A Central Pattern Generator Producing Alternative Outputs: Temporal Pattern of Premotor Activity

Abstract

The central pattern generator for heartbeat in medicinal leeches constitutes seven identified pairs of segmental heart interneurons. Four identified pairs of heart interneurons make a staggered pattern of inhibitory synaptic connections with segmental heart motor neurons. Using extracellular recording from multiple interneurons in the network in 56 isolated nerve cords, we show that this pattern generator produces a side-to-side asymmetric pattern of intersegmental coordination among ipsilateral premotor interneurons. This pattern corresponds to a similarly asymmetric fictive motor pattern in heart motor neurons and asymmetric constriction pattern of the two tubular hearts, synchronous and peristaltic. We provide a quantitative description of the firing pattern of all the premotor interneurons, including phase, duty cycle, and intraburst frequency of this premotor activity pattern. This analysis identifies two stereotypical coordination modes corresponding to synchronous and peristaltic, which show phase constancy over a broad range of periods as do the fictive motor pattern and the heart constriction pattern. Coordination mode is controlled through one segmental pair of heart interneurons (switch interneurons). Side-to-side switches in coordination mode are a regular feature of this pattern generator and occur with changes in activity state of these switch interneurons. Associated with synchronous coordination of premotor interneurons, the ipsilateral switch interneuron is in an active state, during which it produces rhythmic bursts, whereas associated with peristaltic coordination, the ipsilateral switch interneuron is largely silent. We argue that timing and pattern elaboration are separate functions produced by overlapping subnetworks in the heartbeat central pattern generator.