The development of sensory projection patterns in embryonic chick hind limb.

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Abstract
The distribution within individual dorsal root ganglia (drg) of sensory neurons projecting to different targets in the embryonic chick hind limb was determined using the retrograde transport of horseradish peroxidase (HRP). The segmental pattern of sensory neuron projections was defined, using retrograde and orthograde HRP labeling and electrophysiological techniques, from the onset of axonal outgrowth into the limb until after the period of sensory cell death. At stages (St.) [stage] 29-30, shortly after initial axonal outgrowth into the limb, the large lateroventral neurons in the drg projected both to skin and to muscle. At St. 36-37, after cell death in the drg, cells from both the lateroventral and mediodorsal populations projected both to skin and to muscle. These 2 cell populations do not correspond to cutaneous and proprioceptive afferents, respectively. The cells projecting along individual cutaneous nerves or to individual muscles were always widely distributed throughout the ganglia. Sensory neurons cannot be specified to project to particular peripheral targets as a result of their position in the drg. Nevertheless, small clusters of cells frequently projected along the same peripheral nerve. Since there is a correlation between position in the drg and time of origin, neurons projecting to each target have a wide range of birthdates. Sensory neurons cannot, therefore, be specified as a result of their birthdate. At St. 36-38, after cell death, afferents to a given muscle or cutaneous nerve arise primarily from 2 or 3 adjacent segments out of the 8 lumbosacral segments. For muscles these are the same segments that supply the motoneurons to that muscle. Each drg sends a characteristic proportion of axons down each of several peripheral nerves in a consistent and orderly pattern. During initial outgrowth, the segmental projection pattern is similar to the pattern found in mature embryos. Thus, extensive projection errors are not made and neither cell death nor retraction of axons is necessary for establishing the appropriate connectivity pattern. The majority of neurons do not send branches down more than one peripheral nerve. Axons projecting to the same target are initially dispersed in the spinal nerves, and gradually segregate out in the plexus region, ultimately to form a separate nerve trunk. Axons projecting to different targets cross each other. Cutaneous and muscle nerves first form at the same stages. The particular pathways axons take do not depend in any simple way on either axonal position in the plexus or time of arrival at the base of the limb. Simple timed outgrowth mechanisms and models in which axons maintain constant topographical relationships with each other therefore cannot generate the observed projection pattern. The questions of whether sensory neurons are specified prior to outgrowth, whether afferents actively choose certain pathways or are passively channelled into them, and whether motoneurons might play a role in guiding afferent outgrowth are discussed.