Development of the spinal nerves in the lamprey: II. Outflows from the spinal cord

Abstract

During a series of studies on the development of spinal nerves in the tail of larval lampreys (13 mm, 26 days), Lampetra japonica, we observed outflows of cytoplasmic processes (cytoplasmic outflow) or whole cell bodies (cellular outflow) from the neural tube or from the cord. Three types were distinguished according to their site of exit from the surface of the neuraxis. The dorsal outflow (DO) is the cellular outflow seen on the midsagittal surface of the dorsal wall of the caudalmost region of the neural tube, just rostral or caudal to the opening in the dorsal tube wall. It is hypothesized that the cells from the dorsal neural tube become polymorphous cells scattered in the extramedullar space. The dorsolateral outflow (DLO) is the cytoplasmic outflow emerging from the dorsolateral aspect of the spinal cord at the intermyotome level. DLO fibers are non-myelinated fibers arising from the dorsolateral tract (DLT) and, after piercing the basal lamina and the glia limitans, run in the myosepta laterally to spread along the deep surface of the dermis. DLO fibers terminate in two different ways: those of one group pierce the dermis and the basal lamina to end as intraepidermal free endings that contain aggregates of clear vesicles, and those of the other group form varicosities that lie within depressions on the lateral cell surface of myotomes. DLO fibers in the extramedullary space characteristically lack any sheaths, including the basal lamina. The ventrolateral outflow (VLO) represents primitive ventral roots consisting of both the cytoplasmic and the cellular outflows: the former shows the axonal outgrowth from primitive somatomotor neurons, and the latter is represented by elongated cells derived from the glia limitans, extending along the axonal processes to form the Schwann cell sheath around the proximal portion of the ventral root axons. The basal lamina covering the cord does not extend along the VLO fibers. The developing ventral root contains axons at different stages of differentiation. Some axons end on the medial surface of the myotome at the midsegmental level to form neuromuscular junctions. However, axonal processes of primitive motoneurons form close contacts with muscle cells by means of small cytoplasmic projections that contain no synaptic vesicles and lack the basal lamina interposed between them. The proposed sequence of development, based on stages in caudal to rostral sections, is the DO, the DLO, and then the VLO.(ABSTRACT TRUNCATED AT 400 WORDS)

Development of Cephalic Neural Crest Cells in Embryos of Lampetra japonica, with Special Reference to the Evolution of the Jaw

“…In the present study, the morphological distribution pattern of crest cells in L. japonica has been described primarily based on SEM observation. Although there have been several histological (von Kupffer, 1896;Damas, 1944;Johnels, 1948;Nakao and Ishizawa, 1987) and experimental works (Newth, 1956;Langille and Hall, 1988) on the lamprey crest cells, this is the first to provide threedimensional data on crest cell distribution in this group of animals. The DiI injection also revealed that our speculation concerning crest cell origin along the neuraxis and their distribution was consistent with the labeling pattern, as well as with previous mapping performed by Langille and Hall (1988).…”

The evolution and elaboration of vertebrate neural crest cells

“…Are they central nervous system derived glia, like the spinal cord derived glial cells that contribute to the perineurium around vertebrate motor nerves [44,45,46 ], or are they more like neural crest derived Schwann cells? Neural crest cells emigrate from the chick spinal cord long after the 'usual' period of neural crest cell emigration is over [47].…”

Cranial and Spinal Nerve Organization in Amphioxus and Lampreys: Evidence for an Ancestral Craniate Pattern

“…It is unclear, however, how the somatic motoneurons in craniates relate to those that are present throughout almost the entire neuraxis in amphioxus but never project out of the CNS. The existence of a relationship would require that axons of somatic motoneurons pass through the basal lamina [23]. It is possible that growth cone-associ ated proteases [46] help somatic motoneurons to digest their way through the basal lamina to form ventral roots, much as cancer cells digest their way through the basement membrane around blood vessels 196].…”