Action‐potential initiation and maintained activity of the isolated frog muscle spindle

Abstract

The initiation of afferent action potentials represents the basic signalling process integrating and coding information of an external stimulus. There is also evidence in sensory receptor neurons of spontaneously generating action potentials that interfere with and modify the stimulus evoked activity. The present study investigates the generation of spontaneous action potentials in the isolated muscle spindle of the frog by recording receptor potentials, small subthreshold depolarizations, propagated impulses and interspike transients from the first Ranvier-node of the afferent stem fibre. The temporal pattern of spontaneous discharges at resting length depended on several variables interacting at the encoding site. In the absence of mechanical stimulation, a large resting receptor potential steadily depolarized the encoding node and provoked action potentials at irregular intervals. After each action potential, the hyperpolarizing afterpotential provided a slowly increasing depolarizing interspike transient of decreasing slope (time constant 128 ms), which evoked small subthreshold depolarizations (decay time > 5 ms; multimodal amplitude distribution) before the following action potential discharged. The probability of the small subthreshold depolarizations increased the longer the resting receptor potential stayed constant at its maximum amplitude. When increasing the static prestretch level encoding depended also on the stretch-evoked receptor potential as an additional parameter. The resulting depolarizing interspike transients were then larger and also more steeply rising, so that the afferent discharges increased in both rate and regularity. The experiments show dynamic threshold patterns that control action-potential initiation by the assessment of the actual amplitude of depolarization and its rate of rise.