Similarities between the muscle synergies associated with the flexion reflex and locomotion in reduced preparations have suggested that spinal circuits subserving these two motor tasks might share common interneurons. To test this hypothesis in functionally complex muscles, we studied the interaction between low-threshold cutaneous afferents and the locomotor central pattern generator (CPG) during treadmill locomotion in awake, intact cats. Electrical stimuli were delivered via implanted nerve cuff electrodes at all phases of locomotion, and EMGs were recorded from fourteen intramuscular subregions in eight bifunctional thigh muscles (adductor femoris, biceps femoris, caudofemoralis, gracilis, semimembranosus, semitendinosus, tensor fasciae latae, and tenuissimus). In addition, the EMG patterns recorded during locomotion were compared with those recorded during two other centrally driven rhythmical behaviors, scratching and paw shaking, to determine whether the functional relationships among these intramuscular subregions were fixed or task dependent. Four of the five broad, bifunctional muscles studied (biceps femoris, gracilis, semimembranosus, and tensor fasciae latae) had functional subunits that could be differentially activated in one or more of the three movements studied; adductor femoris was consistently uniformly activated despite its distributed skeletal attachments. The pattern of recruitment of the intramuscular functional subunits was movement-specific. The locomotor CPG and cutaneous reflex pathways both similarly subdivided some bifunctional muscles, but not others, into intramuscular subregions. The results of the present study confirm that some combinations of muscle subregions and cutaneous nerves constitute simple reciprocal categories of flexors and extensors, as described originally by Sherrington (1910). "Typical" low threshold excitatory or inhibitory reflex responses were produced in muscles or muscle subregions that were recruited as "net" flexors of extensors, respectively. However, muscles with complex activation patterns during walking often had very individualized, complex reflex responses during locomotion that did not conform to the background locomotion synergies. All of the reflex responses observed were mediated by low threshold cutaneous afferents. These data indicate that there are multiple, low threshold, excitatory and inhibitory cutaneous reflex pathways that have highly specialized connections with flexor and extensor muscles and even their intramuscular subregions. It is also clear that the premotoneuronal circuits mediating these cutaneous reflex effects are not necessarily synonymous with those of the locomotor CPG. These two systems do interact powerfully, however, suggesting some convergence. The nature of the convergence between the CPG and the many independent subsets of spinal interneurons mediating cutaneous reflexes is specialized and muscle subregion-specific.