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Strieder Essay 1

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Some Thoughts on "Naturalization" and Morphological Homology

When cells migrate from a subpallial germinal zone into the dorsal pallium, does that mean that the dorsal pallium is partly subpallial? More generally, when an adult cell group is derived from several different precursor zones, how does that influence our thoughts about its homology? We usually take the site of a structure’s developmental origin as a strong indicator of its homology (i.e., structures that resemble each other in terms of where they develop from are probably homologous to one another), but what do we do when an adult structure comes from several different precursor regions? I was discussing these questions with Laura Bruce and Loreta Medina late one night in Murcia, towards the end of a big meeting there, when Loreta drew an interesting analogy. She suggested that the GABAergic cells that migrate from the subpallial ventricular zone into the dorsal pallium might be considered as "naturalized immigrants" into the dorsal pallium. Being a naturalized U.S. citizen, I think I understood what she meant (but, as they say, don’t blame her for anything I write). Since then, I have thought some more about this and found it to be a rather complex, but still fruitful, analogy. Although I have not come to any firm conclusions, I thought I’d share my thoughts with you. Perhaps collectively we can sort it all out.

As I see it, naturalized citizens are fully integrated into their adopted (adoptive?) country but need not drop all of their native cultural heritage. To become a naturalized citizen of the US, for example, you must speak a minimum amount of English, know something about the history and governance of the US, and repudiate your allegiance to "any foreign prince or potentate". You need not, however, become an "average citizen". They used to talk about America being a "melting pot" but I think it is really more like a stew, composed of many different chunks that all contribute to the overall flavor yet retain some identity. Naturalized immigrants may imbibe a great deal of "mass culture" (e.g. TV) but still hang out with their "own kind", practice a different religion, eat different (‘ethnic") foods, or buy a satellite dish to watch foreign channels. In other words, cultural integration comes in many different forms and can vary in extent. Naturalization has relatively little to do with how much of the native identity has been surrendered.

So, assuming I’ve got this right, let’s examine how the naturalized immigrant analogy might apply to brains, and let’s consider first the cells that emigrate from the subpallium into the dorsal pallium (neocortex in mammals) where they ultimately become GABAergic interneurons. These immigrant neurons are integrated with their native neighbors in the sense that they interconnect with other dorsal pallial neurons, but this is a relatively weak form of integration (perhaps analogous to the communication between tourists and native residents). Better evidence for "full integration" would be to show that the immigrant cells are induced to express some genes that they would not have expressed had they "stayed home". To my knowledge, we do not know how the development of the GABAergic immigrants is influenced by their "host region" (I suspect people are working on this). Until we have such evidence, it is difficult to know how "fully integrated" the cellular immigrants are. Even less clear would be the point at which these immigrants would earn the appellation "naturalized immigrants". One might call the immigrants "naturalized" if they "vote" together with the other cells in some computational sense, but what precisely that would mean is unclear. Thus, it is possible to make the analogy work in this case, but proving developmental integration is difficult and the naturalization criteria are rather arbitrary.

Now let us consider another case, where the degree of immigrant integration is likely to be even lower. As I understand it, David Perkel, Tony Reiner, Sarah Bottjer and others have collectively shown that some neurons in the avian area X resemble those of the mammalian striatum, while others in the same area bear a striking resemblance (in terms of physiological properties and histochemistry) to cells in the mammalian globus pallidus. This suggests that perhaps there has been some developmental intermingling of cells (though this is not the only imaginable explanation) to create area X but that the different immigrant cell populations have retained much of their native characteristics. To really show this, of course, one would have to conduct experiments. But let us assume for the moment that area X really forms by the developmental intermingling of "striatal" and "pallidal" cell populations. Which population should be considered "naturalized immigrants" and which should be considered to provide area X with its "national identity"? Should it be a majority decision? Before you say yes, consider that many countries are dominated (both culturally and militarily) by a minority of their population. Should national identity be decided by the cells that reached their ultimate target via the shortest route (e.g. by radial rather than tangential migration)?

