning. [Wiki]" (The telencephalon is split into two parts, one on each side, a feature not visible in Figure 1.)


Figure 1: Parts of the neural tube.  (From Wiki)

We'll come back to the neural tube, but for the moment let's take a look at the structure of the neocortex, by comparison with other structures: ... those that develop from the medial and ventro-lateral part of the pallium, and those in reptiles such as turtles and lizards (crocodilians are too closely related to dinosaurs and birds, and will not be considered) that have been shown to be almost certainly homologous to the neocortex: the dorsal and dorso-lateral cortex.  These latter structures develop from the same part of the pallium in these reptiles as the neocortex does in mammals, and they share many similar connections, so it's worthwhile drawing parallels.

Most sites discussing the neocortex will tell you that it has six layers rather than the three found in these other structures, and that the cells mature from the outside in rather than the opposite.  Many will also tell you that incoming axons arrive from the bottom rather than the top: that is from the direction of the inside of the neural tube rather than the outside.  All these facts are generally true, although some details are often left out and the language is often obscured by the use of various anatomical terms.  Let's go over it in detail.

The first difference has to do with the direction of maturity, the fact that cells mature from the outside in.  Neurons in this part of the neural tube are created by cell divisions in the very inner part of the neural tube, called the ventricular zone.^[8] From there, they migrate radially, towards the outer part of the tube (called the pial surface).  In turtles and lizards, these cells begin by settling in the outer part of what will become the dorsal cortex, and later cells settle inwards of them, closer to the center of the nerual tube.  This is what is meant by outside-in maturation, since once they settle, these cells begin to mature.

What most sites discussing the neocortex don't mention is that in the mammalian hippocampus (except for the dentate gyrus) the first cells settle on the inside, closest to the middle of the neural tube, and later cells settle farther out.^[8] This is exactly what they do in the developing neocortex,^[25] which means that this change is not limited to the neocortex, but is somewhat more general to the mammalian pallium.  It's a good guess that it came first, and it allows for a greater thickness of cortex with interconnections, even without the other changes, as is shown by the structure of the hippocampus.

The next change is the six-layered structure, which arises in the upper dorsal pallium and the dorsal part of the lateral pallium.  This structure probably derives from the more primitive three-layered structure found in turtles, lizards, and the mammalian hippocampus, although the latter has evolved a much thicker outer layer and a characteristic "double-C pattern" with the dentate gyrus curved around the hippocampal gyrus.  The three-layered structure in general is called the "allocortex": this word specifically stands for the parts of the "cerebral cortex" with a three-layered structure, although it's often used for other areas with the same cortical structure.  (The "cerebral cortex" technically refers to the entire cortical area formed from the pallium, but is often instead mistakenly identified with the neocortex.)

We need to start by describing the three-layered structure, then, before we can compare it with the six-layered.  The three layers are like a sandwich, with areas of mostly neurites (axons, dendrites, synapses, and glial cells) making up the bread, while the filling is densely filled with neural cell bodies (somas).  Most of the neural connections come from the outside (the side away from the center of the primitive neural tube), while in this area most of the axons leaving do so out the bottom (the side towards the center of the neural tube).  This provides for a simple "pass-through" system, in which the nerve cells process the incoming information and produce an output which goes to another brain region.

The disadvantage of this system is that the incoming axons are growing along the top of this layer, and trying to make synaptic connections with any cells they encounter.^[8] Since most of these cells don't want any specific connection, most of these attempts are refused, which constitutes a major waste of resources.  Which leads us to the third difference, which is that many incoming axons from other parts of the brain come from below in mammals, in more evolved mammals, such as primates and carnivores, virtually all.  We'll discuss this shortly.

Before we do so, we need to consider the layers of the neocortex, which are very different from the allocortex.  The layers of the neocortex are usually numbered I through VI (usually using Roman numerals, although many websites use Arabic).  Layer I is almost completely free of neuron somas, being mostly made up of neuropil, along with blood vessels and other support structures.  Layers II and III have many neuron somas, a good mix of pyramidal cells (see below) and interneurons, the latter usually making local connections with their axons as well as their dendrites.  Layer IV is composed of a mix of stellate cells, which like interneurons make local connections, in the sense that they typically don't extend their axons out of the area they reside, but they extend much farther than interneurons, and they tend to be exitory rather than inhibitory (see below).  Layers V and VI contain mostly pyramidal cells, although with some interneurons, and the lower part of layer VI often contains a large proportion of neurites, especially axon branches.

In the allocortex, the majority of the interconnections are in the upper layer, although the lower layer (the one closest to the middle of the neural tube) has lateral extensions of outgoing axons, which make some connections, probably rising into or through the middle layer.  In the neocortex, the bottom layer, called layer VI, roughly corresponds to this layer, consisting mostly of lateral branches of outgoing axons, which then make connections with other neurons (or glial cells).  The middle layer of the allocortex has often been compared to layers V and the upper part of layer VI of the neocortex, because the cells (with somas) there usually extend their axons to other parts of the brain, as do most of those in the allocortex.^[25]

Very few cells of the allocortex (at least in turtles and lizards) make connections to other areas of the allocortex; they mostly talk to other regions of the brain.  Thus, areas II and III of the neocortex, most of whose pyramidal cells send their axons to other parts of the neocortex,^[25] can reliably be considered new in mammals.  That leaves areas I and IV, either of which might be compared to the outer layer of the allocortex, although there are differences in both cases.  Axons coming from other regions of the brain usually terminate in layer IV of the neocortex, especially those coming from below, which would make this area comparable to the outer layer of the allocortex.  Axons coming from other areas of the neocortex usually terminate in layer I, which would suggest that it's new.  However, axons that crawl along the outside of the neocortex, most of which come from lower parts of the brain, probably interact with layer I in the same way that similar axons in the allocortex interact with its outer layer, which would imply some comparability there as well.  It's well to remember that these comparisons are merely tools, artifacts of our need to use analogy to understand what's going on.  Evolution is hardly constrained to fit within the categories we make for our convenience.

Before we consider the various connections into and out of the neocortex, let's take a look at the early evolution of the neural tube.  This structure is inherited by vertebrates from their chordate ancestors, indeed recent research shows that the chordates themselves almost certainly inherited it from the earlier common ancestor of the echinoderms, hemichordates, and chordates.^[24] I have already suggested that concentration of nerves into a cord was primarily dependent on the availability of a circulatory system that could deliver enough oxygen to power their energy-dependent activity, a development that could have ramped up via the cold temperatures of the "snowball earth" conditions long before the Cambrian.

In chordates and their ancestors this oxygen was essential both to the neuropil, the system of nerve somas, neurites, and glial cells that performed calculations, and the axons which carried the results to other locations within the neuropil.  However, in vertebrates we find Myelin, which insulates the axons and both increases the speed of impulses by perhaps an order of magnitude (or even more, depending on its thickness), and substantially reduces the energy requirements.  This means that the primary requirement for energy was to the neuropil, the "grey matter", while the mass of axons, the "white matter" required much less.

In the original neural tube the neuropil was on the inside, while the axons were on the outside.  This structure is almost certainly primitive, since it's carried over into the retina, where the reversed structure of the neural tube is expressed, and the nerves carrying information from light-sensitive cells actually travel over the surface of those cells (gathering and passing behind the retinal surface in the "blind spot").  In the spinal cord, it was developed into the standard structure of gray matter on the inside and white on the outside, which is very expandable, since most of the axons are traveling in a forward/backward (anterior/posterior) direction, and they are simply pushed farther apart (rather than lengthened) by expansion.  Similarly, an expansion of the gray matter simply thickens it, with little impact.

In the front of the neural tube, things became a little more complex.  Most of the primitive spinal cord was originally dedicated to controlling the actions of a body that was basically eel-like, swimming with an undulating movement, perhaps modifying it's motion with movements of the "fin-flaps" along each side of its body.  Even when the "fin-flaps" came to be replaced with dedicated fins at the front and back, this just caused a small specialization of pre-existing bundles of ganglia, without impacting the effectiveness of the basic structure.


Figure 2: Five vesicle stage of embryo.  (From DEVELOPMENT OF THE CENTRAL NERVOUS SYSTEM

But from the beginning, the brain was different.  As you can see from figure 2, the di-encephalon has a pair of extrusions, which actually develop into the retinas.  The olfactory system, OTOH, develops from the very front of the telencephalon.  This puts the rest of the telencephalon between the optical system and the olfactory system.  What does that mean?

For the earliest vertebrates (or chordates), swimming involved an undulatory movement that caused both the eyes and the nostrils to weave through the water.  In order to identify whatever objects were seen in the water, their path in the visual system had to be integrated with the knowledge of the body's movement (coming from parts of the brain further back) to provide their location relative to the animal's actual path through the water.  With chemicals diffusing through the water, the situation was more complex.  Each object was emitting various chemicals that the olfactory system could sense, which diffused away from it subject to local currents and variations, until after a certain time it impacted the path of the nostrils (usually located at the very front of the animal) as they wove through the water.  Thus the integration of olfactory cues with observed objects was a very complex problem.

