development

Last week, the NY Times printed a short article by Kate Murphy marking the beginning of the National Children's Study (Official site) this coming January:

After nearly a decade of planning, researchers will begin recruiting pregnant women in January for an ambitious nationwide study that will follow more than 100,000 children from before birth until age 21.

The goal of the federally financed project, the National Children’s Study, is to gain a better understanding of the effects of a wide array of factors on children’s health.

At a total cost of $2.7 billion, the study has been controversial -- it looks like a giant fishing expedition, and its planning involved decisions not only about science but about which congressional districts would be home to study sites. In other words, it may be science but it's larded with a lot of pork. Still, as fishing expeditions go, this one has a lot more potential than many high-energy physics or space projects that have comparable budgets.

The study was conceived at a time when substantial genetic information would not have been expected. But the study has been retrofitted with genomics, to some extent. Over the 21-year duration, the cost of full genetic sampling of each study participant (and parents) will be trivial relative to the total cost of the study. They're already planning intrusive biological sampling for chemical agents:

Participating mothers and children (fathers will be encouraged but not required to take part) will be given periodic interviews and questionnaires. They will further be asked to submit samples of blood, urine and hair. Air, water and dust from their environments will also be sampled and tested.

Heck, if all the participants got 23andMe today, it would be a drop in the bucket compared to the total budget. It will be interesting to see how they alter the study protocol to include whole-genome sequencing when it becomes feasible. It shouldn't be that hard to convince a few congressmen...

As presently described, their genetic methods are sort of rudimentary -- they have the usual problem of a very large number of comparisons, and need ways to deal with it. You can believe that people who solve problems in this area will be in high demand. Today, the methods to deal with genome-wide data have to fall back on widespread tools like PHASE and STRUCTURE, which really don't solve the problems at the level of information resolution that might be available. This is an increasingly an anthropological problem, since the fine-scale information about human history and prehistory can contribute to the statistical power of association studies, if the researchers take this information into account.

Also of interest: the entire cohort will include around 3000 sets of twins.

I'm just doing some background reading about the body size of pygmies (for both obvious and not-so-obvious reasons) and I thought it worth making a note of this quote, from last year's paper by Andrea Migliano, Lucio Vinicius, and Marta Lahr:

Finally, the data presented here show that pygmy body size evolved through earlier cessation of growth, being therefore the result of changes in late rather than early stages of growth. This explains why brain growth, which is completed years before the onset of adolescence (28), is not affected in human pygmies (29). Therefore, if Homo floresiensis is a dwarfed form of Homo erectus, as proposed in ref. 29, the evolution of small body size on Flores could be understood as the life history consequence of ecological conditions in islands, such as increased extrinsic mortality rate and reduced resource availability (30); however, its small brain size and low encephalisation require the postulation of different adaptive mechanisms affecting earlier stages of development.

That's the concluding paragraph of what is a very nicely-done study of mortality and fertility in pygmy populations. It came out the during the acceleration press flurry in December, so I wasn't able to write it up at the time. It's certainly worth doing so, though.

The paper proposes that pygmy human populations are small because of a life history tradeoff. A "tradeoff" is the idea that a phenotypic change in either direction may have advantages and disadvantages, and selection may arrive at different optima in different populations.

In the case of life history and body size, both growing longer (and larger) and maturing faster (and smaller) have possible payoffs. Growing longer may have a fertility payoff, as larger size facilitates larger infants and shorter birth intervals. But maturing faster has a direct payoff of shortening the generation length -- all other things equal, an individual improves her fitness by reproducing younger.

So either younger or older maturation may enhance fitness, in some circumstances. Which will work in any given population depends on other factors -- in particular, the mortality pattern. If individuals have a high risk of death in early adulthood, delaying reproduction will be a bad strategy. In short, individuals should reproduce at 16 (or earlier) if there is a fair chance they will be dead by 25 or 30.

Naturally, everyone would rather live longer. But assuming that people can't control when they die, the only way to insure their fitness is to reproduce earlier.

This hypothesis, presented by Migliano et al., is about the proximate mechanism of evolution. The authors seem content to rely on traditional hypotheses about locomotion, nutrition, and thermoregulation to explain the ultimate causes of small body size -- "ultimate" in the sense that these may be the environmental causes of high mortality:

If our hypothesis is correct, the causes of the extremely high mortality rates among human pygmies need to be explained. It is here that the traditional hypotheses explaining the small body size of pygmies may prove useful. Although the challenges posed by thermoregulation, locomotion in dense forests, exposure to tropical diseases, and poor nutrition do not account for the characteristics of all pygmy populations, as pointed out by Diamond (5), they may jointly or partially contribute to the similarly high mortality rates in unrelated pygmy populations. We argue that the small body size of African and Asian pygmy populations evolved independently as a case of evolutionary convergence, resulting from a life history tradeoff between the fertility benefits of larger body size and the costs of late growth cessation under the circumstance of significant young and adult mortality.

The demographic data presented in the paper are sobering -- particularly the low survivorship values for pygmy populations across late childhood and early adulthood. However, I wonder how much of the early adult mortality in the pygmy demographic data is attributable to new pathogens. These are certainly important today, but they would not have been during most the time that small body size was being selected in these groups. On the other hand, ancient endemic pathogens and parasites also may contribute to those mortality numbers, and these might well have occurred at higher intensities in forest peoples across their histories.

References:

De Souza R. 2006. Body size and growth: The significance of chronic malnutrition among the Casiguran Agta. Ann Hum Biol 33:604-619. doi:10.1080/03014460601062759

Migliano AB, Vinicius L, Lahr MM. 2007. Life history trade-offs explain the evolution of human pygmies. Proc Nat Acad Sci USA 104:20216-20219. doi:10.1073/pnas.0708024105

Last year's New Yorker piece on retroviral inserts in the human genome made some of my readers curious -- could such retroviral DNA be involved in recent human evolution? I think it's fair to say that I've been asked about retroviruses almost as much as about blue eyes -- and that's saying a lot!

Matt McIntosh has written a nice short piece describing what we know about retroviral genes and placental mammal evolution:

A significant chunk of our DNA had its origins as retroviral DNA. Most of these are now inactive, but a tiny portion actually appear to still code proteins. It's been found in mice, sheep and humans (and presumably generalizes to all placental mammals) that a particular kind of endogenous retrovirus is highly expressed in the outermost layer of the blastocyst (see e.g. Venables et al. 1995 for the human example). Furthermore, when you inhibit the expression of these genes the result is uniform spontaneous abortion immediately following implantation (Dunlap et al. 2006).

Most retroviruses are immunosuppressive, the most infamous example being HIV. Connecting the dots, it's quite plausible that these particular ancient retroviruses have been recruited into the mammalian genome and serve as local immunosuppressors in the uterus during development. In fact, we already know that syncytin, a protein crucial in placenta formation, is the product of a retroviral gene (Knerr et al. 2004), so there's nothing at all far-fetched about this.

If all this pans out, it stands as one of the most important cases of lateral gene transfer in eukaryotic evolution, with early mammals possibly accreting genes from many different viral lineages. As McIntosh points out, these genes are not acting as viruses now; they are imports into our genome -- just like most ancestral mitochondrial proteins are now nuclear genes. McIntosh ends with a short list of retroviral-origin genes that may be active during human development.

This is too weird:

Thus when dogs were attracted to something, including a benign, approachable cat, their tails wagged right, and when they were fearful, their tails went left, Dr. Vallortigara said. It suggests that the muscles in the right side of the tail reflect positive emotions while the muscles in the left side express negative ones.

That's from a NY Times article by Sandra Blakeslee. The whole article's about this dog tail-wagging emotional asymmetry.

And then there is all this:

Honeybees learn better when using their right antenna, she said. Male chameleons show more aggression, reflected as changes in body color, when they look at another chameleon with their left eye. A toad is more likely to jump away when a predator is introduced to its left visual field (right brain/fear). The same toad prefers to flick its tongue to the right side when lashing out at a cricket (left brain/ nourishment).

Chicks prefer to use their left eye to search for food and right eye to watch for predators overhead, Dr. Rogers said. But when chicks are raised in the dark, they do not develop normal brain asymmetry. In trying to eat and watch for hawks overhead, such nonlateralized chicks become confused and vulnerable to attack.

Now that's one messed-up experiment. Chicks raised in the dark, suddenly put out in the open where hawks are circling overhead.

Hmmm:

And left-handed chimps are more fearful of novel stimuli than right-handers. Their dominant right brains may make them more cautious.

The article ends with a bunch of adaptive-sounding explanations for asymmetry and lateralization of "approach and withdrawal" traits, but nothing very convincing. Personally, I would guess the mechanism is essentially like gene duplication: you get two copies of something, and one of them may mutate to take on new functions. Lateralization should be favored as a pathway above functionally redundant brain structures.

But then, there seems to be incredible plasticity to much of brain development, including lateralization in humans. Maybe lateralization in humans has high plasticity because enlarged human brain sizes are comparatively recent -- there hasn't been a lot of time for the evolution of functional lateralization in the new volume of the neocortex. As it becomes clearer what is new and what is old in the human brain, there will be the chance to test hypotheses about the origins of lateralized functions.

Regular readers of the blog will remember previous occasions when I have written about dental development in fossil humans. I am by no means an expert on the topic of dental development. I don't use a scanning electron microscope, or micro-CT equipment. I can recognize perikymata and striae of Retzius, but I've never counted them. I am perfectly willing to accept the idea that other people count them accurately, and even that they can determine their periodicity (that is, how many days of development each line represents).

In 2005, Guatelli-Steinberg and colleagues showed that the variation in perikymata counts for the anterior teeth of different human populations is more extensive than the differences between living people and fossil humans. I discussed that paper at the time. The perikymata counts in modern human populations are so variable, that the variation in sample means encompasses almost all fossil humans. As I noted, there are few fossil exceptions -- KNM-WT 15000 being the most important. What's worse, the variation among living people encompasses most australopithecine teeth.

To me, this was the end of the story of tooth development and maturation rates in early humans. Modern human variation encompasses most australopithecines? End of story.