Proceeding to even more extreme examples, consider the case of microglia. As I understand it (from textbooks, admittedly), microglia probably invade the brain during development and thus become, essentially, the brain’s resident macrophages. In a sense, they are "permanent residents", doing some of the work that the other glia are either unwilling or unable to do (I suppose my pro-immigrant bias is showing here). If this is correct, should we consider the microglia to be naturalized citizens of whatever brain area they are in? Or should we specifically exclude the microglia when we talk about a particular brain area in homology comparisons? Similarly, we know from Drew Noden’s work that the endothelial cells lining the brain’s blood vessels are derived from mesoderm rather than neurectoderm (which gives rise to the neurons and most of the glia). Functionally, the endothelial cells are certainly integrated rather tightly with the neurons that are nearby (just imagine what would happen to those neurons if there were no endothelial cells), but does that mean they are naturalized citizens of the brain? Or have we crossed a line into fruitless mental exercises?

I don’t know, but I come away from these musings with the following tentative resolutions. One, where cells come from in terms of lineage is less important than how tightly they are integrated with other cells. Two, functional integration (e.g. synaptic communication) is less important for "naturalization" than developmental integration (i.e. being developmentally influenced by your neighbors). Three, to think clearly about this issue, it is necessary to distinguish between homologies (or identities) at the cellular and aggregate levels of analyses (e.g. aggregates may be homologous as aggregates, even though not all of their constituent cell populations are homologous as cell populations). Four, none of this may matter all that much for homology comparisons unless there are significant differences in developmental origin and/or cell composition between similar structures in different species (e.g. the dorsal pallium may receive subpallial immigrants in most species, as Luis Puelles has suggested; but note that Rakic and his collaborators have shown that humans differ from other species in having telencephalic cells contribute to part of the dorsal thalamus). Five, in the few cases where these issues become important (where there are significant differences between species), some arbitrariness tends to creep in (i.e. we humans will be tempted to decide by committee or ex cathedra which cell population is immigrant and which is native, and how much developmental integration is sufficient to consider the immigrants naturalized).

Of these conclusions, only the fifth one bothers me because I like to think that structural identity and homology are not simply constructs that we impose (arbitrarily) on nature. The dividing line between a limb and a trunk may be arbitrary to some extent, but I think limbs and trunks are nonetheless distinct entities, independently of whoever is arguing about them. Similarly, I hope that the dorsal pallium is an entity independently of whatever a committee of scientists decides are its critical features (or its identity-conferring cells). Perhaps I am philosophizing excessively, but to me this issue is important, and I think it can be resolved. For me, resolution lies in the observation that there are (seem to be?) such things as developmental units, or modules, that develop largely independently of one another. When these modules form, they work with whatever materials they can use, much as a whirlpool incorporates whatever water molecules (or swimmers) it can pull in. From this perspective (which I would call a "dynamic systems" perspective), the "immigrants" I talked about before might be the leaves that fell into river but are sucked into the whirlpool just like the water is. The leaves become part of the whirlpool (i.e. naturalized if you will) as soon as they become part of the overall whirlpool pattern. Returning to neurobiology, I think that the major challenge for neurobiologists is to figure out what kind of dynamic patterns are involved in creating particular brain areas (e.g. the dorsal pallium) and how any immigrant cell populations are integrated into those processes.

In sum, I think that the term "naturalization" can be used to denote cells that become developmentally integrated with other cells in a distant brain region. In contrast, non-naturalized immigrants do not interact developmentally with their "host" cells, which means that the resultant adult structure is heterogeneous or "composite".

I know that the issues I have discussed here don't bear on the question of how to name various telencephalic areas in any obvious way, but I think they are relevant to some of the deeper issues that are at stake and bound to come up. I hope my musings are helpful at least insofar as they stimulate thought.
Georg Striedter (gstriedt@uci.edu),
Aug 29, 2001

Acknowledgements: Thanks to Loreta Medina and David Perkel for feedback.

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