Sensory integration in presynaptic inhibitory pathways during fictive locomotion in the cat

The aim of this study is to understand how sensory inputs of different modalities are integrated into spinal cord pathways controlling presynaptic inhibition during locomotion. Primary afferent depolarization (PAD), an estimate of presynaptic inhibition, was recorded intra-axonally in group I afferents (n = 31) from seven hindlimb muscles in L(6)-S(1) segments during fictive locomotion in the decerebrate cat. PADs were evoked by stimulating alternatively low-threshold afferents from a flexor nerve, a cutaneous nerve and a combination of both. The fictive step cycle was divided in five bins and PADs were averaged in each bin and their amplitude compared. PADs evoked by muscle stimuli alone showed a significant phase-dependent modulation in 20/31 group I afferents. In 12/20 afferents, the cutaneous stimuli alone evoked a phase-dependent modulation of primary afferent hyperpolarization (PAH, n = 9) or of PADs (n = 3). Combining the two sensory modalities showed that cutaneous volleys could significantly modify the amplitude of PADs evoked by muscle stimuli in at least one part (bin) of the step cycle in 17/31 (55%) of group I afferents. The most common effect (13/17) was a decrease in the PAD amplitude by 35% on average, whereas it was increased by 17% on average in the others (4/17). Moreover, in 8/13 afferents, the PAD reduction was obtained in 4/5 bins i.e., for most of the duration of the step cycle. These effects were seen in group I afferents from all seven muscles. On the other hand, we found that different cutaneous nerves had quite different efficacy; the superficial peroneal (SP) being the most efficient (85% of trials) followed by Saphenous (60%) and caudal sural (44%) nerves. The results indicate that cutaneous interneurons may act, in part, by modulating the transmission in PAD pathways activated by group I muscle afferents. We conclude that cutaneous input, especially from the skin area on the dorsum of the paw (SP), could subtract presynaptic inhibition in some group I afferents during perturbations of stepping (e.g., hitting an obstacle) and could thus adjust the influence of proprioceptive feedback onto motoneuronal excitability.