Physiology and Morphology of Shared and Specialized Spinal Interneurons for Locomotion and Scratching

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Abstract
Distinct types of rhythmic movements that use the same muscles are typically generated largely by shared multifunctional neurons in invertebrates, but less is known for vertebrates. Evidence suggests that locomotion and scratching are produced partly by shared spinal cord interneuronal circuity, although direct evidence with intracellular recording has been lacking. Here, spinal interneurons were recorded intracellularly during fictive swimming and fictive scratching in vivo and filled with Neurobiotin. Some interneurons that were rhythmically activated during both swimming and scratching had axon terminal arborizations in the ventral horn of the hindlimb enlargement, indicating their likely contribution to hindlimb motor outputs during both behaviors. We previously described a morphological group of spinal interneurons (“transverse interneurons” or T neurons) that were rhythmically activated during all forms of fictive scratching at higher peak firing rates and with larger membrane potential oscillations than scratch-activated spinal interneurons with different dendritic orientations. The current study demonstrates that T neurons are activated during both swimming and scratching and thus are components of the shared circuitry. Many spinal interneurons activated during fictive scratching are also activated during fictive swimming (scratch/swim neurons), but others are suppressed during swimming (scratch-specialized neurons). The current study demonstrates that some scratch-specialized neurons receive strong and long-lasting hyperpolarizing inhibition during fictive swimming and are also morphologically distinct from T neurons. Thus this study indicates that locomotion and scratching are produced by a combination of shared and dedicated interneurons whose physiological and morphological properties are beginning to be revealed.