Neuronal substrates for state-dependent changes in coordination between motoneuron pools during fictive locomotion in the lamprey spinal cord

Locomotion relies on a precisely timed activation of sets of motoneurons. A fundamental question is how this is achieved. In the lamprey, fin and myotomal motoneurons located on the same side of the spinal cord display alternating activity during straight swimming. The neural mechanism underlying this alternation is studied here during fictive locomotion induced by superfusion with NMDA, or locomotor bursting induced by electrical stimulation. If the spinal cord is split longitudinally, each hemicord still displays rhythmic locomotor related burst activity, but now fin and myotomal motoneurons become active in-phase. The out-of-phase activation of fin motoneurons persists only when at least three segments are left intact in the rostral part of the spinal cord. Proper coordination of fin motoneurons thus requires input from contralateral rostral segments. We show that commissural excitatory interneurons with long descending axons, previously reported to be active in phase with their ipsilateral myotomal motoneurons, provide monosynaptic excitation to contralateral fin motoneurons. Together, these results strongly indicate that, although myotomal motoneurons receive their phasic excitation from ipsilateral excitatory interneurons, fin motoneurons are mainly driven from the contralateral segmental network during bilateral locomotor activity. However, during unilateral bursting, fin and myotomal motoneurons instead receive a common input, which is apparently masked during normal fictive swimming. The spinal organization thus also provides circuitry for different patterns of coordination, i.e., alternation or coactivation of the two pools of motoneurons, which may subserve different forms of locomotor behavior.