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Neuroanatomy

From fin to forelimb

The vertebrate invasion of land was made possible in part by evolution of the tetrapod forelimb from the fish pectoral fin. But what changes occurred in neural control during this transition?

Robert Baker and colleagues have tackled this question using a thorough application of comparative neuroanatomy (L.-H. Ma et al. Nature Commun. 1, 49, doi:10.1038/ncomms1045; 2010) Their study centred on the developmental biology of several species of ray-finned fish, which are by far the largest group of extant fish. But it also included lobe-finned fish (a lineage that led to tetrapods) and cartilaginous fish such as sharks.

Motor-neuron innervation in tetrapods (forelimb) and fish (pectoral fin) arises from the spinal cord. But for ray- and lobe-finned fish, there is evidence that these nerves also originate in the hindbrain. In following up that evidence, the authors looked at the gross anatomy of the developing pectoral fin buds of various ray-finned fish. They found that they all have a similar organization of the buds themselves, of the myotomes that give rise to muscles, and of the neuroepithelium that generates pectoral motor neurons. Using dye-labelled fin buds (pictured here in a species called the plainfin midshipman fish, attached to its egg yolk), the authors also demonstrated that the motor neurons project from both the hindbrain and the spinal cord.

Studies with transgenic zebrafish, containing a fluorescently tagged enhancer that reports the activity of the developmental gene hoxb4a in motor neurons, confirmed the mapping of pectoral-fin neurons. Further work involved injection of the messenger RNA for a photoactive fluorescent protein, kaede, into zebrafish embryos. The labelled neurons could then be followed during development, crucially showing that they develop in situ rather than migrating to their final location.

Baker and colleagues' extension of their study to lobe-finned and cartilaginous fish provided evidence that, in these groups too, pectoral-fin motor-neuron control is exercised from the hindbrain as well as the spinal cord. Overall, the authors conclude that this dual contribution is the ancestral condition in vertebrates. As to the functional context, they speculate that the advent of spinal-only motor innervation of the forelimb allowed another notable characteristic of tetrapods compared with fish — their greater freedom of head movement.

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Ridd, K. From fin to forelimb. Nature 466, 701 (2010). https://doi.org/10.1038/466701a

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