When the nerves of isolated frog sartorius muscles were stimulated at 10 Hz, synaptic vesicles in the motor nerve terminals became transiently depleted. This depletion apparently resulted from a redistribution rather than disappearance of synaptic vesicle membrane, since the total amount of membrane comprising these nerve terminals remained constant during stimulation. At 1 min of stimulation, the 30% depletion in synaptic vesicle membrane was nearly balanced by an increase in plasma membrane, suggesting that vesicle membrane rapidly moved to the surface as it might if vesicles released their content of transmitter by exocytosis. After 15 min of stimulation, the 60% depletion of synaptic vesicle membrane was largely balanced by the appearance of numerous irregular membrane-walled cisternae inside the terminals, suggesting that vesicle membrane was retrieved from the surface as cisternae. When muscles were rested after 15 min of stimulation, cisternae disappeared and synaptic vesicles reappeared, suggesting that cisternae divided to form new synaptic vesicles so that the original vesicle membrane was now recycled into new synaptic vesicles. When muscles were soaked in horseradish peroxidase (HRP), this tracerfirst entered the cisternae which formed during stimulation and then entered a large proportion of the synaptic vesicles which reappeared during rest, strengthening the idea that synaptic vesicle membrane added to the surface was retrieved as cisternae which subsequently divided to form new vesicles. When muscles containing HRP in synaptic vesicles were washed to remove extracellular HRP and restimulated, HRP disappeared from vesicles without appearing in the new cisternae formed during the second stimulation, confirming that a one-way recycling of synaptic membrane, from the surface through cisternae to new vesicles, was occurring. Coated vesicles apparently represented the actual mechanism for retrieval of synaptic vesicle membrane from the plasma membrane, because during nerve stimulation they proliferated at regions of the nerve terminals covered by Schwann processes, took up peroxidase, and appeared in various stages of coalescence with cisternae. In contrast, synaptic vesicles did not appear to return directly from the surface to form cisternae, and cisternae themselves never appeared directly connected to the surface. Thus, during stimulation the intracellular compartments of this synapse change shape and take up extracellular protein in a manner which indicates that synaptic vesicle membrane added to the surface during exocytosis is retrieved by coated vesicles and recycled into new synaptic vesicles by way of intermediate cisternae.

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Evidence for recycling of synaptic vesicle membrane during transmitter release at the frog neuromuscular junction

Degeneration and regeneration of the nervous system

The retinae of monkey and man have been studied by electron microscopy to identify cell types, their processes and synaptic contacts. In the inner plexiform layer, the morphological characteristics of the three types of cells (bipolar, ganglion and amacrine) are described and seven synaptic relationships are identified. The bipolar terminals contain ribbons at points of synaptic contact, and, at these points, there are typically two postsynaptic processes, one a ganglion cell dendrite, the other an amacrine cell process. This synaptic arrangement is here termed a dyad. The amacrine cell processes themselves make synaptic contacts with ganglion cell dendrites and somata, other amacrine cell processes, and, most frequently, with the bipolar cell terminals. Often, the amacrine-bipolar contact is adjacent to a bipolar-amacrine junction, forming a reciprocal synaptic arrangement between the bipolar and the amacrine. In the more peripheral retina, large bipolar cell terminals (probably of rod bipolars) are occasionally observed adjacent to the perikarya of the ganglion cells. At these junctions, areas of fusion between the plasma membranes are seen, suggesting that such axosomatic junctions could be electrical. In the outer plexiform layer, synapses have been identified only in the receptor cell bases where receptor cells contact bipolar and horizontal cell processes. Synaptic contacts of the horizontal cells have not been clearly identified, but their strategic terminations in the receptor cell ending are described and interpreted as possibly synaptic. A model of the retina, based on the described anatomy, is presented and correlated with ganglion cell physiology.

Organization of the primate retina: electron microscopy.

Synaptic patterns on different cell types in the different laminae of the cat visual cortex. An electron microscope study.

The formation of synaptic junctions in developing rat brain: A quantitative electron microscopic study

Publisher Summary This chapter focuses on the morphology of specialized neuronal contacts in general and of synaptic contacts in particular. The term “synapse” is used as a morphological term to describe specialized regions of contact between nerve cells and between nerve cells and effector organs. The structure of this specialized region is of crucial importance. Whereas epithelial cells in general show symmetrical contact regions such as the desmosomes and tight junctions the nervous system shows, in addition, asymmetrical contact regions, the “synaptic thickenings”. It is emphasized that, in addition to transmission of impulses, the organization of neuroneuronal junctions is likely to include other important properties. The interaction between neurons by which a nerve cell can maintain or even stimulate the growth and maturation of an innervated structure is likely to involve neuronal contacts, as is the ability of developing and regenerating axons to grow to and make contact with specific cell groups. Although relatively little is known about these aspects of neuroneuronal interaction they cannot be ignored when the morphology of synaptic contacts is being considered.

R.W. Guillery

Papers

Synaptic Morphology in the Normal and Degenerating Nervous System