Intracellular Analysis of Reflex Pathways Underlying the Stumbling Corrective Reaction During Fictive Locomotion in the Cat

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Abstract
In cat and humans, contact between an obstacle and the dorsum of the foot evokes the stumbling corrective reaction (reflex) that lifts the foot to avoid falling. This reflex can also be evoked by short trains of stimuli to the cutaneous superficial peroneal (SP) nerve in decerebrate cats during the flexion phase of fictive locomotion. Here we examine intracellular events in hindlimb motoneurons accompanying stumbling correction. SP stimulation delivered during the flexion phase excites knee flexor motoneurons at short latency [minimum excitatory postsynaptic potential (EPSP) latency 1.8 ms; mean 2.7 ms]. Although a similar short latency excitation occurs in ankle extensors (mean latency, 2.8 ms), recruitment is delayed until successive shocks in the stimulus train overcome the locomotor-related hyperpolarization of ankle extensors. In ankle flexor motoneurons, SP stimulation evokes an inhibition (mean latency, 2.7 ms) that briefly reduces or stops their firing during the flexion phase. There is a phase-dependent modulation of SP-evoked EPSP amplitude as well as latency during locomotion. However, the more obvious change in SP reflex pathways with the onset of fictive locomotion is the reduced inhibition of ankle extensor motoneurons and the increased inhibition of ankle flexors. These results show that the characteristic pattern of hindlimb motoneuron activation during SP nerve–evoked stumbling correction results from 1 ) di- and trisynaptic excitation of knee flexor and ankle extensor motoneurons; 2 ) increased inhibitory postsynaptic potentials in ankle flexors and a suppression of inhibition in extensors, 3 ) sculpting of the short-latency SP postsynaptic effects by motoneuron membrane potential, and 4 ) longer latency excitatory effects that are likely evoked by lumbar interneurons involved in the generation of fictive locomotion.