Cryptic responses to tissue manipulations in avian embryos

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Experimental embryology performed on avian embryos combines tissue manipulations and cell-labeling methods with increasing opportunities and demands for critical assays of the results. These approaches continue to reveal unexpected complexities in the normal patterns of cell movement and tissue origins, documentation of which is critical to unraveling the intricacies of cell and tissue interactions during embryogenesis. Viktor Hamburger's many pioneering contributions helped launch and promote the philosophical as well as technical elements of avian experimental embryology. Furthermore, his scholarship and profoundly positive presence influenced not just those of us fortunate to have trained with him, but several generations of developmental biologists. The first part of this article presents examples of the opportunities and rewards that have occurred due to his influences. Surgical manipulation of avian embryonic tissues always introduces a greater number of variables than the experimenter can control for or, often, readily identify. We present the results of dorsal and ventral lesions of hindbrain segments, which include defects in structures within, beside, and also at a considerable distance from the site of lesion. Extramedullary loops of longitudinal tract axons exit and re-enter the neural tube, and intra-medullary proliferation of blood vessels is expanded. Peripherally, the coalescence of neural crest- and placode-derived neuroblasts is disrupted. As expected, motor neurons and their projections close to the sites of lesion are compromised. However, an unexpected finding is that the normal projections of cranial nerves located distant to the lesion site were also disrupted. Following brainstem lesions in the region of rhombomeres 3, 4 or 5, trigeminal or oculomotor axons penetrated the lateral rectus muscle. Surprisingly, the ability of VIth nerve axons to reach the lateral rectus muscle was not destroyed in most cases, even though the terrain through which they needed to pass was disrupted. These axons typically followed a more ventral course than normal, and usually, the axons emerging from individual roots failed to fasciculate into a common VIth nerve, which suggests that each rootlet contains pathfinder-competent axons. The lesson from these lesions is that surgical intervention in avian embryos may have substantial effects upon tissues within, adjacent to, and distant to those that are being manipulated.