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Thigh and calf discrimination in the motor innervation of the chick hindlimb following deletions of limb segments

In this paper we report studies on the organization of the motor projections to chick hindlimbs lacking limb segments as a result of surgical manipulations during early embryonic development. The innervation of partial limbs, missing either a thigh or both a calf and a foot, was studied using both retrograde and orthograde horseradish peroxidase nerve-tracing techniques, as well as by serial reconstruction. In addition, [3H]thymidine autoradiography was used to characterize motoneuron production and loss. Motor organization was assessed both before and after the period of naturally occurring motoneuron death. Prior to the period of cell death, we verified by autoradiography that the organization of the motor column (i.e., motoneuron birthdates and settling patterns) was normal despite deletions of the periphery. It was also found that, initially, the entire motor column projected to the partial limbs, entering via normal crural and sciatic pathways. The proximal branching patterns of the nerves leaving the plexus were normal; however, the distal projections of the nerves which would normally serve the missing limb segment were truncated. After the period of cell death, the motor columns serving segment-deleted limbs were excessively and selectively depleted of target-deprived motoneurons. The remaining motor pools appropriately innervated their normal targets. Thus, when both thighand calf-serving motor axons invaded a given limb segment, only the axons which normally serve that segment successfully innervated it. Our findings on the innervation of partial limbs cannot be explained on the assumption that motor projection patterns are determined solely by the timing or spatial arrangement of axon arrival at the limb bud. They indicate that motor axons destined to innervate thigh and calf muscles differ from one another such that their initial growth trajectories are distinctive and their final termination sites are appropriate for the muscles available. These differences are evident both from the pattern of selective cell death and from the normal projections of the surviving motoneurons. In the chick, as in many other vertebrates, limb muscles receive motor innervation from discrete clusters of neurons in the lateral motor column (LMC) (Romanes, 1951, 1964). The motoneurons that innervate a given muscle are called the motor pool for that muscle. The motor projection to the chick hindlimb has been described using both anatomical and electrophysiological techniques (Landmesser and Morris, 1975; Landmesser, 1 This work was supported by National Institutes of Health Grant NS-14066 to M. H. V. W. was supported by United States Public Health Service Grants GM-07183, GM-07839, and NS-14066. We thank Dr. Paul Grobstein for valuable discussions and for help in writing this