So I was surprised to see last week's paper by Tanya Smith and colleagues (2007) claiming that the Jebel Irhoud 3 dentition was the earliest example of "modern" human dental development. It seems pretty clear from Guatelli-Steinberg's work that there is no modern human pattern of enamel formation.

The paper deals with this problem in a surprising way. It just doesn't talk about any of the work showing extensive variation among living people!

Still, the data are clearly there, reported in Table 2, where it is obvious that there is no significant difference between Neandertals and the modern samples. Moreover, there is no significant difference between Neandertals and Jebel Irhoud 3, except for the lower canine perikymata number, which is even more different between JI3 and the recent Africans!

The real story of the paper seems to be that Jebel Irhoud 3 has an unusually long period of enamel development compared to most recent people, and also compared to Neandertals and other early humans. But since humans vary in these traits between populations more extensively than fossil Homo, this observation demands an adaptive explanation, not a phylogenetic one.

References:

Smith TM, Tafforeau P, Reid DJ, Grün R, Eggins S, Boutakiout M, Hublin J-J. 2007. Earliest evidence of modern human life history in North African early Homo sapiens. Proc Nat Acad Sci USA (online early) doi:10.1073/pnas.0700747104

Lampl M, Mann A, Monge J. 2000. A comparison of calcification staging and histological methods for ageing immature modern human specimens. Anthropologie (Brno) 38:51-62.

Guatelli-Steinberg D, Reid DJ, Bishop TA, Larsen CS. 2005. Anterior tooth growth periods in Neandertals were comparable to those of modern humans. Proc Nat Acad Sci USA 102:14197-14202. doi:10.1073/pnas.0503108102

Guatelli-Steinberg D, Reid DJ, Bishop TA. 2006. Did the lateral enamel of Neandertal anterior teeth grow differently from that of modern humans? J Hum Evol 52:72-84. doi:10.1016/j.jhevol.2006.08.001

Dean C, Leakey MG, Reid D, Schrenk F, Schwartz GT, Stringer C, Walker A. 2001. Growth processes in teeth distinguish modern humans from Homo erectus and earlier hominins. Nature 414:628-631.

Ramirez Rossi FV, Bermudez de Castro JM. 2004. Surprisingly rapid growth in Neanderthals. Nature 428:936-939. Full text (subscription)

The introduction of game theory into evolutionary biology is often credited to George Price and John Maynard Smith. This is for good reason; together they were able to generalize Hamilton's (1967) work on parental investment strategies. By doing so, they provided an account of the evolution of variant strategies of many kinds from a gene-centered perspective.

Before their landmark contribution, there had been earlier forays attempting to integrate a game theoretic perspective into evolutionary terms. Hamilton's own work was immensely important, since his "unbeatable strategy" concept was a clear precursor of the ESS concept. Additionally, we should include the series of papers by Richard Levins (e.g., 1963), which considered the optimum adaptive solutions for various problems relating to spatial and temporal changes in the environment. These didn't explicitly involve the terminology of game theory, but dealt with the mathematical conditions under which variant strategies would pay off.

But the earliest major paper was Richard Lewontin's "Evolution and the Theory of Games," published in 1961 (and presaging Maynard Smith's own 1982 book of the same title). This paper introduced the concepts of game theory to many biologists, and some of them started playing with the ideas in interesting ways that weren't ultimately integrated into the later development of evolutionary game theory.

Waddington on game theory

One of these interesting early efforts is a short paper by C. H. Waddington (1965), which served as an introduction to a symposium on the evolution of colonizing species. Waddington discussed Lewontin's 1961 paper in some detail, and used it to frame the problem of colonizing versus noncolonizing species. He took these two alternatives as possible strategies that a species might adopt in its contest against Nature.

This is an unusual formulation from the perspective of later evolutionary game theory, and reminiscent of "good of the species" Wynne-Edwards-type thinking, but Waddington lays it out very clearly:

In the "evolution game" which it is playing, a species has to contend with unforeseen eventualities which the future may bring -- a new parasite, a new predator, possibly an Ice Age. Another element of uncertainty arises from the fact that there may be several different ways in which the species makes a place for itself within the whole ecological network available for its exploitation -- it could change its food habits or length of life cycle, or it could migrate to another locality, and so on. The game it is playing is perhaps best formulated as a zero-sum three-person game, the players being (1) the species or population under consideration, (2) the whole environment, organic as well as inorganic, that impinges on that species, and (3) the bio-system that would occupy the living sace of first player, if it were eliminated. This third player may include species which are also involved in the second player, but by formulating the game in this way, the third player is reduced to a dummy whose only function is to absorb the gains and losses of the first player; in this way we retain the advantages of dealing with a zero-sum game and only have to consider the moves of two players, the species and Nature (Waddington 1965:2).

In the next sentence, Waddington defines the "score" of the game as the number of offspring produced by the first player in the succeeding generation, which of course is easily scaled to the population mean fitness. In my mind, this shows the "game theoretic" description here to be a conceit, since he is not really describing a situation different from the ordinary assumptions of population genetics. Indeed, his description of the "third player" is entirely superfluous from this point of view.

But I find the conceit illuminating, because it reminds us that there are other species there to absorb Nature's gains. A species must compete in reproductivity at a high level due to these interspecific interactions, or it will not last. Later in the book, Lewontin describes some models where the typical viability fitness of the mean genotype is far less than unity, which of course means that the fertility of these genotypes must be very high, indeed, for them to manage to survive. These are only modeling questions, but the possibility of losses against the field are important to the models.

He goes on to describe the game as an interdemic process, in which different populations within a species may adopt different strategies:

A population has, of course, no intelligence of its own which would make it possible for it to choose which move to make, i.e., to adopt a strategy. But no large population is fully panmictic; it is always broken up, if only by distance, into a number of smaller subpopulations which are partially independent in genotype. Each subpopulation will make a somewhat different move, some of which will be more successful and others less; a global or "Monte Carlo" strategy will emerge as that sequence of moves that has proved most successful up till the stage the game has reached. As we shall see, there are really many different games going on simultaneously, affecting different levels of individual and population organization, and each game elicits a corresponding strategy (Waddington 1965:2-3).

The point of his paper is to suggest that colonizing may be a strategy that is adaptive under some circumstances and not in others. The theme is developed later in the volume by Edward O. Wilson, Ernst Mayr, and Lewontin, and I may post a bit on those contributions later.

What I found provoking in Waddington's paper was this passage:

At a fundamental biochemical level, there are alternative strategies possible in the organization of the genetic control of enzyme seqeunces. Consider a metabolic pathway in which successive steps are catalyzed by enzymes P, Q, R, S, T, .... As Kaeser (1963) has pointed out, in some cases it is found that one of these enzymes, say R, is rate-determining for the whole sequence of steps, the throughput being highly dependent on the quantity or activity of R, but little affected even by considerable changes in the activities of the other enzymes; in other metabolic pathways, all of the enzymes may have more or less equal importance in controlling the over-all flow through the system. If the first strategy is adopted, the system is little affected by mutations or environmental effects controlling the nonrate-determining enzymes, but is very sensitive to effects on R; with the second strategy, the system is affected somewhat by mutations or other influences on any of the enzyme proteins, but is not affected drastically by any of them. The second would therefore seem to be the Minimax strategy, but a species might often be able to get away with the first gambit, in which it would only rarely suffer any loss of efficiency, at the expense of failing completely in a few individuals (Waddington 1965:4).

With this "first strategy", Waddington is describing a strategy for developmental robusticity: resistance to alteration in the developmental program due to alterations in the genetic background. For example, some developmental programs continue to generate adaptive outcomes even if there is a knockout mutation in one of their essential genes. We could say that these systems "degrade gracefully," so that many kinds of mutations lead to phenotypes that are not markedly reduced in fitness. Yet a few of the key genes in most systems cannot tolerate such changes. These developmental programs have evolved in such a way that reduces the impact of most mutational variants in their essential genes, but has emphasized the impact of others.

Now, this kind of structure might be a necessary consequence of genetic and developmental networks. Maybe it just isn't possible to build a genetic system like Waddington's hypothetical every-gene-equally-crucial example.

But the current trend in evo-devo is to propose that such network structures (so called hub-and-spoke networks) are themselves selected based on optimizing some biological property, such as modularity or reliability. Optimality theory and game theory are closely conceptually related to each other -- Maynard Smith was a central figure in the introduction of both to evolutionary biology -- but few studies of developmental processes seem to have explicitly focused on the idea of alternate developmental strategies.

Switches, canalization, and genetic variation

Waddington is best known for his concept of developmental canalization (I posted a quick review of the topic early last year). In this paper, he suggests canalization as one of a set of four developmental strategies that might be adaptive in different environmental contexts:

In order to meet the demands of differeing environmental effects on development, and on selective pressures, a species has, in general, to preserve considerable genetic variation within its populations. But this variation can be deployed in a number of ways: (a) The species can become very good at producing one particular phenotype under almost any circumstances, relying upon the environment always offering a possibility for this phenotype to get by. This leads to the evolution of systems of developmental canalization of the phenotype...

In other words, genetic evolution tends to reduce the effect of environmental variance on the phenotype. That insensitivity to environmental (and background genetic) variability is canalization.

...(b) The species can become good at doing one or another of a few alternative things. This leads to switch mechanisms between canalized phenotypes, e.g., in species which have hot and cold weather or aquatic and terrestrial forms. (c) The species can allow the environment to have a strong influence on individual ontogeny, provided it is ensured that the environmental modifications are toward the selection optimum for that particular environment. This leads to the evolution of developmental systems which are highly adaptable. (d) The species can have a development which is relatively unaffected by normal environmental variations, but in which most genetic changes come to phenotypic expression, and can rely on its wealth of genetic variation always to throw up some phenotypes near the selection optimum. This leads to systems in which there are considerable random or periodic changes in the gene pool from time to time, but little genearl long-term movement in any particular direction (e.g., fluctuations in inversion frequencies according to season, as in some species of Drosophila (Waddington 1965:4-5).

This list is worth remembering: (a) canalization, (b) developmental switches, (c) environmental variance, (d) genetic variance.

