Fine structure of dendritic and axonal growth cones in embryonic chick spinal cord

Abstract

Our preliminary electron microscopic observations of embryonic chick spinal cord indicate that the majority of synapses in the cervical cord at the fourth and sixth days of incubation are found in the marginal layer rather than the mantle layer. These findings raise two basic questions about the type of connections in the marginal zone during the first week of development: are all these early synapses axondendritic, and are synaptic junctions present on axonal and dendritic growth cones? Since criteria for distinguishing between axonal and dendritic growth cones are scarce or nonexistent, serial section electron microscopy was employed to definitively identify the two types of terminals.Two types of dendritic growth cones are present in the marginal layer during the first week of development. The first type is distinguished by a dendritic stalk which expands into a club-shaped or bulb-like terminal. A characteristic feature of this type of dendritic ending is the presence of numerous vesicles which vary in diameter from about 1000 A to 2500 A. Its cytoplasm has a floccular appearance and is frequently electron lucent. In contrast, the second type of dendritic terminal is electron dense, has a consistently homogeneous appearance, and usually lacks the large vesicles of the first type. The shape of the second type is a finger-like process (flopodium) roughly of the same diameter as the main dendritic trunk. Evidence is presented that some dendritic growth cones observed in this study represent growing, motile processes rather than quiescent enlargements. Synapses on dendritic growth cones are quite numerous and, in addition, the first synapses on dendrites appear to form on growth cones. The hypothesis is put forward that synapses on dendritic growth cones are incorporated onto the dendritic trunk as the terminal continues to grow.Axonal growth cones may be distinguished from dendritic growth cones on the basis of their overall morphology and their cytoplasmic components. An axonal growth cone is, in general, a larger and more irregular structure than the dendritic terminal. This irregularity is due to the large number of processes radiating away from the terminal enlargement or varicosity. While dendritic terminals almost always have finger-like projections, processes of axonal growth cones are more often sheet-like extensions of cytoplasm (foliopodia). Another important difference between axonal and dendritic growth cones is that ribosomes in axonal varicosities are infrequently encountered and rarely aggregated into polysomes as in dendritic terminals. Axonal growth cones are occasionally observed to be presynaptic to a dendrite during the first week of development.This investigation deals with two aspects of early synaptogenesis in the chick embryo; the frequent occurrence of axodendritic synapses in the marginal zone, and the presence of synapses on axonal and dendritic growth cones, On the basis of Golgi impregnations, Cajal ('09, '60) 108ROBERT P. SKOFF AND VIKTOR HAMBURGER dendrites grow into the...

Temporal and spacial relationships between PSA-NCAM-expressing, newly generated granule cells, and radial glia-like cells in the adult dentate gyrus

“…Second, strongly PSA-NCAM-expressing dendrites have an irregular surface. Similar structures have been seen in developing dendrites and dendritic growth cones (Skoff and Hamburger, 1974;Miller and Peters, 1981). Third, PSA-NCAM-expressing dendrites hardly possessed dendritic spines, which are frequently found in mature dendrites.…”

Synaptogenesis of the Calyx of Held: Rapid Onset of Function and One-to-One Morphological Innervation

“…This observation must be further evaluated but leads to the intriguing hypothesis that calyx growth is limited to only a portion of the surface of the MNTB cell, as proposed by Jhaveri and Morest (1982) for auditory nerve innervation of the chick nucleus magnocellularis. Insertion of postsynaptic densities (Skoff and Hamburger, 1974;Oppenheim et al, 1975;Vaughn, 1989) or the appearance of polarized flocculent cytoplasm (Jhaveri and Morest, 1982) before innervation has been documented in other systems. Although we did not observe either of these structural arrangements, it seems likely that signals originating from the MNTB cell, and not the calyx-forming axon, determine that a calyx terminal should develop.…”

Developmental course of EphA4 cellular and subcellular localization in the postnatal rat hippocampus

“…To facilitate their visualization, some cellular profiles displayed in the figures were colored in light blue, green, lavender, pink, or yellow, using the Layer tool and the Difference Blending option in Adobe Photoshop CS. Cellular profiles were identified in EM according to criteria defined by Peters et al (1991), Skoff and Hamburger (1974), and Deitch and Banker (1993). Processes of protoplasmic astrocytes were recognized by their irregular and angular shapes, which distinguished them from neuronal profiles having a characteristic rounded shape.…”

“…Axon terminals corresponded to enlarged portions of axons containing aggregated synaptic vesicles and often showing a synaptic specialization. Axonal growth cones were identified as considerable enlargements of axons, presenting a dark cytoplasm filled with large amounts of smooth endoplasmic reticulum and pleomorphic vesicles (Deitch and Banker, 1993;Peters et al, 1991;Skoff and Hamburger, 1974). They were distinguished from dendritic growth cones by their more frequent filopodial extensions, which were often contacting dendritic branches rather than axon terminals.…”