In an earlier discussion I mentioned that even the earliest "swimming sponges" would have found a highly beneficial (speaking selectively) use for integrative intelligence, and the same holds true here.  We can't estimate the intelligence of these animals, or this part of their brain, by the number of axons going into or coming out of it, because it might not take many axons to carry the information needed for the calculation, relative to the complexity of the calculation itself.  But this would have made the region of the brain that later became the neocortex essential to the survival and prosperity of these animals, and when the necessary number of neurons and connecting axons grew, evolution provided the answer with the changes we observe in mammals.

If we fast-forward to the development of the earliest mammals, we find animals that used the three-layered allocortex for this process.  At this time, the areas of the dorsal pallium primarily received input from other regions of the brain, especially those that would become the thalamus, and sent their output to other layers, also often (other parts of) the thalamus.  Presumably, this part of the brain performed calculations that were, in effect, straight transformations: integrating and massaging incoming information to provide answer(s) that could be sent on for further use.

I've mentioned that in the allocortex inputs primarily arrived at the outer layer.  Cells in the middle (and lower) layer had to make connections to them, which they did by extending a large dendrite, called the "apical dendrite", to the surface.  What makes them pyramidal in shape (which gives them their name) is that they also extend smaller dendrites in other, lateral, directions, to receive inputs from other cells in their own layer.  This tends to control the shape of the cell, which looks like a pyramid because each of these large dendrites tends to create a "corner" on the cell.  The axon, with its axon hillock, tends to be much smaller, and doesn't really affect the shape of the cell.  Pyramidal cells are the primary type of cell that send axons out of cortical area to other parts of the brain.

The other primary type of cell in these cell-rich layers are interneurons, which are usually inhibitory cells: unlike pyramidal cells (and stellate cells) they use a neurotransmitter (GABA) that tends to cause the target nerve cell not to fire action potentials rather than making it fire as excitatory cells do.  Interneurons tend to have smaller arbors for both their dendrites and axons, although they often enough couple together via electrical (gap) junctions so that a single action potential can spread over quite a distance.  They also usually migrate tangentially from other parts of the developing brain.^[25]

In mammals, as well as in dinosaurs and birds, the need for more complete integration of the various calculations, as well as more sophisticated time-dependent analysis, resulted in many further connections between various areas of the future neocortex.  In the ancestors of dinosaurs, this led to the evolution of the wulst, a structure that has sometimes been compared to the neocortex, but has convincingly been shown to have developed independently.^{[4] [17]} In mammals, the neocortex evolved.

The early interconnections between cortical regions, in reptilian ancestors, went via the thalamus.  However, to create a new intercortical connection via the thalamus it's necessary to create a new population of thalamic nerve cells, as well as processes to guide axons from these new cells to the target area of the cortex.  Of course, a new population of pyramidal cells in the cortex is also necessary, which will sample the calculations going on in the neuropil and send the output via their axons to the appropriate spot.  It's also necessary for guidance processes to evolve so that those axons can find their way to where their output is needed.  But if the connection is directly cortical-to-cortical, these are all that are needed: nothing involving the thalamus is required.

The development of new cell types, with their new connections, depends critically on the six-layered structure of the neocortex.  In this regard, I want to mention a recent paper, Cerebral cortex development: From progenitors patterning to neocortical size during evolution (by Alessandra Pierani and Marion Wassef), which unfortunately is behind a paywall.  This paper surveys current knowledge of how pyramidal cell formation is regulated during the development of the neocortex.  A key point is the specification of different subtypes destined for different layers:

The distinct laminar subtypes of neocortical neurons are born in a tightly regulated 'inside-out' sequence.  The neurons destined to the deep layers are produced first followed by neurons fated to populate successively more superficial layers.  Lineage tracing of single radial glia progenitors indicated that, at early stages, radial glia progenitors can produce successively the full repertoire of the major layer-specific neuronal types both in vivo and in vitro.  Transplantation and cell culture experiments have, however, shown that the repertoire of the radial glia progenitors becomes progressively restricted ([refs]).  The group of McConnell has shown that early cortical progenitors at the stage when they normally form layer VI neurons are multipotent and can generate later-born neurons of upper layer II/III, if exposed through transplantation to signals from a late cortical environment ([ref]).  In contrast, later progenitors at the stage when they normally give rise to layer II/III neurons fail to produce deep layer neuronal types when transplanted to an early environment ([refs]).

This means that a complex interaction of transcription factors, and feedback loops among them, progressively tightens the ability of these progenitor cells to differentiate, limiting them to the current stage and later stages.

There have been some exceptions discovered to this pattern in rodents, which might complicate things, they are still under investigation.

There are also tight structures of transcription factors and loops among them that regulate the proliferation of early progenitor cells, controlling the ultimate area of each part of the neocortex.  Pierani and Wassef also discuss the means by which the various parts of the neural tube are sectioned into regions such as the neocortex, and how the areas within it come to be defined.  Gradients of various signalling molecules are built up, so the the ratio of these different molecules at any point is unique, after which a system of cross-repression divides the developing neural tube into specific regions, with gradients of signaling molecules within these regions which presumably allow incoming neurons to find their way to their specific target spot within the region involved.

Precisely how the new layers of the cortex, layers II and III, first arose can only be guessed at (at this point).  It seems likely that the inside-out progression, and the tightly regulated system of distinct laminar subtypes described by Pierani and Wassef, evolved first, laying the groundwork for layers II and III.  Once these layers were present, a new cell population could arise via mutation that targeted another cortical region, a far more likely (or less unlikely) event than depending on a thalamic relay.  We can envision that the progressive evolution of the mammalian neocortex proceeded from this point.

We can see, then, that the neocortex, with its more sophisticated structure, allowed a substantial increase in the interconnectivity of the various regions of calculating neuropil, which in turn permitted the massive expansion of the brains, and intelligence, of the evolving mammals.

Alessandra Pierani, & Marion Wassef (2009). Cerebral cortex development: From progenitors patterning to neocortical size during evolution Development, Growth and Differentiation, 51 (3), 325-342 DOI: 10.1111/j.1440-169X.2009.01095.x

Links: (I've included only the link called out in this leader.) Not all of these are called out in the text, and too many are behind a paywall. Use the back key if you came via a footnote.

1.  The evolution of the neocortex in mammals: how is phenotypic diversity generated? paywall

2.  Genetic and epigenetic contributions to the cortical phenotype in mammals

3.  Similarity and Diversity in Visual Cortex: Is There a Unifying Theory of Cortical Computation?

4.  Do birds possess homologues of mammalian primary visual, somatosensory and motor cortices? paywall

5.  The contribution of spike threshold to the dichotomy of cortical simple and complex cells paywall

6.  Laminar processing in the visual cortical column

7.  Neuronal circuits of the neocortex

8.  The early differentiation of the neocortex: a hypothesis on neocortical evolution

9.  Cortical mechanisms of action selection: the affordance competition hypothesis

10.  Area Patterning of the Mammalian Cortex

11.  Hagfish embryology with reference to the evolution of the neural crest paywall

12.  Cyclostome embryology and early evolutionary history of vertebrates

13.  Migratory neural crest-like cells form body pigmentation in a urochordate embryo paywall?

14.  Brain and Behavior (IPHY 3730), University of Colorado at Boulder not peer-reviewed, but a good overview

15.  Brain segmentation and forebrain development in amniotes paywall

16.  Vertebrate head development: Segmentation, novelties, and homology paywall

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

18.  The emergence and evolution of mammalian neocortex paywall

19.  The functions of the preplate in development and evolution of the neocortex and hippocampus paywall

20.  Cortical Excitatory Neurons and Glia, But Not GABAergic Neurons, Are Produced in the Emx1-Expressing Lineage

21.  Postnatal development of the telencephalon of the tammar wallaby (Macropus eugenii). An accessible model of neocortical differentiation paywall

22.  Development of the olfactory system in a wallaby (Macropus eugenii) paywall

23.  The Medial Pallium

24.  Centralization of the Deuterostome Nervous System Predates Chordates paywall

25.  Cerebral cortex development: From progenitors patterning to neocortical size during evolution paywall

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Greening the Earth

It's an interesting question, when did photosynthetic life first invade dry land, and what type was it? The tradition is that green plants first invaded the land in the Ordovician or Silurian, if not later, sometime after 500 MYA,^[7] well after the Cambrian, when we first see fossils of animals developing in the ocean (there are actually some from earlier, but those may not be animals, and we know little about them). However, there are various lines of evidence that there was already extensive land-based photosynthesis going on a good deal earlier,^{[3] [4]} including a very recent paper:^[2] The late Precambrian greening of the Earth (by L. Paul Knauth and Martin J. Kennedy, unfortunately behind a paywall), which examined the correspondence of ratios of carbon isotopes and oxygen isotopes in precambrian deposits, specifically from areas influenced by runoff from continents:

Here we compile all published oxygen and carbon isotope data for Neoproterozoic marine carbonates, and consider them in terms of processes known to alter the isotopic composition during transformation of the initial precipitate into limestone/dolostone. We show that the combined oxygen and carbon isotope systematics are identical to those of well-understood Phanerozoic examples that lithified in coastal pore fluids, receiving a large groundwater influx of photosynthetic carbon from terrestrial phytomass. Rather than being perturbations to the carbon cycle, widely reported decreases in ¹³C/¹²C in Neoproterozoic carbonates are more easily interpreted in the same way as is done for Phanerozoic examples. This influx of terrestrial carbon is not apparent in carbonates older than ~850 Myr, so we infer an explosion of photosynthesizing communities on late Precambrian land surfaces. As a result, biotically enhanced weathering generated carbon-bearing soils on a large scale and their detrital sedimentation sequestered carbon. This facilitated a rise in O₂ necessary for the expansion of multicellular life.

