Effective quadrupedal locomotor behaviors require the coordination of many muscles in the limbs, back, neck, and tail. Because of the spinal motoneuronal somatotopic organization, motor coordination implies interactions among distant spinal networks. Here, we investigated some of the interactions between the lumbar locomotor networks that control limb movements and the thoracic networks that control the axial muscles involved in trunk movement. For this purpose, we used an in vitro isolated newborn rat spinal cord (from T2 to sacrococcygeal) preparation. Using extracellular ventral root recordings, we showed that, while the thoracic cord possesses an intrinsic rhythmogenic capacity, the lumbar circuits, if they are rhythmically active, will entrain the rhythmicity of the thoracic circuitry. However, if the lumbar circuits are rhythmically active, these latter circuits will entrain the rhythmicity of the thoracic circuitry. Blocking the synaptic transmission in some thoracic areas revealed that the lumbar locomotor network could trigger locomotor bursting in distant thoracic segments through short and long propriospinal pathways. Patch-clamp recordings revealed that 72% of the thoracic motoneurons (locomotor-driven motoneurons) expressed membrane potential oscillations and spiking activity coordinated with the locomotor activity expressed by the lumbar cord. A biphasic excitatory (glutamatergic)/inhibitory (glycinergic) synaptic drive was recorded in thoracic locomotor-driven motoneurons. Finally, we found evidence that part of this locomotor drive involved a monosynaptic component coming directly from the lumbar locomotor network. We conclude that the lumbar locomotor network plays a central role in the generation of locomotor outputs in the thoracic cord by acting at both the premotoneuronal and motoneuronal levels.

Studies devoted to understanding locomotor control have mainly addressed the functioning of the neural circuits controlling leg movements and relatively little is known of the operation of networks that activate trunk muscles in coordination with limb movements. The aim of the present work was (1) to identify the exogenous neurotransmitter cocktail that most strongly activates postural thoracic circuitry; (2) to investigate how the biogenic amines serotonin (5-HT), dopamine (DA), and noradrenaline (NA) modulate the coordination between limb and axial motor networks. Experiments were carried out on in vitro isolated spinal cord preparations from newborn rats. We recorded from ventral roots to monitor hindlimb locomotor and axial postural network activity. Each combination of the three amines with excitatory amino acids (EAAs) elicited coordinated rhythmic motor activity at all segmental levels with specific characteristics. The variability in cycle period was similar with 5-HT and DA while it was significantly higher with NA. DA elicited motor bursts of smaller amplitude in thoracic segments compared to 5-HT and NA, while both DA and NA elicited motor bursts of higher amplitude than 5-HT in the lumbar and sacral segments. The amines modulated the phase relationships of bursts in various segments with respect to the reference lumbar segment. At the thoracic level there was a phase lag between all recorded segments in the presence of 5-HT, while DA and NA elicited synchronous bursting. At the sacral level, 5-HT and DA induced an intersegmental phase shift while relationships became phase-locked with NA. Various combinations of EAAs with two or even all three amines elicited rhythmic motor output that was more variable than with one amine alone. Our results provide new data on the coordinating processes between spinal cord networks, demonstrating that each amine has a characteristic “signature” regarding its specific effect on intersegmental phase relationships.