Formation of the receptive fields of leech mechanosensory neurons during embryonic development

We have charted the embryonic development of the epidermal receptive fields of the PV and PD mechanosensory neurons present in each segmental ganglion of the ventral nerve cord of the glossiphoniid leech Haementeria ghilianii. The receptive field of either of these neurons is established by several peripheral axons, each of which grows into its own skin territory, so that the receptive field is subdivided into a quiltwork of contiguous, mutually exclusive subfields of various sizes. The largest subfield develops first from the primary peripheral axon of the PD or PV neuron. The PD and PV primary axons grow directly to their respective territories and begin to innervate them at approximately the same time (see also Kuwada, J.Y., and A.P. Kramer (1983) J. Neurosci. 3: 2098-2111). The smaller secondary and minor subfields develop later from the secondary and intersegmental peripheral axons, respectively. These axons, too, grow directly to their appropriate skin territories. The arborizations of the peripheral axons expand until the adult receptive field pattern is established late in embryogenesis; they do not appear to initially overgrow and later trim down to the normal boundaries of the adult receptive field. The receptive field of the PV neuron develops from a stereotyped skeletal branching pattern of the peripheral axons that is elaborated in a regular way to form a grid-like pattern that matches the arrangement of muscle fibers in the body wall. Thus, this branching pattern may be the result of axon growth along prespecified pathways, perhaps delineated by the muscles. Throughout embryonic development, as in the adult leech, axon branches of neighboring homologous P neurons overlap considerably, but separate axon branches of the same neuron are virtually non-overlapping. These observations suggest that developing branches of a neuron are excluded from territory occupied by other branches of the same cell, in contrast to branches belonging to different neurons which can occupy the same territory.