This analysis basically plotted the isotope ratios from thousands of observations on a two-dimensional axis, and observed that those from after about 850MYA fell into the same groups whether they were after the beginning of the Cambrian or before. This leads to the very plausible conclusion that photosynthesizers had colonized the land and were producing large amounts of carbon-rich detritus that was then oxidized and deposited.

This has some interesting implications: ...

The contrasting isotope data between 850 Myr ago and the Neoproterozoic suggest that the terrestrial expansion of photosynthesizing communities preceded the significant climate perturbations of the late Precambrian glaciations, and was followed by a rise of O₂ ([ref]) and a secular change in terrestrial sediment composition. The onset of significant biotically enhanced terrestrial weathering would have increased the flux of lithophile nutrient elements and clay minerals to continental margins. This would have increased production and burial preservation of organic C towards modern values and consequently facilitated the stepwise rise in atmospheric O₂ necessary to support multicellularity. The terrestrial expansion of an extensive, simple land biota indicated by the isotope data may thus have been a critical step in the transition from the Precambrian to the Phanerozoic world.

The biggest problem with this is the lack of fossils identifiable as from plants, although the "squishier" plants leave few fossils.

There is one very important feature of plants that allowed them to colonize the land: the invention of mixtures of lignin and cellulose that protects them against the "soft" ultraviolet radiation (UV) that makes it through the ozone layer. This mixture, in turn, depends on a synthesis pathway that begins with an enzyme called Phenylalanine Ammonia Lyase (PAL), "which catalyses the first and essential step of the general phenylpropanoid pathway, leading from phenylalanine to p-Coumaric acid and p-Coumaroyl-CoA, the entry points of the flavonoids and lignin routes."^[8]

Another very recent paper, A horizontal gene transfer at the origin of phenylpropanoid metabolism: a key adaptation of plants to land (by Giovanni Emiliani, Marco Fondi, Renato Fani, and Simonetta Gribaldo) reports an intriguing discovery: that the gene for this enzyme was almost certainly acquired via horizontal gene transfer from a soil bacterium, or perhaps from a fungus that had in turn acquired it from a soil bacterium. What they did was to examine the phylogenetic tree of "160 representative sequences" from various species, discovering that all the genes in plants and fungi are descended from a single ancestor related to those of one bacterial lineage. This gene "is homologous to histidine ammonia lyase (HAL), which is involved in the catabolism of histidine and is widespread in prokaryotes and eukaryotes [refs]. It has been proposed that "PAL developed from HAL when fungi and plants diverged from the other kingdoms" [ref]. However, the current view of eukaryotic evolution based on phylogenetic analyses indicates that fungi and plants do not share an exclusive ancestor [refs]. In fact, Fungi are more related to Animals than to land plants. Moreover, land plants belong to the phylum Plantae, which also includes Glaucocystophytes, red algae, and green algae [refs]."


Figure 1: Phylogenetic tree of HAL/PAL gene. Click on image to see original with caption. (From Ref 8 Figure 2)

This, combined with the observations of Knauth et al., brings us to an interesting suggestion: is it possible that, before green plants invaded the land, it was covered with lichens? Lichens, even today, often grow in areas that are heavily exposed to sunlight (UV) but lack the soil necessary for plant roots (and their symbiotic association with certain fungi). Absent plants, they may well have been able to colonize just about any area with sufficient rainfall to provide the water they needed. Lichens are known to invade rock for nutrients,^[6] and even cyanobacteria, one of the groups of algae that for symbiotic relationships with fungi to create lichens can chemically erode rocks.^[5] The possibility that there was a coating of lichens over most of the Earth's surface as long as 850MYA is quite intriguing.

An obvious question is: what, if anything, ate these lichens? Here I want to hark back to a suggestion I made a while back, regarding the origin of multi-celled animals, and probably other forms of life:

Could it be that the common ancestor of fungi and animals was actually multinucleate, an amoeba-like creature with lots of nuclei, a flexible shape, and a feeding pattern based on engulfing its food?

Such a creature would be well positioned to evolve into both fungi and metazoans, with the latter branch having lots of collared flagelli. The question is, why evolve multiple cells? The answer could well be an explosive adaptive radiation of invasive, intracellular predators. Such an explosion would explain the sudden acquisition of multicellularity by many lineages.

It isn't just animals and fungi that would be so descended, and it's quite possible that a variety of multinucleate amoeboids were present in these early times that fed on the early lichens I've proposed. (Indeed, there are many such today. These may well have lived in small, shaded tunnels during the day (when solar UV may well have threatened them), and come out at night to feed on the upper levels of the lichens. The lichens themselves may have used some form of lignin (or dyes depending on PAL for synthesis) to protect themselves from the sun, although another possibility is that they shed their upper levels as they were damaged, regrowing from cells located deeper, where they were protected from UV. Or it could have been a combination of both.

The possibility that there was a full-blown ecosystem present on the land this long before the Cambrian offers exciting possibilities in understanding the earliest evolution of the animals (in the ocean), as it would have provided large quantities of detritus for food, along with the oxygen needed to take advantage of it. Especially important is that it this would have been true during the two proposed eras of "snowball earth" or "Slushball Earth", when glaciation extended quite far towards the equator: large areas of the earth's coastline would have experienced freezing temperatures along with intense sunlight.

This is important because water close to the freezing point can actually contain enough oxygen to function as blood in an animal that isn't too active, unlike warmer water. This means that animals during those periods might have invented sophisticated circulatory systems, carrying oxygen for all their needs, without the need for cells containing haemoglobin or some other compound specialized for carrying larger amounts of oxygen. By the time the glacial ages were over, presumably some lineages (at least of chordates) had already developed blood cells containing haemoglobin, thus kicking off the chordate/vertebrate adaptive explosion.

Knauth, L., & Kennedy, M. (2009). The late Precambrian greening of the Earth Nature DOI: 10.1038/nature08213

Emiliani, G., Fondi, M., Fani, R., & Gribaldo, S. (2009). A horizontal gene transfer at the origin of phenylpropanoid metabolism: a key adaptation of plants to land Biology Direct, 4 (1) DOI: 10.1186/1745-6150-4-7

Links: (I've included only those links called out in this leader.)These are almost all behind paywalls, unfortunately. I wish they weren't, but...

1.  Plant-driven fungal weathering: Early stages of mineral alteration at the nanometer scale paywall

2.  The late Precambrian greening of the Earth paywall

3.  Late Precambrian Oxygenation; Inception of the Clay Mineral Factory free registration required

4.  Molecular Evidence for the Early Colonization of Land by Fungi and Plants free registration required

5.  Effect of cyanobacterial growth on biotite surfaces under laboratory nutrient-limited conditions paywall

6.  Mineralogical transformation of bioweathered granitic biotite, studied by HRTEM; evidence for a new pathway in lichen activity paywall

7.  The early development of terrestrial ecosystems

8.  A horizontal gene transfer at the origin of phenylpropanoid metabolism: a key adaptation of plants to land

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Concepts, Cognition, and Anthropomorphism

Ever since Plato, western philosophers have looked at words, and the objects they represent, as a sort of fixed ideal:  the word "couch", for instance, represents an object, or rather one of a class of objects.  Lately, in the last few centuries, scientists and/or philosophers have recognized that the same word might represent different, but widely overlapping, classes under different circumstances (contexts), a fact that often leads to confusion, sometimes deliberate.  All of this tends to focus attention on the relationship between words and symbols, strengthening the notion that humans are the only "Symbolic Species", since the evidence is overwhelming that no other species (with a few possible cetacion exceptions) uses language in anything like the way we do. 

But is that true?  How closely are symbols, and the concepts they represent, tied to language and the use of words as symbols?  For that matter, what is a symbol, in terms of cognition, or the mechanics of our brains? 

