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Peripheral and central control of flexor digitorum longus and flexor hallucis longus motoneurons: the synaptic basis of functional diversity. The two long toe flexor muscles in the cat, flexor digitorum longus (FDL) and flexor hallucis longus (FHL), have essentially identical mechanical actions, yet are used very differently during locomotion (O'Donovan et al. 1982). We attempted to identify the origin of the synaptic drive responsible for this functional differentiation. The organization of peripheral and central synaptic drive to FDL and FHL motoneurons was examined using two basic paradigms. (1) In animals anesthetized with chloralose or after ischemic destruction of the brain, peripheral reflex circuits were studied by recording intracellular responses from alpha-motoneurons produced by electrical stimulation of muscular and cutaneous nerves. (2) "Fictive locomotion", the centrally generated rhythmic synaptic drive produced in paralyzed, decerebrate animals by stimulation of the mesencephalic locomotor region or intravenous injection of L-DOPA and Nialamide, was monitored by recording electroneurograms from the central end of cut motor nerves. Despite their functional dissimilarity, FDL and FHL motoneurons received monosynaptic EPSPs from both FDL and FHL la afferents. Ipsilateral cutaneous afferents in the sural nerve and from the central plantar pad produced multiphasic PSPs which were not different in FDL and FHL cells. However afferents from the saphenous and superficial peroneal nerves did exert differential effects: the first component of the multiphasic PSP in most FDL cells was an EPSP, which was not present in most FHL cells. The central latency of this early EPSP in FDL motoneurons (0.8-1.5 ms) strongly suggests a disynaptic linkage. Cutaneous afferents from the ipsilateral forelimb produced IPSPs in most FHL cells but in only one of 18 FDL cells. Since some peripheral reflex circuits exerted differential effects on FDL and FHL cells, but others did not, the intracellular data did not demonstrate that the functional differences between FDL and FHL could be explained by differences in reflex organization. During fictive locomotion elicited by electrical or pharmacological stimulation, FHL motoneurons were coactive with ankle extensors during the extension phase of the fictive step cycle. In contrast, FDL motoneurons were most consistently activated in a brief burst at the onset of the flexion phase, showing much weaker and more variable coactivity with ankle extensors. These patients were essentially identical to those reported for FDL and FHL motor pools during treadmill locomotion by O'Donovan et al. (1982). We conclude that the central pattern generator (CPG) for locomotion produces distinct and highly differentiated sets of instructions for FDL and FHL motoneurons.(ABSTRACT TRUNCATED AT 400 WORDS)