Invertebrate central pattern generator circuits

Abstract

There are now a reasonable number of invertebrate central pattern generator (CPG) circuits described in sufficient detail that a mechanistic explanation of how they work is possible. These small circuits represent the best-understood neural circuits with which to investigate how cell-to-cell synaptic connections and individual channel conductances combine to generate rhythmic and patterned output. In this review, some of the main lessons that have appeared from this analysis are discussed and concrete examples of circuits ranging from single phase to multiple phase patterns are described. While it is clear that the cellular components of any CPG are basically the same, the topology of the circuits have evolved independently to meet the particular motor requirements of each individual organism and only a few general principles of circuit operation have emerged. The principal usefulness of small systems in relation to the brain is to demonstrate in detail how cellular infrastructure can be used to generate rhythmicity and form specialized patterns in a way that may suggest how similar processes might occur in more complex systems. But some of the problems and challenges associated with applying data from invertebrate preparations to the brain are also discussed. Finally, I discuss why it is useful to have well-defined circuits with which to examine various computational models that can be validated experimentally and possibly applied to brain circuits when the details of such circuits become available.

Figure 1.

Lobster cardiac ganglion. Four neurons with pacemaker properties drive five heart motor neurons. Tildes represent intrinsic burst properties. Resistors represent electrotonic coupling.

Figure 2.

Tritonia CPG. Symbols: dots, inhibitory synapses; triangles, excitatory synapses. DSI, dorsal swim interneuron; VS, ventral swim interneuron; C2 interneuron.

Figure 3.

Swimming CPG in Clione limacine uses a mix of mostly inhibitory synapses (dots) and intrinsic burst-generating mechanisms. Resistors are electrical coupling. Triangle, excitatory chemical synapse.

Figure 4.

Lymnaea feeding CPG. Diagram showing known connections between SO, a modulatory feeding interneuron and the various CPG interneurons. Symbols as in previous figures (see text for details).

Figure 5.

Leech heartbeat neuronal network. The numbers represent the segments in which the HN cell bodies are located, i.e. there is a left and right 1, 2, etc. Symbols as given previously.

Figure 6.

Aplysia feeding CPG circuit is capable of encoding three separate behaviour-specific modules. All symbols as previously described. Higher order neurons (not shown) can produce different cyclic behaviours depending upon which CPG interneurons receive excitatory input.

Figure 7.

(a) Pyloric and (b) gastric CPG circuits that comprise the lobster stomatogastric nervous system. Symbols as described previously except for diodes that represent rectifying electrotonic connections. The rectangles shown in some of the gastric synaptic connections represent delay lines between spikes in the presynaptic neurons and the postsynaptic excitatory response.