Before we explore these questions, let's back up and take a look at the context:  the paradigm within which we are asking these questions, understanding what they mean, and judging the answers. 

It began with Plato, as mentioned above.  From his work we get the concept of the Platonic Ideal:  the perfect representation, the archetype, behind a concept represented by a word.  As he explained it, we are chained in a cave as it were, looking at the back wall, able to see only shadows cast by the ultimate, ideal, reality cast by the light of "Truth", because we are unable to turn and look out the entrance. 

This paradigm was pretty much universal by Hellenistic times (a few centuries after Plato) in the west, and also, I suspect, in the east where it had spread via Persion/Greek influences to India, and from there via Chan/Zen Buddhism (and possibly other schools) across North Asia to China.  (My suspician is partly founded on the fact that Zen Koans seem well designed to break the tyranny of words/concepts as absolutes, forcing the seeker to recognize that these things are only limited tools, like a set of shelves which are fine for holding small solid objects, but limited for very large objects and useless for liquids.) 

The reality, as recent research is showing, is that our brains typically identify words heuristically:  we learn of a number of items that belong to a class represented by a word, our minds (often subconsciously) identify common features or characteristics of these items, and we tentatively identify new members of the class based on those same shared features/characteristics. ...

Backing up again to Plato, we can see that there's no reason that such classes require an "ideal" at all:  they are just groupings of items that are all similar enough to justify attaching a word, a symbol, to the class.  A concrete example may be helpful:  consider the word "couch".  This may be loosely defined as a bench with a back and armrests (at least in modern usage), long/wide enough for at least two people to sit comfortably.  Can we define a Platonically ideal couch?  Not without context.  For instance, to Victorians such a couch would have had a reasonably vertical back and stiff cushions, helping to support people who were expected to sit up with good posture while socially interacting.  But for modern laid-back music lovers, the ideal couch will be much more relaxed, allowing occupants to lean back and totally relax while losing themselves in musical reproductions not available even live to Victorians. 

Thus, the ideal, singular to Plato, splits into many depending on context, observer, and time.  The problem is that our thought patterns, our paradigms, are constrained by over two thousand years of Plato's influence, and they often interfere with efforts to understand how language, symbols, and concepts work. 

It's certain that the human brain has a mechanism for representing words:  my best guess is that they're normally represented (in at least one area of the brain) as abbreviated "shorthands" for the sequence of tongue, lip, mouth, throat, and diaphragm movements that go into pronouncing them.  But is this true of concepts?  Did recent human ancestors invent the concept, or the symbol that stands for it?  Are even our closest relatives lacking this feature? 

I think not.  We know that many primates possess "mirror neurons", pyramidal cells in parts of the neocortex that tend to fire in the same groups when the animal is performing (or preparing to perform) some action and when it's observing some other animal performing that action.  I would say that actions of this sort represent concepts, and that the processes around the firing of these "mirror neurons" represent neurological symbols (or the use of them).  At a sufficiently abstract level, there's no real difference between a specific pattern of lines on a piece of paper (or clay) and a specific pattern of neurons in the neocortex (or a specific pattern of sounds). 

Before we go farther, we need to examine how the mammalian neocortex operates.  I'm going to use Francis Crick's Astonishing Hypothesis as a base, although it's highly simplistic and probably wrong in some details.  As he does, I'm going to focus on the V1 area in the visual cortex, which receives input from the retina (via the lateral geniculate nucleus: a part of the thalamus), performs a complex transformation on it, and sends the results on to further areas of the brain. 

The large majority of axons coming from the retina carry a single type of message:  each neuron is watching a specific location in the retina, looking for a specific type of spot against an opposite background:  some look for big spots, some for small.  Some for dark spots (against a light background), some for light.  some for red spots (against a presumably green background), some for blue, green, purple, etc.  Now all of these things these different neurons are looking for can be mapped onto an n-dimensional space:  in this case with n probably equal to five:  two dimensions for the location within the retinal field, one for size, one for color, and one for light/dark.  The light/dark axis may be discrete rather than continuous; it may even be two-valued.  The color axis also may be somewhat more complex than my simple description makes it sound:  there are some complications regarding the distribution of cone types within the retina that time and space don't permit discussing.  These points don't affect the basic picture:  the visual field of the retina can be mapped as an n-dimensional space of "spots" with each neuron sampling a specific location in that space and responding accordingly. 

Of course, most of the visual field isn't made up of spots (although in the world of the earliest chordates it may well have been:  our evolutionary history is often built into our design in ways we wouldn't suspect).  What each neuron in the retinal population I'm discussing does is look to see how much the visual input resembles the type of spot it's looking for, and the more it does, the larger its firing rate (the faster it fires action potentials).  Notice, then, that what we have here is a continuous function over a continuous space (disregarding complications involving a discrete light/dark axis) varying continuously over time, but sampled at discrete points in space and time.  Each neuron occupies a specific point in the n-space and samples that one point (although since it's actually examining the vicinity looking for a spot, one close to its location would generate a partial signal).  Each neuron intermittently sends a signal with its instantaneous firing rate, thus the closer it is to seeing what it's looking for, the more frequently its signal is being sampled. 

What does the V1 area do with this information?  The major populations of pyramidal cells look for bars:  wide bars, thin bars, vertical bars, horizontal bars, dark bars, light bars, red, blue, green, purple, etc.  And everything in-between.  The information brought from the retina (relayed via the lateral geniculate nucleus) is integrated and messaged by the cortical neuropil and the stellate cells of layer IV, eventually allowing the pyramidal cells to sample an n-dimensional space of bars and send their signal accordingly.  (Actually, the situation is more complex because these cells are also looking for time-dependent patterns as well, but if they can support the more complex situation, they can certainly support the simpler one.) 

Are we beginning to see a pattern here?  Nerve cells in at least two parts of the brain can, in effect, occupy a discrete location in some n-dimensional space, sample a scalar signal at that location, and output the results to their axons, whence it's carried to other parts of the brain.  (The vertebrate retina is part of the brain developmentally:  it starts out as part of the neural tube and is then drawn away into the eye structure.  It's not part of the neocortex, however, the retina had differentiated and specialized a long time before the ancestors of mammals invented the neocortex.^[1]) 

We don't need, here, to go into how this process is achieved:  it's enough to know it can be done.  And what one area of the brain can do, so can any other:  whatever the mechanism, it's almost certainly reusable.  (Note, however, that just because this mechanism is available to every part of the brain doesn't mean every part of the brain uses it.  OTOH when we're looking for a mechanism to explain some observation, it is an obvious candidate.) 

Let's get back to our "concepts" within the brain represented by specific groups of neurons (such as "mirror neurons") firing when a specific "concept" is called to mind in an animal, either by seeing some other animal performing an action or by performing, or preparing to perform, that action.  Based on the description above, it's a good guess that those neurons occupy a specific location in some n-dimensional "concept space" that corresponds to the specific act involved.  Of course, since at this level of consciousness humans, and probably other primates, normally pay attention to only one general subject at a time, it may be that each individual concept is represented by a unique pattern:  sort of like an ideogram but in n dimensions rather than just two. 


Figure 1:  Cursive hieroglyphs (a type of ideogram) from the Papyrus of Ani, an example of the Egyptian Book of the Dead.  (From Wiki)

At this point I want to discuss some very recent research:  Mirror Neurons Differentially Encode the Peripersonal and Extrapersonal Space of Monkeys ( by Vittorio Caggiano, Leonardo Fogassi, Giacomo Rizzolatti, Peter Thier, Antonino Casile), which is unfortunately behind a paywall, but let me blockquote the abstract:^[3]

Actions performed by others may have different relevance for the observer, and thus lead to different behavioral responses, depending on the regions of space in which they are executed.  We found that in rhesus monkeys, the premotor cortex neurons activated by both the execution and the observation of motor acts (mirror neurons) are differentially modulated by the location in space of the observed motor acts relative to the monkey, with about half of them preferring either the monkey's peripersonal or extrapersonal space.  A portion of these spatially selective mirror neurons encode space according to a metric representation, whereas other neurons encode space in operational terms, changing their properties according to the possibility that the monkey will interact with the object.  These results suggest that a set of mirror neurons encodes the observed motor acts not only for action understanding, but also to analyze such acts in terms of features that are relevant to generating appropriate behaviors.

Unlike many abstracts, this one is pretty easy to understand, and its implications are extremely relevant to the subject here.  The "mirror neurons" under examination are associated with motor activity, and may well be associated with a system of representing "concepts" with shorthands of motor sequences. 

I mentioned above that in my view the representation for words in the human brain is some sort of "shorthand" for the sequence of muscle actions involved in pronouncing it; similarly it makes sense that in monkeys, apes, and other primates with "mirror neurons" the representation in at least one area of the brain for "concepts" involving actions is a similar shorthand for the muscle actions involved.  Or rather, the shorthand in primates came first, and the process was adapted for use with language by adding specific tongue, lip, mouth, throat, and diaphragm movements to a system already adapted for arm, leg, hand, and foot movements. 

