Developmental Changes in the Structure of the Synapse on the Myelinated Cell Bodies of the Chicken Ciliary Ganglion

Abstract

Electron micrographs, stained Epon-embedded sections, and silver stains of the ciliary ganglion of chickens 19 days prehatched, 4 days, 5 weeks, 6 months, and 1 to 2 years of age were studied. The majority of ganglion cells are large neurons; smaller cells are restricted to a dorsal, distal part of the ganglion. The following description applies to the large neurons. Three to twenty lamellae of loose, semicompact, and compact myelin ensheathe virtually every neuron. All these types of myelin form the sheath of a single neuron. The lamellae greatly increase in number and in compactness during the period between the 19-day embryo and the 4-day-old chick. During the period between the 4-day chick and the adult chicken, the myelin becomes only slightly thicker and denser. The calyx is a large synaptic terminal encircling virtually every neuron in the ganglion up to 5 weeks of age. At 6 months of age, the calyx appears to break up; only about half the number of neurons in the ganglion have this large terminal, while the remaining neurons have numerous relatively small, boutonlike synapses. This rather remarkable transformation in the structure of the calyx is virtually complete in the 1- to 2-year-old chickens. In these older chickens all the cells have boutons, and calyces are no longer present. The entering preterminal fiber, the calyx, the neuron, and the axon hillock can all have myelin lamellae on them. It is possible that this entire complex is effectively insulated by the myelin sheath. No synaptic discs or fusion of the membranes of the preterminal fiber and the postganglionic neuron are seen. The chick ciliary ganglion cells are the only myelinated neurons so far described which receive synapses. The neurons in the small-cell part of the ganglion do not have calyces and are not ensheathed by myelin lamellae at any age.

Localization of individual calcium channels at the release face of a presynaptic nerve terminal

“…Most nerve terminals are of such small size that, once isolated in a hydrated state, their surfaces are high ly curved and difficu It to study in detail with a contact scanning technique such as AFM. In contrast, the chick ciliary ganglion calyx synapse is extraordinary for its sheet-like presynaptic terminal that can completely envelope the postsynaptic ciliary neuron ( Figure 1A) (Hess, 1965;de Lorenzo, 1960;Landmesser and Pilar, 1972;Stanley, 1992). This nerve terminal has been used previously to record whole-terminal calcium currents (Stanley, 1989;Martin et al, 1989;Stanley and Goping, 1991;Yawo and Momiyama, 1993) and transmitter release site-associated single calcium channels (Stanley, 1991(Stanley, ,1993.…”

Correlation between transmission and structure in avian ciliary ganglion synapses

“…Further evidence of a dual mechanism of synaptic transmission, electrical and chemical, was obtained when two different ganglionic blockers were used. Figure 1 A Since the ganglion cells send only one axon to the ciliary nerve (Carpenter,191 1; Terzuolo, 1951;Hess, 1965), and since the axon diameters of these cells are unimodally distributed (Pilar & Vaughan, 1969), the area under each component of the extracellular response is 342 AGEING AND CILIARY GANGLIONIC TRANSMISSION 343 proportional to the number of ganglion cells discharged either electrically (first peak of the extracellular response) or chemically (second peak of the extracellular response). Assuming that all the cells of the large cell population are activated, either chemically or electrically, in response to supramaximal preganglionic stimulation, changes in the extracellular response can be related to changes in the mode of synaptic transmission in ganglion cells.…”

“…The morphological findings presented in this report are all from the so-called large cell portion (Carpenter, 1911;Terzuolo, 1951) of the population of ganglion cells. The synaptic regions in the small cell population have neither calyces nor myelin lamellae at any stage of development (Hess, 1965).…”

“…Such a high resistance pathway might force a significant portion of the current generated by the presynaptic action potential to flow through the post-synaptic membrane, thus giving rise to the observed electrical coupling. However, if a high cleft resistance is important for electrical coupling, it appears that it is not due to the large areas of membrane apposition produced by the calyciform presynaptic terminals, because in the adult chicken the calyces are broken up into small terminal boutons (Hatmory & Dyachkova, 1964;Hess, 1965), while electrical coupling appears to improve with age (Martin & Pilar, 1963b). Hess (1965) suggested that the myelin lamellar envelope which is known to ensheath the synaptic apparatus may be of significance for the electrical coupling which occurs in the avian ciliary ganglion.…”

ACETYLCHOLINE RECEPTORS IN THE CILIARY GANGLION AND IN THE IRIS MUSCLE OF THE CHICK: SPECIFIC BINDING AND EFFECT ON THE SYNAPTIC TRANSMISSION OF THE NEUROTOXIN FROM Naja naja siamensis

“…The 'ciliary' cells are larger than the 'choroid' cells, and their surface is almost completely covered by the calix, a large synaptic terminal surrounding the neurone as a cap. The choroid cells are smaller and have relatively few bouton-like synapses (Hess, 1965).…”