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Neural control of heartbeat in the leech and in some other invertebrates
Insights
Leech heartbeat involves coordinated muscle contractions in heart tubes, with spontaneous shifts between peristaltic and non-peristaltic modes. Neural control by heart motor (HE) and interneuron (HN) cells explains these complex rhythms.
Area of Science:
- Neuroscience
- Comparative Physiology
- Cardiovascular Biology
Background:
- The heartbeat in leeches (Hirudo) originates from the rhythmic contractions of circular muscles within bilateral heart tubes.
- Leech heartbeats exhibit complex coordination patterns, including peristalsis and non-peristalsis, with spontaneous transitions between these modes.
- Understanding the neural mechanisms underlying these rhythmic activities is crucial for comprehending invertebrate cardiovascular control.
Purpose of the Study:
- To elucidate the neural control mechanisms governing the bilaterally asymmetric heartbeat coordination modes in the leech Hirudo.
- To investigate the roles of heart motor neurons (HE cells) and heart interneurons (HN cells) in generating and coordinating heartbeat rhythms.
- To explain the spontaneous transitions between peristaltic and non-peristaltic heartbeat coordination modes.
Main Methods:
- Electrophysiological recordings to observe the activity patterns of HE and HN cells.
- Identification of synaptic connections between HE cells, HN cells, and their targets.
- Analysis of neural circuit function to account for observed heartbeat coordination and mode transitions.
Main Results:
- The activity of HE cells, controlled by HN cells, directly drives the segmental heart-tube muscle contractions.
- The rhythmic activity and synaptic interconnections of HN cells establish and maintain the distinct peristaltic and non-peristaltic coordination modes.
- The neural network architecture explains the observed spontaneous transitions between these two modes.
Conclusions:
- The coordinated activity of HE and HN cells provides a comprehensive explanation for the generation and regulation of leech heartbeat.
- This neural circuitry accounts for both the bilaterally asymmetric coordination and the dynamic transitions observed in leech cardiac function.
- Comparative insights into cardiac control mechanisms across different invertebrates, including lobsters and snails, highlight diverse evolutionary strategies.
Abstract:
The heartbeat of the leech Hirudo consists of the contractile rhythm of the circular muscles in the wall of a bilateral pair of celomic sinuses, the heart tubes, that run the length of the leech body. The constriction cycles of the segmental heart-tube sections are coordinated so that on one body side they constrict in a rear-to-front progression (peristalsis), while on the other side they constrict nearly in concert (nonperistalsis). Spontaneous right-left reciprocal transitions between peristaltic and nonperistaltic coordination modes occur every few dozen heartbeat cycles. The constriction of each segmental heart-tube section is controlled via excitatory synapses by a rhythmically active heart motor neuron, or HE cell, of which 17 bilateral pairs are iterated in segmental ganglia of the ventral nerve cord. The activity rhythm of the HE cell ensemble is in turn controlled via inhibitory synapses by a rhythmically active heart interneuron, the HN cell, of which seven bilateral pairs are iterated in the rostral segmental ganglia. The HN heart interneuron owes its activity rhythm to an endogenous polarization cycle, and the cycles of all members of the HN cell ensemble are locked into an appropriate phase relation thanks to their mutual interconnection via excitatory and inhibitory synaptic connections. The observed activity pattern and identified synaptic connections of HE cells and HN cells can account not only for the generation of the two bilaterally asymmetric heartbeat coordination modes but also for the right-left coordination mode transitions. In contrast to the heartbeat of Hirudo, the beat of the single-chambered heart of the lobsters Panulirus and Homarus is controlled by a set of nine rhythmically active neurons that make up the cardiac ganglion. Of these, five larger cells are heart motor neurons that innervate the heart muscle fibers via excitatory synapses. The remaining four smaller neurons of the cardiac ganglion are interneurons that provide excitatory input to each other and to the heart motor neurons. Although all the neurons of the cardiac ganglion appear capable of producing their own endogenous polarization rhythm, it is currently believed that one of the interneurons acts as a pacemaker for the whole ensemble of interneurons and motor neurons. The beat of the two-chambered heart of the marine snail Aplysia is generated by yet an entirely different mechanism. Here, the basic contractile rhythm of the heart is due to an endogenous polarization cycle of the heart muscle fibers. That myogenic rhythm is controlled and modulated by a set of cardiovascular motor neurons located in the abdominal ganglion, some of which make excitatory and others of which make inhibitory connections with the heart muscle fibers. The activity of these cardiovascular motor neurons is controlled by three types of heart interneurons via both inhibitory and excitatory connections. The interneurons are in turn interconnected in a manner that prevents the simultaneous activation of antagonistic cardiac motor acts...