In trying to understand how "concepts" are represented in the brain, we need to consider how they're used.  As Caggiano et al. point out, the relevance of an action undertaken by another depends (in kind as well as quantity) on the distance of that other, and it makes sense that the specific "concept" activated in the brain is slightly different depending on that distance.  Rather than trying to separate these different reactions into completely separate concepts, perhaps we should think of this as more like adverbs modifying a verb:  the same action stimulates the same concept, but the distance, both absolute and operational, stimulates distinct modifying adverbs.  Of course, we must also keep in mind that this research looked at only one area of the brain, and that one being associated with motor activity, specifically the planning and execution of such activity.

We need to keep in mind that the brain is made up of many areas, all talking to one another:  in rhesus monkeys there are 52 areas just on each side of the neocortex, this may also be the number for humans, although the detailed research needed to prove it hasn't been done yet for ethical reasons.  There may be, probably are, more than one area involved in expressing these "concepts", and each area probably uses a different system of representation.  Exactly how these areas express their concepts, and the precise relationships among expressions in different areas, is a subject for future research.  However there are some things we can be fairly sure of from what we know already. 

For one thing, the brain appears to operate on a very associational basis:  if one area is stimulated to "fire" a certain concept it will likely stimulate other areas to fire the same concept.  Some of these areas may act to relate concepts to one another, others may act to related observations of other animals to various concepts that classify their actions, yet others may act to relate concepts for proposed actions to specific conditions such as food lying on the ground nearby or hanging from a nearby branch, yet others may serve to react to various concepts with responses from memory regarding past incidents where similar actions took place in similar circumstances.  The relationship among these various areas may then allow a decision regarding whether, and how, to undertake the action this concept represents. 

Again quoting from Caggiano et al., this time from the conclusion:^[3]

Our results suggest a cognitive role for mirror neurons as a system that not only encodes the meaning of observed actions but also contributes to choosing appropriate behavioral responses to those actions.  In particular, a stimulating (although admittedly speculative) interpretation of our results is that mirror neurons not only may represent a neuronal substrate for understanding "what others are doing," but also may contribute toward selecting "how I might interact with them."

Notice that in all this I've essentially expanded the use of "concepts" to all primates possessing "mirror neurons".  This makes sense, since if the firing of a certain pattern of neurons in even one area of the brain represents an attentional focus on one particular idea, such as a class of actions, it makes a valid symbol, and symbols can be reasonably considered to represent concepts.  Language doesn't come into it.  Or rather, language came into it very late in the game, when one lineage of apes came to represent a well-established system of symbolism within the brain with something that could be easily communicated to other members of the local group. 

Thus we can see that while language is very likely (but not certain) to be a human invention, the use of symbols, and the concepts they represent, is probably much older:  language certainly added a dimension or more to the utility and effectiveness of symbols and concepts, but the original system was in place at least tens, and possibly hundreds, of millions of years earlier. 

Caggiano, V., Fogassi, L., Rizzolatti, G., Thier, P., & Casile, A. (2009). Mirror Neurons Differentially Encode the Peripersonal and Extrapersonal Space of Monkeys Science, 324 (5925), 403-406 DOI: 10.1126/science.1166818

Links: Not all of these have been called out in the text.  Use the back key if you came via clicking a footnote. 

1.  The Early Differentiation of the Neocortex:  a Hypothesis on Neocortical Evolution

2.  Genetic and epigenetic contributions to the cortical phenotype in mammals

3.  Mirror Neurons Differentially Encode the Peripersonal and Extrapersonal Space of Monkeys paywall Read more!

Encephalon 73 is Up

With three of my better (IMO) posts, along with a great line-up. Each post is accompanied by a video searched out by the editor, Sandra Kiume. See it here. Read more!

The Earliest Eumetazoan Progression

I have commented several times on the early evolution of the animals, especially in regard to their ability to handle information.  Here I want to look at the progression from a plausible common ancestor of the latest-branching clade of sponges and the Eumetazoans to the point of a plausible last common ancestor of the Ctenophores, the Cnidarians, and the Bilaterians. 

Symmetry and Development

Since, in my view, all (or most) of the animals in the sequence we're looking at had biradial symmetry, I'll start with a discussion of that.  (Especially since Wiki has only a stub on the subject). 

First, as I've mentioned before, symmetry in all animals that move in response to external directional cues must be superficial.  Even if the animal is only a sphere with sensory cells and ciliated swimming cells distributed evenly over its surface, the communications needed to coordinate its swimming with the direction of threats and food will require each cell to know its location relative to the whole.  There can be no confusion between left and right, front and back, top and bottom.  This requires a coordinate system of some sort, even if the physical morphology doesn't show it.  For a spherical surface, there are two obvious options:  radial (or angular) and multipolar. 

The radial system is like the system of latitude and longitude:  it starts with a pair of poles on opposite sides of the sphere, which we will call "oral and "aboral", named after the blastopore or (single) gut opening in these early animals.  (Sponge larvae also demonstrate this polarity in their distribution of cell types, although they lack a blastopore.)  A line between the poles (along the surface -- one through the center of the sphere is the axis) is then defined as the "zero longitude" line, after which any spot on the spherical surface may be uniquely located by its angular location relative to the poles (latitude), and its angular location relative to the "zero longitude" line.  Of course, it will still have to know clockwise from counter-clockwise:  30° longitude is very different from -30°. 

The multipolar system also starts out with a polar axis, but then goes on to define another (which might roughly correspond to 0° and 180° longitude) and then yet another (which might correspond to 90° and 270°).  any location on the spherical surface is uniquely defined by three numbers:  how far it is between each of the three pairs of poles. 

Controlling the Development of Symmetry

Now, location in animals is almost always defined in terms of the diffusion of signaling molecules, a system well supported by a good epithelium.  The tight junctions among all the superficial cells prevents these molecules from diffusing out into the surrounding medium, and the basal layer(s) can be specialized to allow much faster diffusion along than across it.  The first set of poles, then, can define "latitude" with a cluster of cells at one end releasing a diffusible signal:  latitude is known by the concentration of the signal.  ...

A more robust mechanism would have cells at the other end also releasing a signaling chemical, a different one.  Now a cell on the surface could get its latitude by sampling the relative concentrations of two chemical signals.  This is a typical system in some developing embryos, although the oral signal usually comes from a ring of cells surrounding the blastopore. 

If we try to use such a mechanism in the radial coordinate system, the "zero longitude" line would have to emit its signal in only one direction (or two signals, each in one direction), or else it would be impossible to distinguish clockwise from counter-clockwise.  (Alternatively, a separate signal could be released at a point some angle away from the "zero longitude" line, but this is becoming a hybrid with the multipolar system.) 

The multipolar system has this problem solved, at the cost of three signals (or pairs of signal chemicals).  this is, in effect, what bilaterians all use, and IMO it's likely that research will eventually discover that the Ctenophores and Cnidarians do as well. 

With all this in hand, let's look at symmetry.  Since the Cnidarian medusa forms have a well-defined radial symmetry around their oral/aboral axis, we'll start with that.  If we imagine a glove with poles, latitude, longitude, and an equator, let's break the equator into four equal sections, broken at 0°, 90°, 180°, and 270°.  We'll define a primary mirror image at each break line, so each section looks identical to its reflection in each mirror.  We'll also define a second set of mirrors intermediate to the the first, at 45°-225° and 135°-315°.  Each section, then, is identical to every other, and to its reflection across the primary mirror line.  Each section's halves are also identical but inverted across the secondary mirror line running down its middle.  This is radial symmetry with an index of four.  A simple square has this sort of symmetry.  It can be divided into four identical sections, reflected in the two mirror axes, with each section having identical but inverted "left" and "right" halves.  Note that if you divide a square into eight sections, four of them will be inverted relative to the others.  Note also that it doesn't matter which set of axes you define as primary, and which secondary:  a square can be divided into four sides (sharing corners) or four corners (each with two half-sides). 

Now, many Cnidarians have a higher index than four, such as eight, or sixteen.  It's easy to see how these body plans can be achieved developmentally.  for instance, if we start with an index of four, at each point where one of the primary planes of symmetry (reflection) intersects the equator (or some other circle of equal "latitude"), there's a small patch of cells emitting a chemical signal.  For robustness, there should be another patch at each point where a secondary plane intersects, emitting another chemical.  By sampling this signal, any cell can know where it is within the section it occupies.  Note that for coordinated control, each arm, at least, will have to know its location relative to the entire organism's coordinate system. 

How does a developing organism double its index?  At a specific point in development, a signal is released telling the cells at the secondary points to begin emitting the primary signal (instead of the secondary), and a group of cells halfway between each set (who already knew their position from the earlier signals) begin emitting the secondary signal.  Now the index is eight.  this process can be repeated as many times as needed, and it's a simple mutation to increase (or decrease) the number of repeats. 

