Neuronal Substrates for State-Dependent Changes in Coordination between Motoneuron Pools during Fictive Locomotion in the Lamprey Spinal Cord

Abstract

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.

The Activity of Spinal Commissural Interneurons During Fictive Locomotion in the Lamprey

“…Three excitatory commissural interneurons were phasically modulated in different parts of the cycle, but the population is too small to comment on further. It should be noted that in the caudal part of the spinal cord, commissural excitatory interneurons are known to monosynaptically excite fin MNs, which are typically active in phase with myotomal MNs on the contralateral side (Mentel et al 2008). The role of the excitatory INs in the rostral part of the spinal cord, recorded in this study, remains unclear.…”

Bilateral connectivity in the brainstem respiratory networks of lampreys

“…For instance, in feeding systems, interneurons were found to synchronize bilaterally the networks underlying suckling in neonatal rats (Koizumi et al, 2009). Locomotor networks of the spinal cord also need bilateral coordination, with the particularity that this coordination is often in anti-phase (Fagerstedt et al, 2000;Grillner, 2003;Mentel et al, 2008;Brocard et al, 2010).…”

Migration of Motor Pool Activity in the Spinal Cord Reflects Body Mechanics in Human Locomotion

“…Spinal segmental localization charts are created by integrating anatomical and clinical data from several different sources (Kendall et al 1993). This approach can be used to characterize network architecture for different gaits by considering relative intensities, spatial extent, and temporal structure of the spinal motor output (Bonnet et al 2002;Cuellar et al 2009;Falgairolle et al 2006;Golubitsky et al 1999;Ivanenko et al 2008;Mentel et al 2008).…”