Mechanisms of action potential propagation failure at sites of axon branching in the crayfish.

Abstract

SUMMARY1. The phenomena leading to action potential conduction block during repetitive stimulation of the excitor axon of the opener muscle in the crayfish walking leg were studied.2. Action potentials, recorded extracellularly with micro-electrodes, failed to propagate past sites of axonal bifurcation following at least 3000 impulses; reduction of the rate or brief cessation of stimulation resulted in restored conduction.3. Failure occurred initially at branch points located most peripherally and then more centrally as stimulation continued; this centripetal progression of the site of block resulted in a stepwise reduction of the number of synaptic terminals from which transmitter was released.4. Prior to conduction failure, the conduction velocity and the sodium inward current of the action potentials decreased.5. Local application of hyperpolarizing current or of physiological saline with low [K+] in the vicinity of a block can restore propagation; thus depolarization of the membrane most probably causes failure.6. Soaking the preparation for as long as 2 hr in the metabolic inhibitor 2,4-dinitrophenol had no effect on the number of stimulus impulses before initial conduction block; however, the time required for recovery from the failure was prolonged.7. The number of impulses prior to block was related directly to the temperature of the preparation; this had a Q10 calculated to be about 1*3.8. It is suggested that during repetitive activity, the K + gradient across the membrane is reduced, resulting in depolarization and eventually in conduction failure.

Information processing in the axon

“…Although the possibility that propagation might fail at branch points was previously discussed by Krnjevic and Miledi 69 , the first clear indication that propagation is perturbed by axonal branch points came from the early studies on spiny lobster, crayfish and leech axons 33,[70][71][72][73]82,83 . The large size of invertebrate axons allowed multi-electrode recordings upstream and downstream of the branch point to be performed.…”

“…When the action potential fails to propagate along the axon, no signal can reach the output of the cell. Conduction failure filters communication with postsynaptic neurons, and has been observed experimentally in various axons including vertebrate spinal axons 68,69 , spiny lobster or crayfish motor neurons 33,64,70,71 , leech mechanosensory neurons [72][73][74][75][76] , thalamocortical axons 77 , rabbit nodose ganglion neurons 78 , rat dorsal root ganglion neurons 63,79 , neurohypophysial axons 17,80 and hippocampal pyramidal cells 39,66,81 . Several factors determine whether propagation along axons fails or succeeds.…”

“…In fact, hyperpolarization of the axon membrane or local application of physiological saline with a low concentration of potassium in the vicinity of a block can restore propagation in crayfish axons 71 . Elevation of the extracellular potassium concentration produced conduction block in spiny lobster axons 82 .…”

Effects of hypertonic solutions on quantal transmitter release at the crayfish neuromuscular junction

“…The ratio of the positive relative to the negative phase of the action potentials was not affected by hypertonicity, indicating that the magnitude of the sodium inward current was unchanged (cf. Smith, 1980). Furthermore, thresholds for nerve excitation were unchanged in saline or melezitose solution unless the osmolarity exceeded 1-00 Osm.…”

“…The inner side of the muscle, along which the axon projects, was exposed by removing the overlying closer muscle, and the vascular and connective tissue which interfered with clear visualization and electrode placement was carefully dissected away (Smith, 1980).…”