I did a little noodling around and found that a few people have followed up on this idea that developmental robusticity versus plasticity may be treated in a game theoretic perspective. For many purposes, the benefits and drawbacks of a given developmental program may be examined without reference to the idea of strategies. Still, plasticity itself is presumed to be adaptive to changing environments, so that the system of benefits and drawbacks in particular environmental contexts (and their frequency) may be usefully considered in ESS terms. Some have picked up on this analogy and mentioned the relation between a plastic developmental program and a "mixed strategy" ESS solution.

Lively (1986) considered the case of "developmental switches" in a game theoretic context. Picking up on the work of Levins (1963) and Levene (1953), Lively examined the circumstances under which organisms may adapt a stress-tolerant phenotype. Such phenotypes may be adaptive to low-resource environments, or cold, or high-predator environments. The possibility of such stress-tolerant phenotypes presents some complexities for interpreting

If the inducing cue [in the environment] is highly correlated with the harsh patch and rare in the benign patch, a conditional strategy can be stable over a wide range of patch frequencies, and this range increases with increasing cost to the stress-tolerant morphology. Hence, a change from one patch type to the other over geological time could result in a correspondingly "rapid" change in morphology without speciation or even any genetic evolution. This would happen without a trace of intermediate forms. Care must be taken, therefore in interpretation of the fossil record when developmental conversion is suspected to be an alternative to strict genetic determination of morphology (e.g., Reyment 1982) (Lively 1986:569).

The relevance of such stress-tolerant phenotypes might seem to be clearer for short-lived, high-predation animals than for hominids.

But there are obvious applications of the idea of developmental strategies in human evolution. For one thing, the maturation time is a prime target of research into fossil humans. A long series of papers has been devoted to uncovering whether Neandertals developed on the schedule of modern humans or some other (presumably more ape-like) schedule. Only recently has this literature brought in the substantial variation in dental development time among recent human populations.

As yet, the subject of nutrition-induced variation in development time has not been a major topic in papers examining skeletal development in Neandertals or other early humans. The normal phenotypic response to developmental stresses in humans is to elongate the developmental span, delaying maturation and/or truncating body size. The relevance of stress-tolerant phenotypes is reasonably clear in this context.

Lively also elaborates on the game-theoretic properties of such a system, including a surprising observation about variant strategy morphs:

The present study also shows that interactions among morphs are required for a mixture of unconditional strateies (i.e., genetically determined polymorphism) to ba an evolutionaily stable state of the population. Hence, we have the apparent paradox that, in the absence of mutualistic effects, genetically determined morphs must compete in order to coexist. This result is analogous to results gained from genotypic models, which show that density dependence is required for the maintenance of allelic polymorphisms (Maynard Smith 1962, 1970; Anderson and Arnold 1983). The competitive interactions within and between morphs may be completely symmetrical (all e_ij = e), provided there is some cost associated with the stress-tolerant morphology [if the stress-tolerant morphology had no costs, it would be the only ESS]. Asymmetrical competition that favors the nontolerant morph in the benign patch further increases the range of patch frequencies over which genetically determined morphs may coexist, but this region is narrow even under hte best of conditions. This narrowness may explain why so few genetically determined polymorphisms are observed amon randomly dispersing organisms (Lively 1986:569, emphasis mine).

I also found some work that places development into the perspective of another of my current interests, information theory. Thomas Getty (1996) suggested that developmental plasticity may be interpreted as a signal reception problem. An organism will maximize its fitness if it can adopt the pattern of development that is most adaptive to the environment in which it lives. If we consider a population in which individuals may find themselves in two environments with different requirements, then a plastic developmental program might allow individuals to develop in the way appropriate to one of these environments. This is the classic problem also treated by Levins with relation to environmental heterogeneity. Under certain patterns of different environments, a population may optimize its fitness by retaining or evolving plasticity.

Getty points out that a plastic developmental program with conditional expression of different phenotypes requires some way to detect which environment the organism is in:

The genotype, in effect, discriminates among possible environments on the basis of cues. Although it has long been reconized that the evolution of phenotypic plasticity hinges on the availability of reliable cues (Levins 1963; Lively 1986), most recent analyses do not explicitly consider the role of cue discrimination (e.g., Houston and McNamara 1992; Kawecki and Stearns 1993; de Jong 1995; Via et al. 1995). In contrast, Moran (1992) focuses on the role of cues and concludes that they are a dominant factor limiting conditional developmental switching. At the heart of her analysis is a probabilistic relationship between (proximate) environmental cues and (ultimate) environmental quality within generations. This probabilistic relationship suggests that "reliable cues" are like "noisy signals" in signal detection theory (SDT). In both cases, there are risks that a response will not correctly match the ultimate conditions. I want to show that it is useful to think of this aspect of phenotypic plasticity as a signal detection process (Getty 1996:378).

The term, "bet-hedging" comes up frequently in these kinds of considerations. Sometimes organisms simply don't have access to high-quality (i.e., minimal noise) signals of their environments, at least not at the important stages of early development when significant phenotypic choices must be made. But the higher the fitness payoff from betting correctly on a phenotype-environment match, the higher the risk an organism should be willing to take on the basis of its necessarily limited information.

Predicting the future

Of course, the value of better information-processing mechanisms is clear: if an organism can predict its environment with more certainty, then it can adapt with greater plasticity because the risk of a poor match between phenotype and environment will be greatly reduced.

This relation comes up again and again from the consideration of phenotypic plasticity and environments. Generally, phenotypic variation is adaptive to more predictable environments.

Sound counter-intuitive? Surely, it seems that the way to adapt to a more variable environment is with a variable phenotype?

Indeed, not so. Phenotypic variation is just as likely to make an organism less adapted to a varying environment as more adapted. This is worse than a wash if the environment is unpredictable. The best that selection can do in an unpredictable environment is to minimize heritable (i.e., the genetic component of) phenotypic variation. This is purely a loss-cutting measure, since in generations where the environment is very different from the maximally adapted value, the population fitness will tank. Still, a variable population would be worse, because much of a phenotypically variable population will do poorly even under the mean environment!

Levins (1963) shows that a more predictably changing environment allows another response. In such an environment, the presence of phenotypic variation can allow selection to track environmental changes. So predictability is the key to adaptability by selection.

Levins considered the case where the environment was predictable because it was temporally autocorrelated -- in other words, one generation's environment predicts the next. We may instead consider predictability that emerges from signals available in the environment. An organism that can detect such signals has a way to maximize its adaptation -- choosing the phenotype that is most adaptive to the current environment.

In terms of Waddington's four developmental possibilities; Levins is testing two of them: the canalized phenotype versus the phenotype with substantial genetic variance.

As Getty describes, the signals that would permit an organism to choose between these strategies are typically noisy: they entail substantial errors of reception. You might bet on a cold year because the groundhog sees its shadow, but how often is the groundhog right, really?

It is an open question whether human intelligence once enhanced fitness by better reading the signs that predicted future environments. I think this is unlikely because there is a scaling problem -- take an organism with a lifespan as long as a human, and try to predict the course of the environment in a given area over that timespan. It's certainly beyond me.

But one argument is that human culture really constitutes Waddington's option (c): human behaviors are extensively induced by the environment, allowing a "highly adaptable" response to changing environments.

Information about the environment may smooth the fitness function, so that a given amount of environmental fluctuation presents a smaller fitness cost. This could occur either because information reduces mortality (allowing individuals to survive immediate shortfalls), or because it permits higher fertility. Both are intimately related to energy (how much food is available), nutritional ecology (how much protein is available), and group structure (how many mates are available).

This implies a certain kind of ecology for ancient humans, one with some surprising correlates. More on that later.

References:

Getty T. 1996. The maintenance of phenotypic plasticity as a signal detection problem. Am Naturalist 148:378-385.

Hamilton WD. 1967. Extraordinary sex ratios. Science 156:477-488.

Levene H. 1953. Genetic equilibrium when more than one ecological niche is available. Am Naturalist 87:331-333.

Levins R. 1963. Theory of fitness in a heterogenous environment. II. Developmental flexibility and niche selection. Am Naturalist 97:75-90.

Lewontin RC. 1961. Evolution and the theory of games. J Theor Biol 1:382-403.

Lewontin RC. 1965. Selection for colonizing ability. Pp. 77-94 in The Genetics of Colonizing Species, Baker HG, Stebbins GL, eds. Academic Press, London.

Lively CM. 1986. Canalization versus developmental conversion in a spatially variable environment. Am Naturalist 128:561-572.

Maynard Smith J, Price GR. 1973. The logic of animal conflict. Nature 246:15-18.

Waddington CH. 1965. Introduction to the symposium. Pp. 1-7 in The Genetics of Colonizing Species, Baker HG, Stebbins GL, eds. Academic Press, London.

I posted about the "Sherlock Holmes theory of mind" last month, which I often mention to my classes. The idea is that the mind has a limited (and small) capacity, so that filling it with useless information takes away space that could be better devoted to useful knowledge. The opposite number to the "Sherlock Holmes theory", naturally, is the "Einstein theory of mind" -- namely, the idea that the ordinary human uses only 10 percent of his or her brain.

At the outset, I should point out that the Einstein story is a total urban myth, which lately has been used to great effect by psychics, self-actualization seminar leaders, and various other charlatans. There is no record that Einstein ever wrote or said anything about the useful percentage of his or anyone else's brain.

Neuroscientist and skeptic Barry Beyerstein (1999) traced the myth ultimately to the "New Thought" movement, which "blossomed following the U.S. Civil War among the prosperity-obsessed yet anxiety-ridden middle classes" (Beyerstein 1999:6, paraphrasing Meyer 1965). Popularizers of the idea ranged from devotees of numerology to self-help guru Dale Carnegie, who himself cited William James for the idea. Beyerstein himself investigated whether there is any truth to the Einstein story (there isn't), and with some assistance was able to track down the idea in the text of William James' public lectures.

But despite the fact that the myth itself is bunk, various neurologists have from time to time advanced evidence to support this myth. I'm writing a bit about this, because I've been thinking about the context of the LB1 brain and the hypothesis that it might have had "advanced" capacities. It is obvious that natural selection could reduce the size of the human brain by half or more with functional loss -- this would simply be a reversal of the Pleistocene evolution of brain size. The basic question is whether natural selection could reduce the brain size of a hominid population to half or less, without reducing some cognitive capabilities. Is it possible to build a leaner, meaner brain?

