The command hypothesis: a new view using an old example

Abstract The interneurons that underlie abdominal flexion and extension behaviors in crustaceans were among the first to be called command neurons. They fit the original operational definition as cells that produce a well-defined movement or behavior when stimulated. Many examples of these cells are now known to influence behaviors throughout the animal kingdom. The early observation that stimulation of a single command neuron in a crustacean was sufficient to generate an apparently complete behavior led to the erroneous belief that one neuron might be responsible for one behavior. We now know that the strong stimulation of one command element is sufficient to recruit synaptically a group of similar neurons. In addition to the synaptic recruitment of agonists there is also a synaptic inhibition of their antagonists, resulting in what appears to be a complete behavior with reciprocity. Importantly, there is also evidence for the operation of similar functional groups in behaving animals. During animal-initiated behavior, each neuron in the functional group apparently makes only a minor contribution to the total motor output with the result that no single neuron in the group is necessary to generate the behavior. If the necessity criterion is a requirement to define a command neuron, then abdominal positioning interneurons can no longer be considered command neurons. Instead, they are cells with lesser roles, perhaps command elements in larger command systems. In spite of their diminished status, command elements occupy key positions in this and other motor systems.