Group I disynaptic excitation of cat hindlimb flexor and bifunctional motoneurones during fictive locomotion

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Abstract
1 The incidence of short latency excitation of motoneurones innervating flexor and bifunctional muscles evoked by group I intensity (≤ 2 × threshold) electrical stimulation of hindlimb muscle nerves was investigated during fictive locomotion in decerebrate cats. Intracellular recordings were made from hindlimb motoneurones in which action potentials were blocked by intracellular diffusion of a lidocaine (lignocaine) derivative (QX-314) and fictive locomotion was evoked by electrical stimulation of the midbrain. 2 Few motoneurones (16%) received group I-evoked oligosynaptic excitation in the absence of fictive locomotion. During fictive locomotion 39/44 (89%) motoneurones innervating ankle, knee or hip flexor muscles and 18/28 (64%) motoneurones innervating bifunctional muscles received group I-evoked oligosynaptic EPSPs. In flexor motoneurones, locomotor-dependent excitation was present in both step cycle phases but largest during flexion. In bifunctional motoneurones, EPSPs were often largest at the transition between flexion and extension phases. 3 Activation of homonymous afferents most consistently evoked the largest locomotor-dependent excitation (amplitude up to 4.6 mV), but in some cases stimulation of heteronymous flexor or bifunctional muscle nerves evoked large EPSPs. EPSP amplitude became maximal as stimulation intensity was increased to about twice threshold. This suggests that tendon organ afferents can evoke group I EPSPs during locomotion. The EPSPs resulting from brief, small stretches of extensor digitorum longus tendons indicate that group Ia muscle spindle afferents can also evoke the group I excitation of flexors. Stimulation of extensor group I afferents did not result in excitation of flexor motoneurones. 4 The mean latency of locomotor-dependent group I excitation in flexor and bifunctional motoneurones was 1.64 ± 0.16 ms, indicating a path consisting of a single interneurone interposed between group I afferents and motoneurones innervating flexor and bifunctional muscles. This disynaptic excitation is analogous to that recorded in extensor motoneurones and evoked from extensor group I afferents during locomotion. Differences in the phase dependence and sources of group I excitation to flexor and extensor motoneurones during locomotion suggest the existence of separate groups of excitatory interneurones exciting flexor and extensor motoneurones. 5 The wide distribution of group I disynaptic excitation in motoneurones innervating extensor, flexor and bifunctional muscles acting on hip, knee and ankle joints suggests that these pathways can play an important role in the reinforcement of ongoing locomotor activity throughout the limb.