Should we have a strong opinion about this? So much about the brain is unknown, that the hypothesis may simply be untestable. How could we demonstrate that a population with hobbit-sized brains could not have been just as cognitively adept as some modern human group? It is a daunting question to try to answer. I'm not going to try to answer it here.

What I do want to do is give an account of some of the examples from the neuroscience literature that people have used to support the idea that brains could evolve to be smaller without functional compromise. Many distinct conditions lead to small brain tissue volume, including hydrocephalus, microcephaly, and deliberate hemispherectomy. A number of studies have claimed that people with profound reductions in brain volume -- down to as little as 150ml -- nevertheless have entirely normal cognitive function. This would be a real-world manifestation of the 10 percent myth: a person using literally 10 percent of the average brain volume to live an ordinary life.

But the research in this area is essentially anecdote leavened by CT and psychometric results that might -- or might not -- show what they are proposed to demonstrate. I'm going to focus here on two examples, the work of John Lorber on profound reduction in brain volume associated with hydrocephalus, and hemispherectomy. There are several others that deserve some treatment, including clinical microcephaly presenting with normal intelligence, although in many such cases we are merely looking at unusually small brain volumes and not reductions to half or more of the average size. The examples I'm examining here are some of the most extreme claims of cognitive performance with minimal brain size.

I should mention some caveats at the outset. Most cases of pathology are not as extreme in their effects on brain size as the exceptional cases that have sometimes been cited. For example, the majority of people diagnosed with hydrocephalus actually have only a small reduction in brain volume as a result of slight increase in size of the fluid-filled ventricles. Hydrocephalus is an eminently treatable condition, and many patients have no cognitive deficits at all -- even those for whom the proper treatment is to do nothing. Moreover, there is no debate among neurologists that the mind can sometimes recover, heal, or form around devastating anatomical challenges. The cases reviewed here are extreme ones, where brain volume is reduced to a fraction of its usual size.

Also, it is hard to avoid using the term "normal" in the context of pathology, but we should recognize that "normal" includes a substantial degree of variability. There is no single concept of normalcy applicable to human cognition. The best we can do is apply psychometric and performance measures to samples of people to assess the characteristics of human variability. Hence, when someone asserts that an individual has "normal" cognitive performance, it is far from obvious what they mean. Does it mean that they fit within 2 standard deviations of the mean? Does it mean "average"? With these conditions that often manifest during early development, "normal" often means within some specified distance of the average development expected for a given age. But someone with considerable cognitive deficits may nevertheless be termed "normal" in respect of some developmental scale -- for instance, "normal" when accounting for a 2-year developmental delay.

So, we must approach the idea of "normal" cognition with some skepticism. From an evolutionary point of view, the only "normal" that matters is respect to fitness within a population. And there remains no well-defined connection between cognition and fitness at all, beyond the evidence of our current cognitive adaptations as the result of past selection. This is another area in which our hypothesis is ill-defined, making it very difficult to test.

John Lorber and hydrocephalus

The most well-known neurologist who argued that brain size could radically shrink without functional compromise was John Lorber. Lorber's work with patients of hydrocephalus received substantial public attention, including a documentary film and a profile by writer Roger Lewin in Science. Lorber studied hundreds of cases of hydrocephaly, but the value -- or lack of value -- of his evidence is illustrated by a single anecdote:

"There's a young student at this university," says Lorber, "who has an IQ of 126, has gained a first-class honors degree in mathematics, and is socially completely normal. And yet the boy has virtually no brain." The student's physician at the university noticed that the youth had a slightly larger than normal head, and so referred him to Lorber, simply out of interest. "When we did a brain scan on him," Lorber recalls, "we saw that instead of the normal 4.5-centimeter thickness of brain tissue between the ventricles and the cortical surface, there was just a thin layer of mantle measuring a millimeter or so. His cranium is filled mainly with cerebrospinal fluid" (Lewin 1980:1232).

Much of the apparent "surprise" in this case owes to the presumably small total volume of the brain, and the cerebrum in particular. Lorber interpreted the small cortical volume coupled with normal -- or even "superior" -- cognitive performance as especially surprising.

Let's take this claim part by part. What exactly is surprising about it?

1. The allegedly small cortical thickness: Medical CT scans, particularly those taken during the 1970's, do not have the resolution sufficient to accurately measure tissue thickness down to submillimeter values. A millimeter is about the limit of the resolution. A phrase like "measuring a millimeter or so" should therefore be taken generously: the cortex is very thin, possibly at the limits of detection for the equipment.

Even so, no CT or MRI images I have seen of hydrocephalics -- an admittedly small number -- have shown a cortex that is uniformly thin. The enlarged ventricles reduce the cortical volume by hydrostatic pressure, but this pressure is not uniform around the entire cortex circumference. A single thin layer of tissue would require an extraordinary mechanism to attain. In this and some other of Lorber's patients, the hydrocephaly apparently had an onset later than suture closure, so that the enlarged ventricles did not have a major effect on cranial circumference. This itself is an unusual etiology, but consider what this story omits. What about the size of noncortical brain structures, including the cerebellum? What about the distribution of thickness of the cortex? Are there regions that are thinner than others? It is hard to interpret the "millimeter or so".

The cerebral cortex of a "normal" individual only averages 2mm thick. With a total surface area of around 880cm², this leads to a total cortical volume of only 191ml, again for a normal individual. The impressive thinness of the cortex comes from its internal structure -- organized in humans as in most mammals with only 6 layers of neurons. Hydrocephalus mainly decreases the volume of the white matter, composed of myelinated axons connecting brain regions to each other. White matter damage is the main cause of long-term cognitive deficits resulting from hydrocephalus (discussed a bit more below), but a substantial degree of white matter damage is possible in many brain pathologies (including Alzheimer's) with cognitive impairment that is either limited in extent or limited to a few functions.

2. High cognitive performance with low cortical volume:

Consider this passage from Lewin's (1980) review:

Lorber divides the patients into four categories: those with minimally enlarged ventricles; those whose ventricles fill 50 to 70 percent of the cranium; those in which the ventricles fill between 70 and 90 percent of the intracranial space; and the most severe group, in which ventricle expansion fills 95 percent of the cranium. Many of the individuals in this last group, which forms just less than 10 percent of the total sample, are severely disabled, but half of them have IQ's greater than 100. This group provides some of the most dramatic examples of apparently normal function against all odds (Lewin 1980:1232).

No one can dispute that the brain is capable of amazing feats of repair and reorganization, which sometimes permit normal function in the face of profound pathology. But the notion that "half" of the patients where ventricle expansion is greater than 95 percent of the cranium have IQ's greater than 100 is mathematically implausible. The definition of IQ is that the mean is 100. This means that only half of people without ventricle expansion have IQ over 100. Lorber seems to have claimed that the most severe cases of hydrocephalus actually see an increase in the proportion of high-IQ individuals, despite "many" being severely disabled. I'm not saying it's impossible, but like "a millimeter or so," this is the kind of statistic that deserves skepticism.

3. "Non-pathological" pathology: Lorber was involved in the production of a TV documentary film based on his research, titled, "Is Your Brain Really Necessary?" Beyerstein (1999) gives a good discussion of the implications of the documentary and its importance in perpetuating the myth that brain size is mostly superfluous:

This program, created by the British producer/director Hilary Lawson and narrated by Michael O'Donnell, is replayed regularly throughout the English-speaking world, because of its striking and counterintuitive contents. Given the deliberately provocative title, "Is Your Brain Really Necessary?", the telecast employs the ever-popular theme of a brave outsider struggling against a mulish establishment to suggest that, once again, the so-called "experts" aren't as bright as they think they are. Along the way, the program encourages the misapprehension that there is a huge reserve of unnecessary brain mass that can be casually dispensed with (Beyerstein 1999:14).

There is a quite obvious selection bias in these cases. Lorber identified and publicized them precisely because they did not present with profound cognitive deficits.

Consider an analogy: take a large sample of high-speed rollover auto accidents and study all the victims who received no injuries requiring hospitalization. This sample of victims is a large set, although it is a small minority of the total number of victims. Now, what conclusions will we draw from our set of low injury accident victims? Perhaps we will conclude that seat belts actually increase risk of injury, because uninjured victims were preferentially thrown clear of the crash. Or perhaps we will conclude that swerving to avoid hitting a squirrel is better than running it down, because rollover accidents present no significant risk of injury. Whatever we conclude, the biased sample is likely to mislead us, particularly if we do not recognize the direction of the bias.

We can sympathize with the purpose of this publicity: to show that hydrocephalus is a condition that can be successfully overcome. There is abundant clinical evidence showing that early treatment of infantile hydrocephalus often results in completely normal cognitive functioning in older children and adults, with only slight average deficits. The persistence of deficits often is attributable to other related conditions, such as spina bifida, which can cause hydrocephalus by interfering with cerebrospinal fluid circulation. Some cognitive deficits seem to be attributable to reduced corpus callosum size, one aspect of white matter reduction (Fletcher et al. 1992; 1996).

White matter pathology is simply not the same in its effects on brain functions as gray matter pathology. The ability of the brain to compensate for white matter loss was already fairly well-known in 1980, when Lorber's research was profiled in Science:

What, then, is happening when a hydrocephalic brain rebounds from being a thin layer lining a fluid-filled cranium to become an apparently normal structure when released from hydrostatic pressure? According to [New York University Medical Center researcher Fred] Epstein and on the basis of his colleagues' observations on experimental cats, the term rebound aptly describes the reconstitution process, with stretched fibers shortening, thus diminishing the previously expanded ventricular space. Within a short time scar tissue forms, constructed from the glial cells that pack between the nerve cells. "The reconstitution of the mantle," report Epstein and his colleagues, "does not result in the reformation of lost elements, but rather in the formation of a glial scar and possibly a return to function of the remaining elements (Lewin 1980:1233-1234).

Nor is it obvious from the reports that the condition had "no" cognitive manifestations. Much seems to depend on the single case described above, with an apparently normal college student walking in off the street to discover he had minimal brain mass. But this story is quite obviously incredible as presented: most neurologists don't perform brain scans just because a college student wears a large hat. It seems reasonable to infer that the student was referred by his doctor to Lorber, a hydrocephalus specialist, for some reason. We can only guess what the reason might be, but it hardly gives confidence in the anecdote!

