Differential Effects of Serotonin Enhance Activity of an Electrically Coupled Neural Network

Abstract

Networks of electrically coupled neurons play an important role in coordinating activity among widely distributed neurons in the CNS. Such networks are sensitive to neuromodulation; but how modulation of individual cells affects activity of the entire network is not well understood. In the CNS of the medicinal leech, the S interneuron (S-cell) forms a network of electrically coupled neurons where each S-cell is linked to its two neighboring S-cells by electrical synapses. An action potential initiated in one cell is carried the length of the animal along this S-cell chain. The S-cell network is of interest because it is crucial for sensitization and dishabituation of the whole-body shortening reflex, although it is not necessary for reflexive shortening itself. Mechanosensory stimuli that produce shortening will directly elicit a train of action potentials by the S-cell network. This activity reflects the sum of action potential initiations in several S interneurons within the chain. The activity was enhanced by serotonin (5HT) in terms of both the total number of action potentials initiated and the average frequency of these initiations. Increases in evoked activity were accompanied by differential changes in the rates of action potential initiation in individual S-cells. 5HT only weakly enhanced initiations in S-cells that made a large contribution to the network-level response, while initiations in other, less active, S-cells were strongly enhanced by 5HT. This neurotransmitter also modulated the pattern of how activity was distributed throughout the network. 5HT-induced changes in activity patterns of the S-cell network may represent an important component of learning-related neuroplasticity in the leech shortening reflex.