Incremental and decremental processes in Limulus ganglia: Stimulus frequency and ganglion organization influences

Abstract

Critical habituation criteria have been met at both the behavioral and physiological levels in Limulus polyphemus. Additionally, analyses of abdominal ganglion unit responses to repetitive tactile stimulation of the gill book have demonstrated that there are two phases of the habituation process—there is an initial increment in unit responsivity followed by a decrement. Models proposed by others suggest that habituation is the result of two opposing processes, a decrementing process in the S-R pathway and an incrementing “state” process that sensitizes the output. Stimulation frequency and intensity are critical in activating central state. Dorsal nerve efferents in Limulus abdominal ganglia were activated by several different tactile stimulation frequencies. It was found that with the exception of the slowest (1/60 sec), habituation occurred at all frequencies. The incrementing state process was frequency-dependent, being maximal at the highest rates (2/sec and 1/sec). As a first step in analyzing the neural bases of these habituation processes, the effects of disrupting ganglion organization were also examined. Previous research had shown that contralateral, intraganglionic influences were critical in dorsal nerve cardioregulatory output. These contralateral influences are readily disrupted by a longitudinal division or splitting of the ganglion. The effect of this disruption on habituation of dorsal nerve units was studied in a two-ganglion system at a stimulation frequency that best elicited the incrementing and decrementing processes of habituation. In one group, the segment that first processed the tactile input was split; in another, the segment giving rise to the dorsal nerve that was recorded was split; in a third, both input and output ganglia were divided, and the fourth was an intact abdominal ganglion system. Results demonstrate that habituation was best and central state sensitization least when an output ganglion was split. The most sensitization and poorest initial habituation were seen with an input split. The intact group and the group with both ganglia split were similar and showed response changes that were between the other two groups. These effects persisted on 4- and 12-min retests. The effects of an output split were assumed to disrupt the number of influences (the state system) on the final common path while an input split appeared to interfere with sensory modulation functions.