I've described how the multipolar system could produce four poles equally distributed around the equator, if a patch of cells at each of these poles started emitting the primary signal, and cells that found themselves at the midpoints began emitting the secondary signal, you've got radial symmetry with an index of four.  But more interesting is how those four poles came to be. 

Let's start with a simple sphere with no coordinate system except a single patch of cells (somewhere, anywhere on the surface).  If these cells begin emitting a signal (different from the signals used in radial symmetry), it will diffuse around the sphere while breaking down and diffusing away (at right angles to the surface, which is presumably an epithelium capable of controlling the diffusion rates in different directions).  Thus the concentration will reduce from a maximum at the emitting pole to a minimum at its antipode.  Cells are capable of detecting a concentration gradient, the fact that there is none is enough to let cells at the antipode know that they should begin emitting the opposite signal. 

More problematical is the next pole.  Some mechanism is needed to select this pole (somewhere on the equator), various species use various methods, some of which are essentially random.  Once this pole is selected, cells here may begin emitting a new signal (still probably different from those used in radial symmetry), which diffuses around the equator and allows its antipode to form in the same way as the first.  The third pole also requires some external mechanism to distinguish between left and right, although cells equidistant between the second poles will know it.  In many species this selection is random, although mammals^[20] and everybody's favorite flatworm Caenorhabditis elegans^[21] have fairly reliable mechanisms for determining their left side. 

When it comes to radial symmetry, we've seen how four-fold symmetry can come about, but what if only two poles begin emitting the primary signal, while those at right angles to their axis begin emitting the secondary signal?  This is radial symmetry with an index of two:  biradial symmetry.  Ctenophores have a fundamental biradial symmetry, as do most Cnidarian polyps. 

(Ctenophores have imposed an eightfold symmetry on their oral end and the major expansions of their gut, but the aboral end is biradial.  (The location of the "anal pores" breaks this symmetry, creating a rotational symmetry with an index of 2, but this is a minor feature, and I'm going to class it with the giant left claws of some crabs:  a minor break asymmetry built on the basic symmetry.) Cnidarian Medusae also have a basal biradial symmetry underlying their 4-, 8-, or 16-fold symmetry.  And remember that all symmetry is ultimately superficial:  there is always an underlying coordinate system that uniquely defines each point.) 

Symmetry and Controlling the Body

When it comes to controlling the body, symmetry has an advantage in that the same behavioral program can be used for each unit of symmetry.  This applies both to the behavior of cells in the developing organism, and the behavior of units (limbs, tentacles) in the active animal.  Even when differences arise, they can be overlaid on the repeated pattern:  there will usually be many more similarities than differences, which means much less information is needed to define the entirety when symmetry is used.  It also means that mutation to the underlying pattern can change all the units at once, which has advantages and disadvantages when it comes to overlaid differences.  (But selection can take advantage of mutations that play to the advantages, while weeding out those that run into disadvantages.) 

This makes much more difference to an animal that uses muscles to make coordinated changes to its body shape than to blobs swimming around with cilia, so for the origins of Eumetazoan symmetry we need to look to the ultimate origins of muscles. 

Symmetry in the Earliest Animals

I've suggested that the common ancestor of Eumetazoans and the latest-branching clade of sponges, the homoscleromorpha, was a small globular animal like a swimming sponge:  containing internal water canals, with the porocytes spread across the front, cilia for swimming in a broad belt around the middle, and a fairly sophisticated system for controlling its activity.  What I didn't make explicit was that the osculum, the exit for water flowing through the body, would have been in the rear, so that the flows of water from swimming and feeding could complement one another, and so that oxygen-depleted water from either would not become input tot eh other.  Being roughly spheroidal, this creature's swimming actions would have been identical in any direction around its "oral/aboral" axis. 

It might seem, in these early days, that there wasn't much need for swimming, given the general lack of predators, but we need to consider the early environment:  most models of the pre-Cambrian biosphere suggest that the deeper oceans were anoxic, with only a shallow layer of oxygenated water overlying it.  With much of the productivity confined to the coastal areas, where tides and wave actions continually stirred things up, there would have been vast opportunities for collecting food in regions with substantial risk of being stranded by wave action.  this means that some ability to predict wave action and position itself so as to be washed back out in a breaking wave rather than getting stranded on a sandy beach would have given an animal a selective advantage, even for an animal that could only swim with cilia.  More predictive ability would have conferred more benefit, so we have a situation where the evolution of intelligence has a nice steep "fitness slope" to climb, even without changes to the body structure. 

In this regard, I want to discuss a particularly important paper,^[14] which is unfortunately behind a paywall:  Sponge Genes Provide New Insight into the Evolutionary Origin of the Neurogenic Circuit (by Gemma S. Richards, Elena Simionato, Muriel Perron, Maja Adamska, Michel Vervoort, and Bernard M. Degnan).  What these researchers did was identify a gene in an early-branching sponge, Amphimedon queenslandica which is a demosponge, that appears to be descended from an ancestor of many types of genes involved in controlling the development of nerve cells in the bilaterians, and presumably also the other eumetazoans.  Not only that, but they injected mRNA for the protein coded by this gene into frog and fruit fly embryos, and determined that it performed many of the neurogenic functions of its purported relative genes native to these animals.

Now in Amphimedon queenslandica this gene, called AmqbHLH1 is expressed along with a similar relative of the notch receptor genes of eumetazoans and a notch ligand, AmqDelta1, in the outer layer of cells of the early embryo.  As it develops, the embryo separates into three layers, the inner cell, subepithelial, and epithelial. 

Prior to the formation of the subepithelial layer (“spot stage”), all three of the conserved neurogenic genes are expressed in the outer layer (Figures 1A–1D), with AmqNotch expressed broadly and AmqDelta1 and AmqbHLH1 restricted to subpopulations of cells. A few hours later at the “early ring stage” (Figures 1E–1H), all three genes are coexpressed in cells of the subepithelial layer.  In “late ring embryos” (Figures 1I–1L), AmqbHLH1 and AmqNotch remain expressed in the subepithelial layer, but AmqDelta1 is now highly expressed in globular cells that are located beyond the subepithelial layer, within the outer layer.  We propose that the expression of AmqDelta1 in the globular cell population is continuous and that it tracks a specific migratory event from its initiation, when cells leave the subepithelial layer, until its conclusion, when the cells reach their final position scattered around the outer margin of the mature larva (Figures 1M–1P).^[14]

These Globular Cells appear to function as sensory cells, helping the sponge "larva" find a spot to settle and metamorphose into a small version of the adult form.

Now, I've previously suggested that when looking at larvae, we shouldn't consider them to be representative of the immediate ancestor of the adult form, but rather a specialized developmental stage, simplified in many respects for the purpose of extremely rapid growth, that may in some respects recall ancestral forms, often very distant ancestors.  I've also pointed out that in the classic definition of "larva", this form is specialized for growth, and we shouldn't assume that a form that does little but swim around and settle is similar to classic larvae.  But it's reasonable that the "larvae" of sponges are descended from a more classic version of larvae, in which case their ancestors spent some time swimming around finding and eating large amounts of food before settling and metamorphosing.

So it's plausible that these larvae used an ancestral method of controlling their swimming, harking back to a "swimming sponge" ancestor that possessed a sophisticated system of controlling its movements, combining sensation and intelligence.  The fact that remnants, quite likely far simpler than what the ancestor had, may be found in ancestral larvae makes it very plausible that the ancestor itself had something much better.  It may not have been strictly divided into nerve cells and sensory cells as is often the case in more developed eumetazoans, but that didn't mean it wasn't capable of considerable intelligence.

And these weren't just the common ancestors of the latest branch prior to the Eumetazoans:  Amphimedon queenslandica is a demosponge, a group that branched prior to the homoscleromorphs, showing that intelligence was already evolving prior to the latest branching.

What, precisely, were the active resources available to this evolving intelligence?  We know that some sponges can propagate an electro-chemical (actually electro-osmoidal) wave along their epithelia, stimulating closure of the porocytes, the latter function being present in all sponge lineages.  We also know of sponges that can expel a large proportion of the water in their canal system, although the process takes too long to be useful in emergency swimming.  (But then, sponges don't swim, so it's plausible that this function had degenerated from a faster one in swimming ancestors.) 

Speculative Reconstructions

But what if our early "swimming sponges" had a greatly enlarged osculum, such that they resembled a hollow sphere with an opening in the back and their systems of water canals and their bodies in a layer surrounding the hollow full of water?  In this case, a contraction around the equator, coupled with a relaxation at a right angle, along the "oral/aboral" lines, could have produced a large reduction in the volume of the enclose space, without reducing the surface area.  Indeed, a reduction in surface area would have been no problem, as long as a thickening of the body layer could compensate to keep the overall body volume unchanged, since the major speed impediment is squeezing the water out of all those tiny channels. 

