Chemically mediated positive feedback generates long-lasting afterdischarge in a molluscan neuroendocrine system

Abstract

The peptidergic neuroendocrine caudodorsal cells (CDCs) of Lymnaea stagnalis control egg laying. The CDC network consists of 100 electroninically coupled neurons that form two clusters in the cerebral ganglia. Upon prolonged, repeated, intracellular stimulation of one CDC, excitation spreads over the network and leads to a 30-min period of spiking activity: the afterdischarge. During the afterdischarge a number of peptides, including the ovulation hormone, are released. When two ganglia rings from different animals were pinned down next to each other, an afterdischarge initiated in the CDCs of one CNS activated the CDCs of the other CNS, indicating that excitation spreads in the absence of physical contact between the CDCs. A single isolated intercerebral commissure (COM), the neurohaemal area of the CDCs, displayed the same discharge-inducing capability when brought in the vicinity of a second, intact, CNS. Other parts of the CNS did not possess this property. CDC afterdischarges could also induce repetitive spiking in adjacent isolated CDC somata showing that the effect can be directly on the CDCs themselves. The discharge-inducing factor was well separated from the ovulation hormone on a Bio-Gel P-6 column. The factor was pronase-degradable and inhibitors of proteolytic enzymes increased the factor's longevity. It is concluded that, contingent upon the CDC-discharge, a small (⩽ 1500 Da) excitatory peptide is released that acts directly on the CDCs. Its function is argued to be: (1) the spread of excitation from a subset of CDCs, receiving external input, over the entire CDC network; and (2) to provide a positive feedback to generate a maximum (all-or-none) response.