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

1. The incidence of short latency excitation of motoneurones innervating fl exor and bifunctional muscles evoked by group I intensity (less than or equ al to 2 x threshold) electrical stimulation of hindlimb muscle nerves was i nvestigated during fictive locomotion in decerebrate cats. Intracellular re cordings were made from hindlimb motoneurones in which action potentials we re blocked by intracellular diffusion of a lidocaine (lignocaine) derivativ e (QX-314) and fictive locomotion was evoked by electrical stimulation of t he 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 olig osynaptic EPSPs. In flexor motoneurones, locomotor-dependent excitation was present in both step cycle phases but largest during flexion. In bifunctio nal motoneurones, EPSPs were often largest at the transition between flexio n 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 lar ge EPSPs. EPSP amplitude became maximal as stimulation intensity was increa sed to about twice threshold. This suggests that tendon organ afferents can evoke group I EPSPs during locomotion. The EPSPs resulting from brief, sma ll stretches of extensor digitorum longus tendons indicate that group Ia mu scle spindle afferents can also evoke the group I excitation of flexors. St imulation of extensor group I afferents did not result in excitation of fle xor 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 consisti ng of a single interneurone interposed between group I afferents and motone urones innervating flexor and bifunctional muscles. This disynaptic excitat ion is analogous to that recorded in extensor motoneurones and evoked from extensor group I afferents during locomotion. Differences in the phase depe ndence and sources of group I excitation to flexor and extensor motoneurone s 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 i nnervating extensor, flexor and bifunctional muscles acting on hip, knee an d ankle joints suggests that these pathways can play an important role in t he reinforcement of ongoing locomotor activity throughout the limb.