We know, from observations of Cnidarians, that it's possible for epithelial cells to produce substantial contractions, and other changes in shape.  What makes muscles so powerful is their organization of myosin, actin, and other proteins into specialized linear structures that can shorten quickly in response to action potentials.^{[4] [5] [6]} All Eukaryote cells possess forms of myosin and actin, which they use for a variety of movements within the cell, including changing its shape and moving organelles around.  The organization of many overlapping fibers of actin and myosin into something like muscles probably constituted a smooth "fitness slope" which could be easily climbed through progressive small mutations to the organization and structure of myosins and actins in the cell.

We can start with the epithelial cells creating bundles of these overlapping fibers connecting membranes on opposing sides of the cell, with some sort of trans-membrane structures providing mechanical linkage across the pair of cell walls.  If the cells were connected by gap junctions that could propagate the electrical waves of action potentials from cell to cell, the entire skin could have contracted quickly to expel water in the oversized osculum for escape swimming.  The development from this point to the simple myotubes of Ctenophores is probably a progression of simple refinements.

A key obstacle to this sort of swimming is that there are limits to the internal flexibility of the water-canal filled sponge, which in turn produce limits to how much water could be expelled.  Although it's hard to be sure, I suspect that no more than 30% to 50% of the total volume could be made up of expellable water.  To enlarge the body cavity further, allowing for greater emergency swimming, the creature would have to give up its circular symmetry around the "oral/aboral" axis, and collapse in some way that produced a lesser symmetry.

An obvious candidate is biradial symmetry.  A spheroid can flatten into a shape roughly like a pumpkin seed, reducing its volume to a tiny fraction of the original.  But to do this, the internal skeleton (presumably much like that of small modern sponges without spicules), would have to become specialized in a biradial pattern.  The part that becomes the flat part of the "pumpkin seed" would have to be resistant to further bending, while being able to flatten out from its spherical curvature.  And the part that becomes the edge would have to be much more conducive to bending, becoming something of a hinge.

Similar biradial specializations would be necessary for the contractile cells.  Indeed, while "shrinking" a sphere could be accomplished by contracting the outer skin, flattening it would require tension from more internal cells.  If such a system evolved gradually, the end result would be lines of cells penetrating the internal structure (between the water canals) which could contract, pulling on one another, to pull the appropriate parts of the outer skin into the "pumpkin seed" configuration.  These structures would be different in different areas around the equator, in a biradial configuration. 

Note that this simple system is only possible with an index of two.  Radial systems with higher indices would require not only a convex bend in the outer skin, but concave bends.  The structure of tensile elements (primitive myotubes) would also be extremely complex.  It is highly unlikely then that a higher index of symmetry would have arisen under these circumstances.

What we have, then, is a small swimming sponge in the form of a hollow sphere, with a fairly sophisticated "brain", capable of maneuvering through the wave-stirred coastal waters where large amounts of edible detritus was available and the constant stirring of the water provided a good supply of oxygen from the air.  It probably didn't have nerve cells (in the sense of having axons carrying action potentials), rather the cells that performed calculations and communications may have looked much more like the modern mammalian astrocytes:  cells with multiple processes reaching out to all (or many of) the cells in its vicinity, having an ability to perform localized calculations and carry signals by means of "calcium waves" that could transfer from one cell to another over the electrical connections made by gap junctions.  They may well have also performed sensory functions, lacking the division into specialized cell types found in Eumetazoans.

Building the First Eumetazoans

The transition from this to the Eumetazoans almost certainly required the key transition from internal water canals and chambers lined with choanocytes to a system of mucociliary feeding similar to that seen in a huge variety of Eumetazoan larvae and many adults.  In this system, mucus is secreted from parts of the skin that are supplied with large numbers of cilia of two types:  one type stays within the mucus and keeps it moving, eventually collecting into channels which feed it into the mouth.  The other type sticks up out of the mucus, and sweeps water along the mucus covered skin, moving in a way that tends to force suspended particles (and life-forms) down into the mucus where they stick and are drawn along with it into the mouth where they are digested.

Mucus is a rather complex secretion, present in sponges as well as most Eumetazoans.  It performs important protective functions by trapping would-be invaders where they can be isolated from the underlying skin.  It is made up primarily of glycoproteins and complex sugars, well supplied with other materials secreted by the underlying cells.  The composition can easily vary by species, and many of the various mucins can co-evolve with digestive enzymes, allowing a species to secrete mucus it can easily digest but that most of the living creatures trapped in it can't break down.

The easiest path by which a swimming sponge might evolve into a mucociliary feeder is to begin with using mucus as a defensive mechanism.  Many sponges have cilia, so it's an easy adaptation to using them to move secreted mucus along the surface to somewhere that trapped would-be invaders wouldn't be a threat.  Most sponges have amoeboid cells that can feed using phagocytosis, which actually isn't that different from the process used by choanocytes when one of the microvilli around their flagellum traps a food particle.  (Indeed, there are sponges that have multinucleated aboeboids that feed on small crabs and other crustaceans with a similar process.) It's an easy adaptation for these cells to develop the ability to secrete proteins (or keep them on the outer surface of their cell membranes) that would cause the mucus to become thinner right around them, allowing them to "swim" through it and chase down, trap, and eat whatever they find caught in it.  They would also have the ability to collect large amounts of this mucus, digest it back into its basic components, and return packages of these materials into the internal matrix of the animal, where they could be transported back to the cells that secrete mucus for reuse.

The next adaptation would be to modify part of the inner surface of the osculum as a "trap" for this mucus, with the cells lining it being specialized to be resistant to attack from whatever invaders are caught in the mucus.  Alternatively, this trap might be lined with a syncytium of cells capable of surrounding and absorbing such invaders.  A further adaptation would be for the "trap" to develop the ability to close itself away from the outside intermittently, then some of the cells lining it could secrete acids or other chemicals that would alter the environment to one much more hostile to invaders adapted to the open ocean (or whatever).  This would also allow the secretion of digestive enzymes, both to break down the mucus for reuse of its components (without the effort of absorption by the amoeboid cells, and to break down the tissues of the various trapped invaders.  At this point we have a rudimentary gastric system, although it has originated as part of a protective mechanism rather than the primary method of feeding.

However, given a creature that already uses cilia to move water around for swimming, and has now developed their use to move mucus over the skin, it's another easy adaptation to modify some of the ciliary action to sweep food particles down onto the film of mucus, enhancing the ability to trap food.  At this point, it's reasonable to assume that some lineages would specialize in this process, abandoning the use of choanocytes and collared flagella.  The developmental mechanisms they had used to control the creation of water canals and choanocyte chambers would then be free to elaborate the shape of their ectoderm, providing specialized improvements for increased trapping of food with their now fully-developed muco-ciliary feeding system.

Here, then, is our fully emerged Eumetazoan.  It has biradial symmetry, uses cilia to swim, posses a blastopore, into which mucus full of suspended food is periodically swept, after which it closes so acids and digestive enzymes can be secreted into it and digestion can take place.  The lining of the digestive tract is probably a syncytium, as it is in the most basally-branching bilaterians, which may well preserve this feature from the earliest Eumetazoans.  (As I recently pointed out, both the Cnidarians and the Ctenophores are probably highly specialized, and cannot be expected to represent the early common ancestors.)

Eumetazaon Developments

Where does it go from here?  When we look at the ctenophores, we see a creature with a rudimentary sensory organ at the aboral end, two tentacles near it, and a system of (typically) eight lines of cilia running up from the oral opening towards the equator.  The Cnidarian medusa, which I've argued is the ancestral adult form of this group, has four-, eight-, or sixteen-fold radial symmetry, which as shown above could easily develop from a biradial ancestral condition (something regressed to in most of the (IMO) larval form represented by the polyp).  It's been shown by gene expression studies that the tentacles of polyps are not homologous to those of the Ctenophores, but I have an alternative suggestion.

I would propose a common ancestor with biradial symmetry, two tentacles at the aboral end used for swimming and other manipulative processes, and a set of tentacles around the mouth used primarily for mucociliary feeding.  The swimming would be for escaping wave action and possibly predators, and the location near the aboral sensory system and brain would allow faster communication.  The tentacles near the mouth would be well provided with cilia, along with mucus grooves, and normal "cruising" would be done using these.  Nerve cells would have been present (as they are in all descendant lineages), and muscle cells would have also been present, primarily in the aboral tentacles.

The progression from this ancestor to the Ctenophores is easily envisioned:  as it converts from filter feeding to pursuing and eating larger prey, the cilia surrounding its mouth become specialized for only swimming, "cruising", and they fold up around the body, producing lines of cilia spreading up from the oral end, and allowing a shorter path for messages from the brain controlling them.  The aboral tentacles, in turn, become specialized for capturing prey.  An intermediate form might have been one that supplemented its original mucociliary feeding with another type of filter feeding:  sweeping its tentacles through the water and trapping and eating whatever they encountered.  This would provide an easy evolutionary path for the development of the colloblasts.  They might well have begun as objects on the feeding tentacles surrounding the mouth, allowing them to trap any food particles they encounter, while the primary feeding method remained mucociliary.  Once they spread to the aboral tentacles, those tentacles could have begun using a sweeping process to capture objects that the oral tentacles couldn't, taking advantage of their muscles and faster responses.