Without question, there are many patients who have this outcome -- no significant cognitive deficit compared to nonpatients, despite profound pathology. This is true of almost any pathology affecting the brain, including tumors, strokes, and developmental abnormalities. The question is whether this provides a valid model for understanding the adaptive importance of brain volume. It seems that later onset hydrocephalus, where a normal brain is compressed within a relatively normal-sized skull by cerebrospinal fluid pressure, does not really apply to the evolutionary question. The reported cases do not apparently involve significant gray matter tissue loss. A "thin" cortex does not necessarily imply functionally small cortical volume, even with substantial white tissue loss.

Hemispherectomy

Another kind of extreme reduction in brain volume is hemispherectomy -- an operation in which either the left or right half of the cerebrum is completely removed. Hemispherectomy is contemplated only for patients with exceptionally severe seizures, which can result from Rasmussen syndrome or congenital irregularities such as cortical dysplasia.

It is a misconception that hemispherectomy generally involves removal of half the brain volume. This really only refers to "anatomical hemispherectomy", which is now rarely performed. Other options include hemidecortication, or removal of cortical gray matter, and "functional" hemispherectomy, which entails removal of diseased brain matter with disconnection of the corpus callosum and white matter tracts connecting frontal, temporal, and occipital lobes. The goal of all these surgeries is to interrupt the abnormal connectivity that leads to seizures. Each procedure results in the functional loss of half the cerebrum, but without the actual reduction in brain volume or the dramatic CT shots showing a half-empty cranium. Illustrated stories about hemispherectomy may mislead by using pictures from 20 years ago or more!

Skoyles (1999) considered hemispherectomy as one example demonstrating that human cognition does not necessarily require brain sizes larger than Homo erectus. He lists a number of individual cases, for example:

Vining and colleagues (1993) report the outcomes for 12 hemispherectomized children at an average of 9 years follow up. They give extended details on five of them. One case, "13," a female, is of interest. She started having seizures at five; by seven she was having up to 20 a day. At seven and half, she had a left hemispherectomy, remaining in coma for six weeks. Two years later she had a full scale IQ of 98. Three years afterwards, though she needed some help in mathematics, she was in seventh grade gaining grades of A and B.

Although the condition is rare, it has been performed often enough to have build a substantial sample to assess its results. To assess the effects on brain function, we must find a valid comparison considering the fact that hemispherectomy patients were highly compromised before the procedure by their underlying conditions. For example, Prayson and colleagues (1999) examined the histology of brain tissues removed during hemispherectomies on 37 patients, finding:

Cortical dysplasias or hemimegalencephaly were identified in 14 patients. The most common patterns of dysplasia observed included architectural disorganization (n = 13), increased molecular layer neurons (n = 11), and neuronal cytomegaly (n = 11). One patient was known to have epidermal nevus syndrome. Six patients had Sturge-Weber syndrome. Remote infarct/ischemic damage was identified as the etiology of seizures in six patients; four of these patients had mild associated secondary cortical architectural abnormalities. Three patients demonstrated pathology consistent with Rasmussen's encephalitis; one additional patient had chronic encephalitis changes, not otherwise specified. In two cases, changes consistent with hippocampal sclerosis were identified; additionally, hippocampal neuronal loss and gliosis was focally identified in three patients. Most of these patients had coexistent cortical dysplasia or radiographic evidence of remote infarct. One specimen demonstrated areas of infarct following resection of an arteriovenous malformation. In two specimens, significant histopathologic findings were not identified; both of these patients had radiographic evidence of remote infarct. The spectrum of pathologic conditions that may be encountered in the setting of a functional hemispherectomy is varied and in this study most frequently included cortical dysplasia, Sturge-Weber syndrome remote infarct, and Rasmussen's encephalitis.

In other words, tissue lost during hemispherectomy includes a high fraction of pathological tissue. Most patients already exhibit developmental differences resulting from their pathology, including the takeup of functions into their more normal cerebral hemisphere. Additionally, most preoperative hemispherectomy patients have extreme seizures that create learning deficits prior to surgery. Almost all hemispherectomies are performed on relatively young children, with a great potential for further learning and development. The intent of the surgery is to alleviate the seizures and enable more effective learning, through an altered developmental pathway. This is an important perspective, because the comparison is between two developmental processes before and after surgery, both of them atypical in many respects compared to nonpatients.

The remaining brain areas show a remarkable plasticity in taking on functions normally localized in the portions of the brain that have been removed. This is maybe the most obvious for language. For example, Boatman and colleagues (1999) studied language recovery in patients who had left hemispherectomies. The left hemisphere is usually the place where language comprehension and speech production are carried out, but left hemispherectomy patients must develop these abilities in the right hemisphere instead:

We investigated the language capabilities of the isolated right hemisphere in 6 children (age, 7-14 years) after left hemidecorticectomy for treatment of Rasmussen's syndrome. Patients were right-handed before surgery and had at least 5 years of normal language development before the onset of seizures. Language testing included speech sound (phoneme) discrimination, single word and phrasal comprehension, repetition, and naming. Within 4 to 16 days after surgery, patients showed improved phoneme discrimination compared with their performance shortly before surgery. Other language functions remained severely impaired until at least 6 months after surgery. By 1 year after surgery, receptive functions were comparable with, or surpassed, patient presurgery performance. Although word repetition was intact by 1 year after surgery, naming remained impaired, and patient speech was limited largely to production of single words. These results suggest that the right hemisphere is innately capable of supporting multiple aspects of phoneme processing. Recovery of higher level receptive and, to a lesser extent, expressive language functions is attributed to plasticity of the right hemisphere, which appears to persist beyond the proposed critical period for language acquisition and lateralization.

This plasticity implies that language lateralization involves developmental processes that can unfold on the opposite side under the right circumstances. Subsequent research has shown that the asymmetry of function emerges alongside an asymmetry in brain microstructure during early childhood (Amunts et al. 2003). This line of reasoning tends toward the interpretation that brain function depends less on a predetermined or canalized structure of neural tissues, and more on the presence of appropriate environmental inputs -- such as maternal and cultural patterning.

But does this plasticity mean that a human population could evolve a vastly smaller brain while maintaining equivalent cognitive functions? To answer this, we need to look beyond the degree of plasticity to examine other outcomes.

Pulsifer and colleagues (2004) examined the outcome of hemispherectomy in 71 children:

Mean age at surgery was 7.2 years. At follow-up, on average 5.4 years after surgery, 65% are seizure free, 49% are medication free, and, of those responding, none rated quality of life as worse than before surgery. Mean IQ was in the 70s for Rasmussen and vascular patients and in the 30s for cortical dysplasia patients. Language and visual-motor skills were consistent with IQ. For Rasmussen patients only, language was significantly more impaired for left than for right hemispherectomy, both before surgery and at follow-up. Adaptive skills were mildly impaired, with greatest impairment in the physical domain. Cognitive measures typically changed little between surgery and follow-up, with IQ change < 15 points for 34 of 53 patients; of the remainder, 11 declined and eight improved. Behavior was free of major problems, but social interactions and activities were limited.

This remains a difficult problem to evaluate, because it is hard to test cognitive performance in young subjects, and because of the variety of functional impacts that may result from major brain surgery. This and other studies indicate that the hemispherectomy generally does no harm to IQ and sometimes allows improvement in this sample of patients. But as Shields (2000) put it:

Many children with catastrophic epilepsy have the seizures as a result of underlying brain abnormalities that will inevitably lead to mental retardation whether or not they have seizures. In some patients, however, the mental retardation appears to be caused by the seizures. Developmental plasticity provides children with an opportunity to recover from significant brain injuries. However, the plasticity may also be the cause of the mental retardation. In such patients, control of the seizures may lead to more normal intellectual development.

The presence of pathology greatly complicates any evaluation -- and of course it goes without saying that "normal" itself implies assumptions about the range of functions under consideration. In some cases, normal cognitive function develops both before and after surgery; in others normal development is possible after surgery but not apparently before, and in yet others, severe impairments remain after surgery.

What we should keep in mind is the extensive degree of cultural assistance and therapy available to patients. Although they have smaller than ordinary brain volume as a result of their surgery, they inhabit a qualitatively different environment with respect to cognitive development; one that is intended to ameliorate any deficits resulting both from their pathology and from their surgery.

So the case of hemispherectomy does not test the proposition that normal cognitive performance is possible after a great reduction in brain size. Instead it possibly tests the proposition that a reduction in brain size may be consistent with normal cognitive performance under a specialized cultural and environmental regime. That hypothesis is refuted by the majority of cases in the clinical record, for whom the specialized learning environment has not managed to eliminate developmental deficits. Still, for many patients some combination of surgery, therapy and learning assistance do make a decisive difference, and they attain normal cognitive performance -- even normal for developmental age.

How do these cases apply?

There is no single conclusion that we can draw from these examples of extreme pathological reduction in brain size in humans. Clearly, the brain is capable of remarkable plasticity in development, including alternate localizations of some functions that are highly localized in most adults.

But can we apply this plasticity more generally, to suggest that almost any brain structure might have evolved in ancient human populations? Even those that involve immense reductions in overall brain size?

It should be mentioned that these assessments build on a rather narrow view of "cognition." For instance, all hemispherectomy patients have some paralysis on the opposite side from the removed hemisphere. The functions of the motor and sensory cortices of the absent side do not appear to have the developmental plasticity exhibited by language. From the perspective of fitness in prehistoric human populations, the adequate control of movement and perception of sensory information would have a substantially greater importance than in today's cultural milieu. So a reduction in brain size that impacts motor and sensory function but leaves other aspects of cognition intact certainly cannot be said to have no impact. Just because a reduction in performance can be managed within our population does not mean that it could have evolved in some past population.

Also, the attainment of "normal" cognition, however defined, requires substantial investment and teaching for the average human. Humans with developmental challenges often can attain normal cognitive performance for their age, particularly when supplementary teaching and therapy is available. All this is to say that human brains are coadapted with behavioral patterns that channel development.

