Corticospinal Output to Hindlimb Muscles in the Primate

The overall goal of this study was to investigate the properties of corticospinal output to a wide range of hindlimb muscles in the primate and to map the representation of individual muscles in hindlimb motor cortex. Compared to the forelimb, little is known about cortical control of the hindlimb despite its obvious importance in motor control. We developed two chronic EMG implant methods, arm-mounted and cranial-mounted, that provide stable, long-term EMG recording from large numbers of muscles of the hindlimb in awake behaving monkeys. Using stimulus triggered averaging (15, 30 and 60 µA; 15 Hz) of EMG activity collected from 19 muscles of the hindlimb, we addressed three facets of the cortical control of the hindlimb in the primate. First, we determined the organization of the hindlimb representation of primary motor cortex (M1) in terms of motor output to individual muscles and muscles grouped at different joints. Second, we determined the output properties of hindlimb M1 in terms of sign, latency, magnitude and distribution of effects in comparison to data for the forelimb collected with similar methods. And third, we investigated the differential cortical control of fast and slow muscles of the ankle. The organization of the hindlimb representation in M1 cortex was similar to that of the forelimb in that there is a core distal representation, surrounded by a peripheral proximal representation separated by a region of proximal-distal cofacilitation. However, there were far fewer poststimulus effects in hindlimb muscles than forelimb muscles. As stimulus intensity increased, both the proximal and distal representations decreased in size. The proximal-distal cofacilitation region, however, increased dramatically in a manner that cannot easily be explained by stimulus-current spread alone. A model of cortical hindlimb organization is presented that includes partial segregation of proximal- and distal-specific corticospinal neurons but also unequal synaptic linkages to proximal and distal motoneurons in the spinal cord. There were similarities between hindlimb and forelimb output effects but a number of striking differences stand out. Most notable was the vast difference in magnitude of output effects to hindlimb muscles despite ample evidence of corticospinal monosynaptic input to hindlimb motoneurons. The magnitudes of poststimulus facilitation (PStF) effects were twice as strong in the intrinsic hand muscles compared to the intrinsic foot muscles at 15 µA. Magnitude differences were even greater for wrist versus ankle muscles. Interestingly, PStF was more common in the distal muscles of both forelimb and hindlimb but these effects were concentrated in the intrinsic foot muscles of the hindlimb while more evenly distributed among the distal joints of the forelimb. Finally, stimulus triggered averages of hindlimb EMG contained broad, long latency suppression and long latency facilitation components that are not present in forelimb averages. Conflicting results have been reported in primate and human studies concerning the role of the motor cortex in the control of slow muscles with some studies suggesting that effects on the slow muscle, soleus, are largely inhibitory. Stimulus triggered averaging of EMG activity provided a more sensitive and higher resolution approach to delineating cortical motor output effects than the methods applied in previous studies. We found that PStF was just as common in the slow muscle, soleus, as the fast muscles of the ankle and that there was no difference between the PStF onset latencies and magnitudes of the fast and slow muscles. Based on our results, it is clear that the motor cortex has a powerful excitatory effect on soleus motoneurons although it was also inhibited from more cortical sites than other ankle muscles. In conclusion, there are important similarities in the organization and properties of hindlimb and forelimb cortical output. Perhaps most notable among them is the basic pattern of cortical map representation of distal and proximal muscles. However, most striking among the differences is the markedly weaker output effects to distal muscles of the hindlimb compared to forelimb. The results suggest a synaptic organization with a much weaker monosynaptic component compared to forelimb muscles. Finally, there is strong evidence of cortical facilitation of the slow muscle, soleus