Similarly, the progression towards the Cnidarians is equally easy to see.  Beginning with a similar animal, the aboral tentacles, already adapted for swimming, become duplicated, creating four, and widen towards the bell shape found in the modern medusa.  This would have started with a swimming action in which both tentacles pushed back at the same time, probably used by the original common ancestor.  Duplicating the tentacles, and widening them, would have been easy mutations, not having to occur in any specific order.  Once both had occurred, fusing them into a bell is another easy mutation.  After that, the development of tentacles hanging off the edge of the bell is also an easy mutation.  If the common ancestor had already had colloblasts, or something ancestral to them, these cells could later have become specialized for capturing active creatures with high-flow bloodstreams and complex nervous systems.  (I've discussed this progression already, in Coelenterates, Cnidarians, and Larvae.)

Getting back to the common ancestor, how did it come about?  Let's go back and start with the small spheroidal creature, with an outer covering of mucus-secreting skin and cilia to sweep this mucus back into the osculum, where it enters a primitive digestive system.  We've seen that the "swimming sponge" would have already had biradial symmetry and a sophisticated "brain" it could use for steering itself through the chaotic waters of food-filled beach areas.  Being hollow, with most of the volume enclosed by its body in the expanded form consisting of water it could expel for swimming, when it needed to escape some wave-created threat it could move quite far and fast for a very short distance.

What if, re-using the same developmental mechanisms it used to control the growth of the water-canal system, it developed a pair of tentacles sprouting from the "flat" sides (the sides that become flat when it expels water)?  These tentacles would ideally be as close as possible to the "brain" at the aboral end, and the myotubes along their length could have one end inserted into the "ganglion" that constituted the "brain", thus allowing this creature to steer itself during its escape swimming.  This mechanism might well have been present before the development of mucociliary feeding; it might even have been present in the common ancestor of the homosclerimorphs and the eumetazoans (and lost by the former as they evolved towards sessile feeding).

Given the ability to create tentacles for one purpose, it's yet another easy mutation for them to appear for another, in this case at the oral end.  If they were covered with mucociliary apparati, they would have enhanced the capture of food particles that didn't make it into the pores, because they were too far away from the line of swimming.  (Particles that were too large would have become trapped in the mucus covering the body; indeed that might well have been the primary reason for adopting mucociliary feeding as a strategy in place of simply recovering and reusing defensive resources and energy.)

An alternative model would be that the mucus flow along the body became concentrated in a pair of channels where they could flow into the osculum, around the rear edge.  This way, the mucus flow would be somewhat isolated from the flow of water, both normal and during escape swimming.  These channels could then have become supplemented by tentacles, again allowing the capture of food particles too far away from the swim line.

Once there were two tentacles, it was yet another easy mutation for them to multiply to four, eight, and even farther (as discussed above).  The more tentacles, the greater fraction of food that missed the body could be captured.

A creature with two major feeding strategies occupies an unstable position evolutionarily.  While such a life-style may be successful, even wildly successful, there is always the option for one or more descendant lineages to specialize in one and abandon the other.  Since the original strategy was a sponge like process, the progression would have been towards total dedication to mucociliary feeding, using the oral tentacles.  The cilia around the main body would have been abandoned (at least for normal swimming), since those on the tentacles would have been sufficient to capture anything in the water stream.  The hollow filled with water would also probably have eventually been abandoned, being replaced with the more efficient swimming using the aboral tentacles.  And there you have it, the common ancestor of the Cnidarians and the Ctenophores proposed above.

Now, most molecular investigations of the early ancestry of modern Eumetazoan lineages tell us that the Ctenophores branched first, with the other branch leading to the common ancestor of the Cnidarians (Coelenterates) and the Bilaterians.  The common ancestor of all three proposed above, then, would have been followed by the common ancestor of the Cnidarians and Bilaterians.  In my view, it probably looked very much like the earlier ancestor, but with a more developed nervous system.

Nerve Cells

The key to the invention of the nerve cell is the need to carry rapid messages over long distances, where muscle fibers can't do the job (because if they can there's no need for nerves, as shown above for the muscles in the early aboral tentacles, as well as some acoels, a group generally thought to be basally branching bilaterians, and thus likely representative of the early state).

We find nerve cells controlling the action of cilia in the Ctenophores, and this actually provides the most plausible explanation for their invention:  the long tentacles extending from around the mouth need their cilia controlled, especially during escape swimming.  We can see how cells originally more like astrocytes became specialized to carry a rapid action potential along their length so that they could deliver an almost simultaneous message to these ciliated cells.  Once this feature had been developed, such cells were also used for controlling muscles, allowing them to connect any two points on the epithelia (either ectodermal or endodermal) without the extra effort of extending processes to the "brain".

Note that there's probably no real need for nerve cells to control the action of the ciliated bands in Ctenophores:  the calcium waves found in astrocytes would probably be sufficient, given the overall slowness of this type of swimming.  However, if they evolved from an ancestor that used nerve cells to control the action of cilia at the end of long tentacles extending from around the mouth, this feature wouldn't have been given up, it would have simply been adapted for the need.

Thus, in this model, the common ancestor of all the modern Eumetazoans had already invented nerve cells, although their most essential use was for controlling ciliary activity.  At some time after the Ctenophore lineage(s) branched off, one group continued the development of its nervous system for more active control of its movement, perhaps extending myotubes into the oral tentacles, and developing a suite of sophisticated movement with the aboral tentacles for complex swimming movements.  Little real development of the physical form would have been necessary, in fact little development of the nervous system is really necessary:  the common ancestor of the Cnidarians and Eumetazoans might well have pretty much resembled the earlier common ancestor, the Cnidarian and Bilaterian lineages may just have branched later than the Ctenophores.

What about the progression to the Bilaterians?  Well, among the things that must have happened is a shuffling of developmental cues, as is shown, for instance, by the fact that the blastopore in developing bilaterians forms at the opposite end of the the egg from that of the others, based on the position of the polar body.  There are many other differences in how the bilaterians use the developmental genes they inherited from the common ancestors (as shown by similarities and differences with the Cnidarians).  But this is pretty much out of the scope of this post, so we'll defer further discussion for a later time.

RICHARDS, G., SIMIONATO, E., PERRON, M., ADAMSKA, M., VERVOORT, M., & DEGNAN, B.(2008). Sponge Genes Provide New Insight into the Evolutionary Origin of the Neurogenic Circuit Current Biology, 18 (15), 1156-1161 DOI: 10.1016/j.cub.2008.06.074

Links: Many of these aren't called out in the text, and too many are behind paywalls.  Use the back key if you came via clicking a footnote.

1.  Conservation of Brachyury, Mef2, and Snail in the Myogenic Lineage of Jellyfish:  A Connection to the Mesoderm of Bilateria

2.  Intracellular Fate Mapping in a Basal Metazoan, the Ctenophore Mnemiopsis leidyi, Reveals the Origins of Mesoderm and the Existence of Indeterminate Cell Lineages

3.  The Development of Radial and Biradial Symmetry:  The Evolution of Bilaterality

4.  Invertebrate Muscles:  Muscle Specific Genes and Proteins

5.  The Chemical Mechanism of Myosin-I:  Implications for Actin-based Motility and the Evolution of the Myosin Family of Motor Proteins

6.  Evolution of the Heart from Bacteria to Man paywall

7.  Amphink2-tin, an amphioxus homeobox gene expressed in myocardial progenitors:  insights into evolution of the vertebrate heart

8.  Gene Regulatory Networks in the Evolution and Development of the Heart paywall

9.  Phylogenetic relationship of muscle tissues deduced from superimposition of gene trees

10.  Anteroposterior Patterning in Hemichordates and the Origins of the Chordate Nervous System

11.  Centralization of the Deuterostome Nervous System Predates Chordates paywall

12.  The evolution of nervous system centralization

13.  Cnidarians and the evolutionary origin of the nervous system

14.  Sponge Genes Provide New Insight into the Evolutionary Origin of the Neurogenic Circuit paywall

15.  Larval and adult brains paywall

16.  The neuroendocrine system of invertebrates:  a developmental and evolutionary perspective

17.  Central neural circuitry in the jellyfish Aglantha:  a model 'simple nervous system'

18.  A Post-Synaptic Scaffold at the Origin of the Animal Kingdom

19.  Early evolution of animal cell signaling and adhesion genes

20.  The left-right axis in the mouse:  from origin to morphology

21.  A transcriptional regulatory cascade that controls left/right asymmetry in chemosensory neurons of C. elegans Read more!