That observation entails a prediction: a vast reduction in brain size could maintain a given behavioral function only within an increasingly specialized cultural environment. Canalization is a function of both development and environment, and if less specification is available in the brain, more must be provided by external mechanisms.

There are reasons to think that such external mechanisms must be extremely difficult to evolve and maintain over long time periods. The human body dissipates approximately 100 watts of energy. That may not sound like much -- it's a good-sized light bulb -- but 20 watts of that energy are consumed by the brain. A hobbit-sized brain should only have required around 7 watts, reducing the energy requirements of the body by 13 percent. This is oversimplified, because it does not account for the total energy budget (including activity), but the simplicity arrives at a single idea: if ancient people ever starved to death, they should have been selected for smaller brains. Humans who could have managed with a smaller brain would have had a great advantage.

Still, evolving humans did not take this pathway. Their brains got bigger. Although it may be conceivable -- even if it is far from demonstrated -- that a radically smaller brain coupled with a specialized culture might have increased fitness, apparently there was no available evolutionary pathway to that adaptation. I would guess that it is simply more difficult to maintain the necessary cultural specializations for such an adaptation within the context of ancient human population structure. It is easier to accomplish development with a large brain that can employ many bottom-up strategies to build its cognitive abilities.

I think that the evidence on development in people with small brain size operates in this context as a valuable illustration of developmental tradeoffs. Developing humans use strategies based on individual learning to acquire information and abilities. These strategies are greatly facilitated by social learning, and deliberate teaching, and the actual manifestation of these social learning strategies varies greatly among human groups. The variation in social learning -- which helps to generate cultural variation among humans -- to some extents limits its ability to provide a developmental substrate for full cognitive development. Over the course of human evolution, social learning itself was constrained by small group sizes, high mortality (which limits the temporal extent of long-term relationships), and unpredictability of kinship relations between group members (other than the mother) and developing children. Individual learning strategies, which are the main learning mechanism in other primates, are instantiated within developing brains and retain a central role in human cognitive development. Even though more extensive and systematized social learning might reduce the adaptive importance of brain size, this solution did not outweigh the importance of individual learning during human evolution. I speculate that this was because of the constraints on the transmission of social learning strategies.

References:

Amunts K, Schleicher A, Ditterich A, Zilles K. 2003. Broca's region: cytoarchitectonic asymmetry and developmental changes. J Comp Neurol 465:72-89. doi:10.1002/cne.10829

Boatman D, Freeman J, Vining E, Pulsifer M, Miglioretti D, Minahan R, Carson B, Brandt J, McKhann G. 1999. Language recovery after left hemispherectomy in children with late-onset seizures. Ann Neurol 46:579-586. doi:10.1002/1531-8249(199910)46:4<579::AID-ANA5>3.0.CO;2-K

Boesch C, Boesch H. 1984. Mental map in wild chimpanzees: an analysis of hammer transports for nut cracking. Primates 25:160-170. doi:10.1007/BF02382388

Lewin R. 1980. Is your brain really necessary? Science 210:1232-1234. JSTOR

Fletcher JM, Bohan TP, Brandt ME, Kramer LA, Brookshire BL, Thorstad K, Davidson KC, Francis DJ, McCauley SR, Baumgartner JE. 1996. Morphometric evaluation of the hydrocephalic brain: relationships with cognitive development. Child's Nervous System 12:192-199. doi:10.1007/BF00301250

Beyerstein BL. 1999. Whence cometh the myth that we only use ten percent of our brains? Pp. 3-24 in Mind myths: exploring everyday mysteries of the mind and brain, Della Sala S, ed. John Wiley and Sons, New York.

Carson BS, Javedan SP, Freeman JM, Vining EPG, Zuckerberg AL, Lauer JA, Guarnieri M. 1996. Hemispherectomy: a hemidecortication approach and review of 52 cases J Neurosurg Full text

Martinussen M, Fischl B, Larsson HB, Skranes J, Kulseng S, Vangberg T, Vik T, Brubakk A-M, Haraldseth O, Dale AM. 2005. Cerebral cortex thickness in 15-year-old adolescents with low birth weight measured by an automated MRI-based method. Brain 128:2588-2596. doi:10.1093/brain/awh610

Prayson RA, Bingaman W, Frater JL, Wyllie E. 1999. Histopathologic findings in 37 cases of functional hemispherectomy. Ann Diag Pathol 3:205-212. doi:10.1016/S1092-9134(99)80052-5

Pulsifer MB, Brandt J, Salorio CF, Vining EPG, Carson BS, Freeman JM. 2004.
The cognitive outcome of hemispherectomy in 71 children. Epilepsia 45: 243-254. doi:10.1111/j.0013-9580.2004.15303.x

Shields WD. 2000. Catastrophic epilepsy in childhood. Epilepsia 41:S2-S6. doi:10.1111/j.1528-1157.2000.tb01518.x

Skoyles JR. 1999. Human evolution expanded brains to increase expertise capacity, not IQ. Psycoloquy 10:2. Full text

Vining, E. P., Freeman, J. M., Brandt, J., Carson, B. S. & Uematsu, S. (1993). Progressive unilateral encephalopathy of childhood (Rasmussen's syndrome): A reappraisal. Epilepsia, 34, 639-650.

MicroRNAs are short sequences (several sources put them at 21 to 25 nucleotides) of noncoding RNA MicroRNA function is a fairly new discovery, with their existence, diversity and operation characterized only within the last five years. A good review was provided by Lin He and Gregory Hannon (2004), which is now getting to be a little old, but covers the basics.

These little RNA snippets may function in many ways. At least some of them function as gene regulatory mechanisms, by interfering with the translation of messenger RNA (mRNA). Interference happens when part of the microRNA complements a small part of an mRNA sequence, and binding between the two effectively represses protein synthesis at the ribosomes. MicroRNAs themselves are results of posttranscriptional processing from longer precursor RNAs, which have a three-dimensional structure that gets cut down

Gene expression and regulation is certainly the "in" topic in genomics, because it is the major unknown connector between genes, phenotypes, and development. MicroRNA regulation is one of the hottest topics in gene regulation, because they are new, cute, and cool. They also get a lot of attention because a few microRNAs can interfere with the normal processes of regulated cell death (apoptosis), and thereby help to cause cancers.

One other thing: "microRNA" is just too long for molecular biologists to type, so they are abbreviated "miRNA".

It has been known for a few years that at least some miRNAs were highly active during the development of the brain in mammals (e.g., Krichevsky et al. 2003). For example, Miska and colleagues (2004) found that microRNA expression pulsed in waves through the developing mouse brain:

We isolated 18-26 nucleotide RNAs from developing rat and monkey brains. From the sequences of these RNAs and the sequences of the rat and human genomes we determined which of these small RNAs are likely to have derived from stem-loop precursors typical of microRNAs. Next, we developed a microarray technology suitable for detecting microRNAs and printed a microRNA microarray representing 138 mammalian microRNAs corresponding to the sequences of the microRNAs we cloned as well as to other known microRNAs. We used this microarray to determine the profile of microRNAs expressed in the developing mouse brain. We observed a temporal wave of expression of microRNAs, suggesting that microRNAs play important roles in the development of the mammalian brain.

MicroRNAs seem to be involved in many different kinds of developmental processes, many of them embryonic -- such as Hox-mediated development -- but also adult functions such as hematopoiesis (Pasquinelli et al. 2005).

Zhenbao Yu and colleagues compared the expression of microRNA targets in adult and developing embryonic tissues of mice and flies. The miRNA targets are the mRNA sequences that the miRNA binds. In other words, these are the genes that are regulated by miRNA, and -- as the results show -- they are more highly expressed during embryonic development. Here's their abstract:

MicroRNAs (miRNAs) are non-coding small RNAs of 22 nt that regulate the gene expression by base pairing with target mRNAs, leading to mRNA cleavage or translational repression. It is currently estimated that miRNAs account for 1% of predicted genes in higher eukaryotic genomes and that up to 30% of genes might be regulated by miRNAs. However, only very few miRNAs have been functionally characterized and the general functions of miRNAs are not globally studied. In this study, we systematically analyzed the expression patterns of miRNA targets using several public microarray profiles. We found that the expression levels of miRNA targets are lower in all mouse and Drosophila tissues than in the embryos. We also found miRNAs more preferentially target ubiquitously expressed genes than tissue-specifically expressed genes. These results support the current suggestion that miRNAs are likely to be largely involved in embryo development and maintaining of tissue identity.

This kind of expression survey at different ontogenetic stages is very important, because it covers a blind spot in analyses that depend on functional categories. For example GO analyses include categories for "development", but as Yu and colleagues point out, many genes change in expression during development that are not part of the "developmental" categories. This is another of the consequences of widespread pleiotropy -- genes that have important effects early in development may continue to be important in restricted tissues later in life. By being scored in a functional category related to these later functions, the earlier functions of the gene may be missed in the functional analysis. Screening gene expression at multiple times helps to catch these temporally sensitive functions.

References:

He L, Hannon GJ. 2004. MicroRNAs: small RNAs with a big role in gene regulation. Nat Rev Genet 5:522-532. doi:10.1038/nrg1379

Krichevsky AM, King KS, Donahue CP, Khrapko K, Kosik KS. 2003. A microRNA array reveals extensive regulation of microRNAs during brain development. RNA 9:1274-1281.

Miska EA, Alvarez-Saavedra E, Townsend M, Yoshii A, Sestan N, Rakic P, Constantine-Paton M, Horvitz HR. 2004. Microarray analysis of microRNA expression in the developing mammalian brain. Genome Biol 5:R68. Free full text

Pasquinelli AE, Hunter S, Bracht J. 2005. MicroRNAs: a developing story. Curr Opin Genet Dev 15:200-205.

