Recruitment of cat motoneurons in the absence of homonymous afferent feedback

This study provides the first test in vivo of the hypothesis that group Ia muscle-stretch afferents aid in preventing reversals in the orderly recruit ment of motoneurons. This hypothesis was tested by studying recruitment of motoneurons deprived of homonymous afferent input. Recruitment order was me asured in decerebrate, paralyzed cats from dual intra-axonal records obtain ed simultaneously from pairs of medial gastrocnemius (MG) motoneurons. Pair s of MG motor axons were recruited in eight separate trials of the reflex d ischarge evoked by stimulation of the caudal cutaneous sural (CCS) nerve. S ome reports suggest that reflex recruitment by this cutaneous input should bias recruitment against order by the size principle in which the axon with the slower conduction velocity (CV) in a pair is recruited to fire before the faster CV axon. Recruitment was studied in three groups of cats: ones w ith the MG nerve intact and untreated (UNTREATED); ones with the MG nerve c ut (CUT); and ones with the MG nerve cut and bathed at its proximal end in lidocaine solution (CUT+). The failure of electrical stimulation to initiat e a dorsal root volley and the absence of action potentials in MG afferents demonstrated the effective elimination of afferent feedback in the CUT+ gr oup. Recruitment order by the size principle predominated and was not stati stically distinguishable among the three groups. The percentage of pairs re cruited in reverse order of the size principle was actually smaller in the CUT+ group (6%) than in CUT (15%) or UNTREATED (19%) groups. Thus homonymou s afferent feedback is not necessary to prevent recruitment reversal. Howev er, removing homonymous afferent input did result in the expression of inco nsistency in order, i.e., switches in recruitment sequence from one trial t o the next, for more axon pairs in the CUT+ group (33%) than for the other groups combined (13%). Increased inconsistency in the absence of increased reversal of recruitment order was approximated in computer simulations by i ncreasing time-varying fluctuations in synaptic drive to motoneurons and co uld not be reproduced simply by deleting synaptic current from group Ia hom onymous afferents, regardless of how that current was distributed to the mo toneurons. These findings reject the hypothesis that synaptic input from ho monymous group Ia afferents is necessary to prevent recruitment reversals, and they are consistent with the assertion that recruitment order is establ ished predominantly by properties intrinsic to motoneurons.