Afferent roles in hindlimb wipe-reflex trajectories: free-limb kinematics and motor patterns

The hindlimb wiping reflex of the frog is an example of a targeted trajectory that is organized at the spinal level. In this paper, we examine this reflex in 45 spinal frogs to test the importance of proprioceptive afferents in trajectory formation at the spinal level. We tested hindlimb to hindlimb wiping, in which the wiping or effector limb and the target limb move together. Loss of afferent feedback from the wiping limb was produced by cutting dorsal roots 7-9. This caused altered initial trajectory direction, increased ankle path curvature, knee-joint velocity reversals, and overshooting misses of the target limb. We established that these kinematic and motor-pattern changes were due mainly to the loss of ipsilateral muscular and joint afferents. Loss of cutaneous afferents alone did not alter the initial trajectory up to target limb contact. However, there were cutaneous effects in later motor-pattern phases after the wiping and target limb had made contact: The knee extension or whisk phase of wiping was often lost. Finally, there was a minor and nonspecific excitatory effect of phasic contralateral feedback in the motor-pattern changes after deafferentation. Specific muscle groups were altered as a result of proprioceptive loss. These muscles also showed configuration-based regulation during wiping. Biceps, semitendinosus, and sartorius (all contributing knee flexor torques) all were regulated in amplitude based on the initial position of the limb. These muscles contributed to an initial electromyographic (EMG) burst in the motor pattern. Rectus internus and semimembranosus (contributing hip extensor torques) were regulated in onset but not in the time of peak EMG or in termination of EMG based on initial position. These two muscles contributed to a second EMG burst in the motor pattern. After deafferentation the initial burst was reduced and more synchronous with the second burst, and the second burst often was broadened in duration. Ankle path curvature and its degree of change after loss of proprioception depended on the degree of joint staggering used by the frog (i.e., the relative phasing between knee and hip motion) and on the degree of motor-pattern change. We examined these variations in 31 frogs. Twenty percent (6/31) of frogs showed largely synchronous joint coordination and little effect of deafferentation on joint coordination, end-point path, or the underlying synchronous motor pattern. Eighty percent of frogs (25/31) showed some degree of staggered joint coordination and also strong effects of loss of afferents. Loss of afferents caused two major joint level changes in these frogs: collapse of joint phasing into synchronous joint motion and increased hip velocity. Fifty percent of frogs (16/31) showed joint-coordination changes of type (1) without type (2). This change was associated with reduction, loss, or collapse of phasing of the sartorius, semitendinosus and biceps (iliofibularis) in the initial EMG burst in the motor pattern. The remaining 30% (9/31) of frogs showed both joint-coordination changes 1 and 2. These changes were associated with both the knee flexor EMG changes seen in the other frogs and with additional increased activity of rectus internus and semimembranosus muscles. Our data show that multiple ipsilateral modalities all play some role in regulating muscle activity patterns in the wiping limb. Our data support a strong role of ipsilateral proprioception in the process of trajectory formation and specifically in the control of limb segment interactions during wiping by way of the regulation and coordination of muscle groups based on initial limb configuration.