Frugal to the point of vacuity

What does it take to get Carl Zimmer to review your research in the New York Times?

I suppose it helps to be at Harvard. It also helps to have a combination of subjects — evolution and the human brain — that Zimmer has written about in the past. It helps to have a paper with lots of very pretty diagrams — the authors' hypothesis is professionally illustrated. It's also a good idea to have a vast sweeping explanation for the exceptionalism of the human brain. In this case, they call it the Tethering Hypothesis, and it's supposed to explain how humans evolved all these remarkable cognitive abilities.

The human cerebral cortex is vastly expanded relative to other primates and disproportionately occupied by distributed association regions. Here we offer a hypothesis about how association networks evolved their prominence and came to possess circuit properties vital to human cognition. The rapid expansion of the cortical mantle may have untethered large portions of the cortex from strong constraints of molecular gradients and early activity cascades that lead to sensory hierarchies. What fill the gaps between these hierarchies are densely interconnected networks that widely span the cortex and mature late into development. Limitations of the tethering hypothesis are discussed as well as its broad implications for understanding critical features of the human brain as a byproduct of size scaling.

You know what you don't need? Data, or a hypothesis that makes sense.

The paper is largely a review of neuroanatomy, describing features of the human brain that we've known about for a long, long time…except now we can illustrate them with lovely color diagrams and fMRI scans. Here's an illustration of the problem in human evolution:

There are areas of the brain that we know what they do: in red, for instance, is the primary somatosensory cortex, which is a map of muscles and sensory areas on our skins, while blue is the primary visual cortex, which is where information from our eyes is processed. In between these known areas are great beige unknowns — regions of the brain called association cortex, which integrate information from various other regions in complex ways. Our primary somatosensory and visual cortices aren't much bigger than those of a chimpanzee, which makes logical sense, since there isn't much difference in surface area or visual acuity between us, and most of the growth has occurred in the association cortex.

All well and good. The question is, what made our association cortex expand in our evolution, and how is that expansion related to specific human intellectual capacities? Those are good questions, and I'd be curious to see them answered. Too bad this paper doesn't.

One problem is that it is a review paper and really doesn't test anything — it catalogs some existing knowledge about brain organization and then throws out this Tethering Hypothesis to explain it all, which it doesn't. I do like the fact that it suggests that most of our abilities are spandrels, not explainable as adaptations, and that what it proposes is that novel abilities arose from regions of the brain that were not constrained by ancestral functional requirements. I just don't see how their mechanism explains that.

Here's one short paragraph from the paper that neatly summarizes their hypothesis.

The idea of some form of radiation outward from core organizing centers is appealing because the hominin cerebral cortex vastly expanded in a short time. It seems implausible that molecular gradients could emerge fast enough to specify new cortical areas, although developmental expression patterns have clearly been modified. Building from Rosa and colleagues’ ideas about visual cortex organization, we propose a more general tethering hypothesis to explain how new features of cortical organization might have emerged during the rapid evolutionary expansion of the cerebral mantle. The word ‘tether’ is used to emphasize that the expanding cortical plate is tethered to gradients that initially evolved in a cortex with a far smaller surface area. Much as taffy, being pulled apart, thins until it breaks in the middle, the expanding cortical zones far from the strong constraints of developmental gradients and sensory input may become untethered from the canonical sensory–motor hierarchies.

OK, that begs the question: why did the hominin cerebral cortex expand in the first place? They keep talking about this "expanding cortical plate", but not why it was expanding or why it necessitates new organizing centers. The taffy metaphor is also telling; why are they talking about things being pulled apart, when expansion of the brain is not caused by external forces pulling on it, but on internal forces of growth generating more tissue between known cortical zones?

I'm also put on edge by the phrase "It seems implausible that…", especially when applied to something that doesn't seem implausible at all. Why balk at a timescale of several million years to evolve a use for a bit of extra brain matter?

But even worse, nervous systems growing bigger is what I study. My Ph.D. research was on connectivity in the developing spinal cord of zebrafish, for instance.

The first neurons in the zebrafish embryo emerge at about 18 hours after fertilization, at a time when the nascent spinal cord is about 2mm long, in total. Cells in the hindbrain send axons all that distance (2mm is a long way in an embryo!), and as they grow, they make a little knot of synapses every 40-50µm with cells called primary motoneurons.

That's in the embryo. In the adult, the spinal cord is roughly 4cm long — there's been a 20-fold expansion in size. What do you think happened to that earlier array of cells? Did the system stretch and break?

No, it grew. In the adult, the same hindbrain neurons are still present, and their axons still reach all the way back to the tailtip. And the same motoneurons are still present, they're just spread out more to be separated by 1-1.5mm, and they still retain the same synapses.

I also did research on the earliest neurons to differentiate in the grasshopper nervous system. I studied Q1, a neuron that established one of the commissures in the grasshopper ganglion. That story is a little different: Q1 doesn't seem to have any function in the adult, and in fact looks to be abandoned and gone. But what it does is send the first slender thread across on a specific pathway; it pioneers a route across the nervous system, and then other axons pile on and follow it across. It's like sending a kite string across a chasm, then using the string to pull a rope across, and then using the rope to pull a cable across, and pretty soon you've got a bridge — and it's doing this as the chasm is widening, because like the zebrafish, the grasshopper is also growing substantially during these events.

Growth is an integral process in the development of the nervous system. Without specific evidence that these developmental mechanisms break down during growth (which seems implausible to me…), why would you postulate that a failure of developmental processes was an essential element of human evolution? A tripling of brain size from the human-chimpanzee common ancestor to the modern human seems like a small shift relative to the much larger expansion of the human fetal brain to the adult brain.

What I'd like to see, and did not find in this paper, are comparative developmental studies. When these various cortical regions of the brain are specified or establishing connectivity, how far apart are they in different species? Compare mouse and rat, for instance, or rhesus monkey and human. I suspect that in early embryos, the distances, and their relative differences, will be minuscule, and that signaling centers will be close enough that it will seem silly to argue that broad patterns of connectivity would be unable to form in the biggest brains, leaving gaps that need to be filled in by novel mechanisms and structures.

But again, the paper doesn't look at any of that at all. I found one paragraph that briefly discusses other observations that association cortex matures later than other regions of the brain, and that's about it — it is definitely not sufficient information to argue that association cortex is out of reach of intrinsic signaling gradients in the early brain.

At least the first subtitle in the paper is "A Speculative Hypothesis," which is entirely accurate. I don't see how it justifies the praise it was given in Carl Zimmer's article.

Dr. Sherwood, the George Washington University expert, praised the hypothesis for being “fairly frugal.” The emergence of the human mind might not have been a result of a vast number of mutations that altered the fine structure of the brain. Instead, a simple increase in the growth of neurons could have untethered them from their evolutionary anchors, creating the opportunity for the human mind to emerge.

Oh, wait. When the best thing you can say about a hypothesis is that it is "fairly frugal", that's not much praise at all.

Buckner RL, Krienen FM (2013) The evolution of distributed association networks in the human brain. Trends Cogn Sci 17(12):648-65.