Impulse conduction in sympathetic nerve terminals in the guinea-pig vas deferens and the role of the pelvic ganglia.
Focal extracellular recording techniques were used to study nerve impulse propagation and the intermittent transmitter release mechanism in sympathetic nerve terminals of the guinea-pig vas deferens in vitro. In particular, the nature of impulse propagation in postganglionic nerve fibres was characterized following pre- or postganglionic stimulation. Conventional intracellular recording techniques were also used to study directly ganglionic transmission in cell bodies in the anterior pelvic ganglia. When brief electrical stimuli were applied to the hypogastric nerve trunk close to the prostatic end of the vas deferens, the nerve terminal impulses recorded extracellularly could be evoked either directly by stimulation of the parent axon (i.e. postganglionically) or indirectly by stimulation of the preganglionic nerve fibre. In 364 separate recordings, nerve terminal impulse conduction failure was not observed during trains of stimuli at 1 Hz. However, apparent "intermittent conduction" of nerve impulses was noted on 16 occasions. In these fibres, the degree of intermittent conduction decreased as the frequency of stimulation was increased. Conduction in these intermittent fibres was reversibly interrupted by removing calcium from the Krebs' solution or by the addition of the ganglion blocker, hexamethonium (30-100 microM). Thus, the cause of intermittent conduction is failure of the transmission of excitation in the sympathetic ganglia. Impulses evoked by postganglionic stimulation never failed to propagate into the nerve terminals, and changes in the shape or amplitude of the nerve terminal impulse during trains of stimuli were not detected. One effect of stimulation was a frequency-dependent increase in the latency of the nerve terminal impulse which developed during the train of stimuli. Thus, intermittence of transmitter release from individual varicosities cannot be attributed to failure of impulse propagation in sympathetic nerve terminals. Transmission in the anterior pelvic ganglia was investigated directly by making intracellular recordings from cell bodies whose terminals projected to the vas deferens. Many cell bodies received a strong synaptic input which generated an action potential in the postganglionic cell body on a one-to-one basis. However, in some cell bodies there was a low safety factor for the generation of the action potential by the excitatory postsynaptic potential. The safety factor for generating an action potential in the postganglionic cell body was raised by increasing the frequency of stimulation. These findings suggest that peripheral ganglia are not simple one-to-one relay stations, but may well play an important role in controlling the patterns of nerve impulse traffic in postganglionic sympathetic neurons.