Changes in binomial parameters of quantal release at crustacean motor axon terminals during presynaptic inhibition.

Abstract

SUMMARY1. The effects of presynaptic inhibition on quantal release of transmitter were investigated at neuromuscular junctions of the motor axon supplying one of the limb muscles of a crab (Pachygrapsus crassipes).2. Binomial analysis of transmitter release recorded at selected neuromuscular junctions with an extracellular 'macro-patch' electrode indicated high probability of release (p) from a limited number of available sites (n). During presynaptic inhibition, both n and p were reduced.3. The binomial model provided a good description of results from non-inhibited junctions. During presynaptic inhibition, results from some junctions could be described by the binomial model, while those from other junctions could not. An interpretation of this finding is that presynaptic inhibition differentially affects the probability of release at various release sites of the neuromuscular junctional complex.4. A morphological study of the region of transmitter release under the macropatch electrode was made. Release-dependent uptake of horseradish peroxidase (HRP) into presynaptic terminals was restricted to the region under the recording electrode, by perfusing the preparation with calcium-free solution containing HRP. Transmitter release, and HRP uptake, occurred only at the site of the electrode, which was filled with a calcium-containing solution. Subsequently, serial sections were prepared for electron microscopy and the region of transmitter release was reconstructed.5. Numerous axo-axonal synapses were found in the HRP-labelled region. Thus, the morphological prerequisite for presynaptic inhibition exists at the site of transmitter release, and not exclusively at a more remote region.6. The number of morphologically identified excitatory neuromuscular synapses exceeded the 'release sites' estimated from the binomial model (n) by a wide margin. Morphological differences among synapses were observed. It is proposed that not all morphologically identified synapses participated in transmitter release under the experimental conditions employed. Thus, morphologically defined synapses are * Present address:

The organization of synaptic vesicles at tonically transmitting connections of locust visual interneurons

“…Presynaptic densities in L-neuron vesicle clouds vary considerably in length, with most extending through only one or two sections but others having lengths up to 1.5 m. At arthropod neuromuscular junctions most presynaptic densities extend into only one or two serial ultrathin (70 nm) sections (Atwood et al, 1993;Jia et al, 1993;Wojtowicz et al, 1994;King et al, 1996), although Atwood and Tse (1988) reported a pattern similar to the one we find for L-neurons at crayfish neuromuscular junctions. Similarly, presynaptic densities at output synapses made in a locust thoracic ganglion by motor neurons (Watson and Burrows, 1982) and an intersegmental interneuron (Watson and Burrows, 1983) can be longer than 1 m, although most are considerably shorter.…”

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

“…At both locations, the axoaxonal synapses are capable of effectively reducing the action potential or depolarization in the terminal Segev, 1990) and thus reducing the release of transmitter. Consequently, one or a few inhibitory axoaxonal synapses can reduce the effectiveness of many excitatory neuromuscular synapses (Atwood and Tse, 1988). The occurrence of axoaxonal synapses on branches of the excitatory axon itself (Fig.…”

“…In practice, physiological measurements have not often shown such an effect; only rarely has it been shown that impulse failure occurs in excitatory terminals during inhibition (Dudel, 1965). More frequently, there is reduction in amplitude of the excitatory action potential (Takeuchi and Takeuchi, 1966;Baxter and Bittner, 19811, but inhibition can occur even without this effect (Atwood and Tse, 1988). Thus, the off-shore axoaxonal synapses are not effective enough to block action potential propagation in most cases studied to date, but the possibility remains that at higher frequencies of stimulation, or over prolonged periods, such an effect could occur.…”

Frequency-dependent selection of alternative spinal pathways with common periodic sensory input

“…Scharstein 1979;Rospars and Lánský 1993;Bressloff 1995;Lánský and Rodriguez 1999a,b;Shimokawa et al 2000;Burkitt and Clark 2000;Feng and Brown 2000;Feng 2001;Pakdaman 2001). Details on the biophysics of excitable cell membranes, during primary afferent depolarisations and shunting inhibition in particular (Atwood et al 1984; Atwood and Tse 1988;Segev 1990;Graham and Redman 1994;Walmsley et al 1995;Lamotte d'Incamps et al 1998;Lamotte et al 1999;Cattaert et al 2001), are omitted.…”