Ultrastructure of Synapses in the Waking State

Summary

Membrane faces of synapses from pigeon optic tectum as well as from rat and cat spinal cord have been examined in a large number of freezeetched replicas. The data have been compared with those of conventional thin section electronmicroscopy. Some progress has been made to analyse the main features of presynaptic membranes morphometrically.

The presynaptic membrane (active site) is characterized according to Pfenninger et al. (1972) by a curving indentation (“lifting”) toward the presynaptic cytoplasm, and, furthermore, by the presence of 200 Å micropits (as seen from outside) and protuberances or craters (as seen from the inside), respectively. These membrane modulations are specific for the presynaptic area and their sites correspond closely to the holes in the presynaptic vesicular grid.

The concept of a dynamic membrane organization (Streit et al., 1972) stems from the fact that the “lifting” of the membrane as well as the “wrinkling” and the relative number of open protuberances (representing vesicular attachment sites) is strongly enhanced in the waking as compared with the anaesthetized state. Thus, the “textbook appearance” of the synapse with rectilinear and parallel synaptic membranes probably represents an unphysiological state, inasmuch as most of the preparations have been made with anaesthetized material. The dynamism of the presynaptic membrane as revealed by morphometric analysis of unanaesthetized preparations provides further support to the vesicle hypothesis of transmitter release.

The postsynaptic membrane is characterized by a sharply circumscribed aggregation of 80–130 Å particles (Sandri et al., 1972) which are characteristic of the outer membrane leaflet. The inner leaflet contains particles of similar size (but perhaps different biochemical composition) which are more diffusely scattered over the membrane. The particle aggregations in the postsynaptic plasmalemma appear to correspond to regions of subsynaptic membrane specialization in terms of differential sensitivity to specific transmitter molecules.

Supported by grants from the Swiss National Foundation for Scientific Research Nr. 3.133.69, 3.134.69, 3.366.70 and from the Dr. Eric Slack-Gyr Stiftung in Zürich.

The collaboration of C. Sandri, K. Pfenninger, and E. Kawana, and the skillful assistance by Miss C. Berger and A. Fäh is gratefully acknowledged. The drawing was prepared by Miss R. Emch and the manuscript by Miss U. Fischer.