Inhibitory axoaxonal and neuromuscular synapses in the crayfish opener muscle: Membrane definition and ultrastructure

Abstract

The specific inhibitory motoneuron to the crayfish (Procambarus clarkii) opener muscle provides neuromuscular synapses to the muscle fibers and axoaxonal synapses to the excitatory motor nerve terminals. Freeze fracture of the membrane in both types of synapses show that the presynaptic active zone consists of clusters of large particles (putative calcium channels), which are often encircled by large depressions representing fused synaptic vesicles on the internal leaflet or P face of the presynaptic membrane. Corresponding pits and protrusions mark the external leaflet or E face of the presynaptic membrane. The postsynaptic receptor-bearing surface, characterized for neuromuscular synapses only, consists of rows of particles on both leaflets of the muscle membrane. The organization differs from that seen at excitatory synapses where particles occur only on the E-face leaflet. Serial thin sections of nerve terminals reveal that neuromuscular synapses are significantly larger in proximal fibers than in their central counterparts and support a greater number of presynaptic dense bars (active zones). Axoaxonal synapses also show regional differences; almost three times as many occur in the proximal region compared with the central region. Most synapses possess a single dense bar. The majority of synapses formed by the inhibitory axon are neuromuscular; a minority are axoaxonal. The latter occur in various locations along the excitatory nerve terminals as well as on branches of the axon itself. This preterminal or "off-shore" location could act to cut off entire populations of excitatory synapses or reduce the amplitude of the preterminal action potential.