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According to the size principle the fine control of muscle tension depends on the orderly recruitment of motor neurons from a heterogeneous pool. We took advantage of the small number of excitatory motor neurons (about 12) that innervate the depressor muscle of the crayfish walking leg to determine if the size principle applies to this muscle. We found that in accordance with the size principle, when stimulated by proprioceptive input, neurons with small extracellular spikes were recruited before neurons with medium or large spikes. Because only a small fraction of the motor neurons responded strongly enough to sensory input to be recruited in this way, we extended our analysis to all neurons by characterizing properties that have classically been associated with recruitment order such as speed of axonal conduction and extracellular spike amplitude. Through a combination of physiological and anatomical criteria we were able to identify seven classes of excitatory depressor motor neurons. The majority of these classes responded to proprioceptive input with a resistance reflex, while a few responded with an assistance reflex, and yet others did not respond. Our results are in general agreement with the size principle. However, we found qualitative differences between neuronal classes in terms of synaptic input and neuronal structure that would in theory be unnecessary, according to a strict interpretation of the size principle. We speculate that the qualitative heterogeneity observed may be due to the fact that the depressor is a complex muscle, consisting of two muscle bundles that share a single insertion but have multiple origins.

Recruitment in a heterogeneous population of motor neurons that innervates the depressor muscle of the crayfish walking leg muscle