Yu Z, Jian Z, Shen S-H, Purisima E, Wang E. 2007. Global analysis of microRNA target gene expression reveals that miRNA targets are lower expressed in mature mouse and Drosophila tissues than in the embryos. Nucleic Acids Res 35:152-164. doi:10.1093/nar/gkl1032

Roberto Macchiarelli and colleagues (2006, link) have published data regarding molar crown formation times in Neandertals. Here is their abstract:

Growth and development are both fundamental components of demographic structure and life history strategy. Together with information about developmental timing they ultimately contribute to a better understanding of Neanderthal extinction. Primate molar tooth development tracks the pace of life history evolution most closely, and tooth histology reveals a record of birth as well as the timing of crown and root growth. High-resolution micro-computed tomography now allows us to image complex structures and uncover subtle differences in adult tooth morphology that are determined early in embryonic development. Here we show that the timing of molar crown and root completion in Neanderthals matches those known for modern humans but that a more complex enamel-dentine junction morphology and a late peak in root extension rate sets them apart. Previous predictions about Neanderthal growth, based only on anterior tooth surfaces, were necessarily speculative. These data are the first on internal molar microstructure; they firmly place key Neanderthal life history variables within those known for modern humans.

The ScienceNOW article by Ann Gibbons stresses the fact that the study involves sectioned teeth instead of external perikymata counts. The result is a lack of any significant difference between the timing and duration of crown formation compared to modern humans:

When the researchers sliced thin sections of the molars, they noticed important similarities between Neandertals and modern humans. The dark birth line emerged at about the same time in dental development as in modern humans, indicating that Neandertal teeth developed at the same rate as modern human teeth do around the time of birth, the team reports online today in Nature. The researchers also found that the crowns and roots of the Neandertals grew at the same rate of those of modern humans, with root growth complete by age 9 as in modern children. "This all points to a dental developmental schedule that was most like that in modern humans," says anatomist and lead author Christopher Dean of University College London, who also is a dentist.

The tooth development story is becoming a bit complicated to follow. As applied to Neandertals, Guatelli-Steinberg and colleagues (2005), and Ramirez Rossi and Bermudez de Castro (2004) assessed dental maturation rates from anterior teeth (incisors and canines), while the current paper by Macchiarelli and colleagues (2006) is about molar development. Additionally Dean and colleagues (2001) examined early Homo and Australopithecus samples, and Ramirez Rossi and Bermudez de Castro also considered earlier Spanish Homo samples.

The notable finding by Guatelli-Steinberg and colleagues (2005) was that modern human samples are themselves hugely variable in their enamel formation times -- at least, as interpreted through enamel tissue characters. This is a very serious problem for interpreting any past population characteristics, because in fact the variation among modern sample means -- without even considering the within-sample variation -- encompasses most fossil samples of Homo and many australopithecines as well.

Here's what I wrote about this last year:

[T]he Neandertals are far from the most interesting part of this perikymata problem. Can we tell a human from an australopithecine from these data? If so, why do some of the earliest humans have the lowest (i.e. sub-australopithecine) counts?

The early human specimen that stood out (considering their anterior dentition) was KNM-ER 15000, and it is not clear from the available papers whether it is actually outside the extant modern sample ranges. Otherwise, early Homo specimens are entirely humanlike in their crown formation times, and this observation is confirmed by Macchiarelli and colleagues' present work on Neandertal molars.

In short, early Homo enamel formation times (and for that matter, non-robust australopithecines) fall entirely within the range of variation of living humans, with most specimens within the range of human population means.

The null hypothesis in this case is that enamel formation times did not differ between fossil and living humans. That hypothesis is not refuted by the available data -- and given the wide variation in enamel formation times among living human populations, it seems likely that further sampling of fossil Homo will arrive at the same result. The issue is not sample size for the fossils, in other words, it is the intrinsic variability among living people, which remains unexplained.

The variation among living humans raises a thornier problem, also. The reason why many people are interested in molar enamel deposition is the idea that enamel formation is linked to somatic maturation in general. But the great variability in enamel formation times in recent humans would seem to disprove a strong link between somatic and dental maturation.

The idea that somatic and dental maturation rates should be tightly linked comes mainly from interspecific comparisons. For example, Ramirez Rossi and Bermudez de Castro (2004:938) draw out the following logic:

Dental growth is a good proxy for the overall rate of maturation in a species (Smith 1989). Short crown formation time in fossil Homo species therefore indicates that somatic development was not as long as in H. sapiens. Importantly, Neanderthals apparently also had a faster pace of somatic development than their ancestor, H. heidelbergensis.

...

A prolonged life-history in hominids has previously been related to a reduction in the mortality rate of adults, and in turn low mortality rates have in the past been associated with an increase in brain size. Metabolic rate has also been linked to brain growth and has been implicated as a primary determinant of variation in life history. However, developmental changes are most probably related to fundamental changes in the timing and frequency of reproduction. Results presented here suggest that brain growth and brain size are not primary determinants of life-history re-scheduling in hominids; rather, it seems that high adult mortality rates are most likely to have driven such rescheduling among Neanderthals. A clearer picture of Neanderthals emerges here--as a species of Homo adapted to particular environmental conditions, when a high-calorie diet and a high metabolic rate were able to fuel fast somatic growth, as well as to grow and sustain a large brain.

This last conclusion was rejected by Guatelli-Steinberg et al. (2005) -- after all, their data showed that Neandertals didn't have short enamel development compared to living Africans.

And reflecting on the balance of data from Neandertals, an especially rapid rate of development seems quite implausible. For instance, if Neandertals had no problem fueling a 3000-5000 kcal per day energy expenditure, then why did their kids have so many enamel hypoplasias? If Neandertals had a limitless tap of food to enable their rapid somatic development, then what killed them so young?

Guatelli-Steinberg et al. (2005) posit that dental development does not provide an adequate correlate of somatic maturation, and suggest that adult brain size makes a better yardstick:

It has also been suggested that if Neandertals suffered high adult mortality rates, then they might be expected to have had abbreviated periods of childhood growth (10, 15). Adult mortality rates directly select for the timing of maturation across mammals; a larger risk of dying selects for rapid maturation (9, 30, 31). However, Smith (32) notes that if Neandertals had accelerated life histories, then this would leave them with a "peculiar" relationship between brain size and maturation, "two variables that are rarely of step [sic]." Because large brains require extended periods of childhood growth (1-7, 33), the presence of large brains in Neandertals suggests that their adult mortality risks were not high enough to have prevented them from evolving prolonged growth periods.

The logic is that a given adult brain volume is linked to maturation schedule because of learning. Crudely, a larger brain takes longer to fill with information. Or more properly (in causal terms), selection for more information processing tends to increase brain size (relative to body size), information processing ability is constrained by learning, so that brain size is correlated to maturation schedule by indirect causal mechanisms.

But I would question even this relationship. For one thing, it doesn't seem to work very well within a population. Or at least, not within the population of living humans, where variation in brain sizes show no clear relationship to skeletal maturation schedules. For another, brain sizes have shrunk in recent humans, but there is no particular evidence that maturation times have reduced, or that humans have less to learn. Some of the smaller brain sizes may be explained by smaller body size, but smaller body size also ought to be correlated with faster maturation.

It seems to me that comparing Neandertals to living people for developmental rates is misleading. Living people are different from other primates in their very low rates of adult mortality (and consequent long period of post-reproductive senescence). And we know that Neandertals were more similar to other primates in this respect: they died younger than humans. But that isn't a new development in Neandertals -- instead, the long lifespans typical of recent people are the new development.

There has as yet been little integration of the literature on human growth with these fossil-related questions. For instance, many nutritionally-limited human populations respond by delaying growth. Sometimes such delays can be resolved by rapid growth later in development, sometimes they lead to reductions in adult body size. This kind of plasticity in growth schedules and ultimate body size ought to have characterized ancient humans, which would have increased their variability (in both maturation schedule and adult body size) compared to any single living human population.

References:

Guatelli-Steinberg D, Reid DJ, Bishop TA, Larsen CS. 2005. Anterior tooth growth periods in Neandertals were comparable to those of modern humans. Proc Nat Acad Sci USA 102:14197-14202. Abstract

Dean C, Leakey MG, Reid D, Schrenk F, Schwartz GT, Stringer C, Walker A. 2001. Growth processes in teeth distinguish modern humans from Homo erectus and earlier hominins. Nature 414:628-631.

Macchiarelli R, Bondioli L, Debénath A, Mazurier A, Tournepiche J-F, Birch W, Dean C. 2006. How Neanderthal teeth grew. Nature (early online) DOI link

Ramirez Rossi FV, Bermudez de Castro JM. 2004. Surprisingly rapid growth in Neanderthals. Nature 428:936-939. Full text (subscription)

This PLoS Biology paper by Pier Ferrari et al. is highly interesting:

Here we report the behavioral responses of infant rhesus macaques (Macaca mulatta) to the following human facial and hand gestures: lip smacking, tongue protrusion, mouth opening, hand opening, and opening and closing of eyes (control condition). In the third day of life, infant macaques imitate lip smacking and tongue protrusion. On the first day of life, the model's mouth openings elicited a similar matched behavior (lip smacking) in the infants. These imitative responses are present at an early stage of development, but they are apparently confined to a narrow temporal window. Because lip smacking is a core gesture in face-to-face interactions in macaques, neonatal imitation may serve to tune infants' affiliative responses to the social world. Our findings provide a quantitative description of neonatal imitation in a nonhuman primate species and suggest that these imitative capacities, contrary to what was previously thought, are not unique to the ape and human lineage. We suggest that their evolutionary origins may be traced to affiliative gestures with communicative functions.

That's the abstract. The second paragraph of the paper is essential background if you don't know much about babies:

To date, studies of early signs of this matching capacity have been largely limited to human infants. Almost 30 years ago, Meltzoff and Moore [3] reported that 2- to 3-wk-old infants responded with corresponding matching behaviors to specific human facial gestures, such as mouth opening (MO), tongue protrusion (TP), lip protrusion, and hand opening (HO). Other studies confirmed this early investigation, although there is still considerable debate about which gestures are actually imitated [4-9]. To avoid the possible interferences of early learning experiences with innate imitation processes, Meltzoff and Moore conducted further investigations immediately after birth and demonstrated that newborns also can imitate adult facial gestures [4,5]. They argued that the specificity of the imitative response indicates a capacity to accurately match the body parts involved. Because newborns cannot see their own face but can only perceive it through proprioception, the matching of their own acts to those observed should require a supramodal representation of the observed gesture, called active intermodal matching [3-5,10].

They note later in the paper that some human babies just don't imitate in this way at all. It's pretty striking when you see it happen, so the variation between infants ought to be explained somehow. The most consistent imitation is sticking out the tongue (this may be why we all try to do it to babies!). And there is a window in humans -- starting at around 2 weeks, the imitations last only up to around 3 months.

Ferrari and colleagues explain the windows for imitation in terms of social learning and the development of independence. They note that human infants start to exhibit new social abilities at around 2-3 months such as smiling and cooing. Chimpanzees have a slightly earlier window for imitation than humans, and also start to show independence earlier. The imitation that they observe in the macaque infants ends by 7 days of age -- and they write that the infants start to show motor independence away from the mother for short periods of time by this age:

Already at 1 wk, infant macaques may leave their mother for short periods of time. Infant exploration, involving mother–infant separation, increases over time. In our experiments, we noticed that holding a 2-wk-old or older infant and capturing its attention with the stimulus became more and more difficult with increasing age. In humans and chimpanzees, neonates stay in body contact with their mother for much longer, and the mother is the only one responsible for maintaining the infant. Thus, neonatal imitation in rhesus macaques occurs with a timing that, considering the species-specific patterns of development of motor and cognitive skills, is comparable with those reported for humans and chimpanzees.

There is a lot in the discussion about "imitation" and what it means, and how it varies among species, such as between apes and monkeys. It seems to me that "imitation" is a term that is starting to cause more confusion than it resolves. Lately, the term has been limited to cases of learning where an individual is replicating the behaviors of another individual -- not only the end result, but also all the steps that lead to that end result. But the infant "imitation" quite clearly doesn't require the kind of conceptual learning that instances of "imitation" among older juveniles and adults seems to take.

Here they focus on a possible neural basis for the infant imitation, suggesting that "mirror neurons" may be responsible. "Mirror neurons" are activated both when doing an action and when seeing another individual do the same action. To the extent that these mirror neurons are "pre-wired" to connect visual and proprioceptive inputs, they might spur an individual to "imitate" the actions he or she sees.

Of course, that doesn't really address just how such a system might evolve, or what it's adaptive value might be. Some have suggested that infant imitation mainly functions to "make them cute" to adults, or to demonstrate some kind of incipient ability for social cognition to make it more likely that the mother will provide timely care (i.e., by showing that the child is a good investment because it is neurologically OK).

But I really don't see these explanations accounting for a developmental window. To me, a window implies opening and closing constraints on neural development. To that end, it is very interesting that the end of the window appears relevant to social development.

The real question is whether monkey mothers inspire imitation and look for it in their infants. Knowing this would help test whether the imitation itself is an adaptation or whether it is a side-effect of some developmental process (presumably related to the development of social cognition and signalling). Since there is so much variation among human infants in this quality, I am pretty tempted to think it is not a significant point where behavior rubs against survival. It may better be seen as a portal on aspects of development that manifest later. For instance, it may be a frequent consequence of the wiring of mirror neurons that they have this effect on infants, but the adaptive consequences of the wiring are manifested later as juveniles learn to associate the facial expressions of others with their likely behaviors.

From that perspective, the most significant aspect of the paper is its demonstration that the window in apes, and then humans, has greatly increased in length and is delayed relative to birth. And yet, despite these relatively great changes in timing, it is still after birth. In other words, it appears to show a necessary early environmental role for the development of social cognition (if it's that), which has extended in the ape and human lineages.

It has stuck a long chunk of learning into a developmental process as a trade-off against earlier independence. Of course, social independence and motor independence are different things...

UPDATE (9/7/2006): Brainethics has pictures.

References:

Ferrari PF, Visalberghi E, Paukner A, Fogassi L, Ruggiero A, et al. (2006) Neonatal Imitation in Rhesus Macaques. PLoS Biol 4(9): e302. Free full text

The Times had this article the other day discussing whether TV is good for preschool-age kids. It's not all that interesting, but this bit near the end caught my attention:

Developmental psychologists say the Vanderbilt research offers an intriguing clue to a phenomenon called the "video deficit." Toddlers who have no trouble understanding a task demonstrated in real life often stumble when the same task is shown onscreen. They need repeated viewings to figure it out. This deficit got its name in a 2005 article by Daniel R. Anderson and Tiffany A. Pempek, psychologists at the University of Massachusetts, who reviewed literature on young children and television.

...

But psychologists still want to get to the bottom of what might explain the difference. Is it the two-dimensionality of the screen? Do young children have some innate difficulty in remembering information transmitted as symbols?

The paper linked in an article is a broad review of early childhood TV viewing, and isn't all that helpful, although it gives about 2 pages of review on the topic. Interestingly, the "video deficit" includes aspects of language learning:

A third line of research is concerned with language learning. Children 2 years and older can clearly learn vocabulary from television (Naigles & Kako,1993; Rice, Huston, Truglio, & Wright, 1990;Rice & Woodsmall, 1988). Nevertheless, when comparisons are made between video and equivalent live conditions in children younger than 2 1/2years, the results suggest a video deficit. Grela, Lin,
and Krcmar (2003) tried to teach object labels either live, in an equivalent video, or in a version of Teletubbies that used the labels. They found better learning in the live as compared to video conditions. Learning from video by children near their 2nd birthday was substantially better than that by younger children.

Infants are able to perceive many phonetic contrasts that are not found in their native language; this ability is lost by about 12 months of age if infants are not exposed to other languages. Kuhl, Tsao, and Liu (2003) exposed American infants to contrasts found in Mandarin. One group of infants was exposed to live speakers of Mandarin for about 5 hours during 12 sessions between 9 and 10 months of age. Other groups were exposed to equivalent audiovisual or audio-only DVDs. The infants exposed to live speakers did not experience the loss of ability to perceive Mandarin contrasts. Infants exposed to the DVD stimuli, however, showed the same loss as infants exposed to no Mandarin at all. Again, this research indicates a profound video (and audio) deficit (Anderson and Pempek 2005:513).

This paper by Georgene Troseth and colleagues delves into the problem:

Young Children's Use of Video as a Source of Socially Relevant Information

Although prior research clearly shows that toddlers have difficulty learning from video, the basis for their difficulty is unknown. In the 2 current experiments, the effect of social feedback on 2-year-olds' use of information from video was assessed. Children who were told "face to face" where to find a hidden toy typically found it, but children who were given the same information by a person on video did not. Children who engaged in a 5-min contingent interaction with a person (including social cues and personal references) through closed-circuit video before the hiding task used information provided to find the toy. These findings have important implications for educational television and use of video stimuli in laboratory-based research with young children.

These researchers frame the issue in terms of the strategies children use to identify socially relevant information:

By the time they reach their second birthday, toddlers have figured out that a prime source of information is other people. They are attuned to socially relevant information: information that is presented by a social partner and accompanied by appropriate cues indicating a shared focus on an aspect of the environment. For instance, numerous studies demonstrate that 2-year-olds are skilled users of a range of social cues for word-learning purposes, including eye gaze, gesture, discourse novelty, and emotional outbursts (see Baldwin & Tomasello, 1998, for a review). Young children's skill at obtaining information from social others may rest in part on their attention to features common to animate agents -- such as the potential for contingent movement and the presence of faces (e.g., Johnson, Booth, & O'Hearn, 2001; Johnson, Slaughter, & Carey, 1998; Shimizu & Johnson, 2004). It is possible that the presence of such features is a precondition for toddlers to use others as potential sources of information. This may be one factor underlying the video deficit in toddlers: in the absence of contingent interaction, they usually fail to regard people on TV as viable information sources. In the current study, when contingent interaction was lacking, children failed to use identical verbal information to solve a problem.

The connection to the ways that children learn to use and respond to explicitly social cues and situations is important. Social interactions are two-way, and that modality is a fundamental part of human reality. Two-way interactions really can't be modeled well by television. But in contrast, three-way interactions are modeled very well by TV. Any program that shows two individuals interacting with each other is fundamentally a three-way interaction, since it implicates the viewer as a third party.

Understanding three-way interactions may be well above the cognitive skills of toddlers. Seeing the relationship between two other individuals is a three-way interaction. Three-way interactions are more difficult for an additional reason -- there are vastly more of them in any social group. With two-way interactions, the total number accessible to any individual is simply the number of individuals in the group, minus the focal individual herself. In other words, it scales linearly with group size. But with three-way interactions, the total possible number of interactions in a group is combinatorial.

Now it is interesting that language learning has been grafted into human development at a time when these kinds of social learning are still being worked out. Plausibly, it reflects the fact that language helps people to organize those more numerous and more complex three-way interactions.

References:

Anderson DR, Pempek TA. 2005. Television and very young children. American Behavioral Scientist 48:505-522. Abstract

Troseth GL, Saylor MM, Archer AH. 2006. Young children's use of video as a source of socially relevant information. Child Development 77:786. DOI link

A really big problem in studying the evolution of the brain is that we have very little idea how the organ develops. So this paper by Bystron and colleagues in Nature Neuroscience is pretty interesting:

We describe a distinctive, widespread population of neurons situated beneath the pial surface of the human embryonic forebrain even before complete closure of the neural tube. These 'predecessor' cells include the first neurons seen in the primordium of the cerebral cortex, before the onset of local neurogenesis. Morphological analysis, combined with the study of centrosome location, regional transcription factors and patterns of mitosis and neurogenesis, indicates that predecessor cells invade the cortical primordium by tangential migration from the subpallium. These neurons, described here for the first time, precede all other known cell types of the developing cortex.

The question is whether these early-migrating neurons, which make it into the developing cortical regions before any local neurons originate, might be essential to laying down pathways that later develop.

There's some clever work detecting gene expression in these neurons to determine if they belong to one or another already-known neural population (they don't). And they're not like any early neurons so-far observed in any other species:

No equivalent of predecessor cells has been described in any other species. In rats there is evidence that the earliest neurons migrating tangentially to the cortex arise from the VZ of the lateral ganglionic eminence at embryonic day 12.5–13, when neurogenesis has already started in the dorsal telencephalon. In contrast, human predecessor cells invade the cortical primordium from the basal telencephalon at CS12, 1 week before the appearance of the lateral eminence. A re-examination of early neurogenesis in rodents and other species is urgently needed to determine whether predecessor cells are unique to the human brain.

So they represent an early step in a "developmental cascade" in the cortex, and they are possibly primate- or even human-speci