A spinal origin for the obligate flexor synergy in the non-human primate: Implications for control of reaching

Stroke survivors frequently develop the flexor synergy, an obligate co-contraction of shoulder abductors and elbow flexors. The neural substrate has to date proven elusive. Here we trained two healthy female monkeys to generate isometric elbow and shoulder torques to move an on-screen cursor, and recorded neuron firing from motor cortical areas and the reticular formation. All regions contained some cells coding for independent contractions about elbow or shoulder. For neurons coding co-contractions, there was a surprising bias: more cells were related to combinations orthogonal to the flexor synergy, e.g. shoulder abduction with elbow extension. We then used threshold microstimulation to examine patterns of muscle activation elicited from the primary motor cortex, reticular formation and spinal cord in five female monkeys. Only in the spinal cord did microstimulation generate coactivation aligned to the flexor synergy. Our results suggest that primitive spinal circuits are limited to synergistic coactivation, a pattern which perhaps evolved for locomotion. Prehensile reaching movements aligned to these synergies require only limited descending control from the cortex and brainstem. By contrast, reaching orthogonal to the flexor synergy relies heavily on descending drive both to suppress spinal circuits and to sculpt motoneuron activity. The findings suggest that apparently similar reaches in different directions have different neural substrates. After a stroke, loss of descending drive leaves movements limited by spinal motor primitives.Significance Statement The flexor synergy is often a major contributor to disability when individuals recover from a stroke. It has been suggested that synergies arise because a surviving neural center has a pre-existing bias to generate co-contraction, and is released from inhibitory control after cortical damage. Here, we show that all brain centers tested were biased to code for co-contractions orthogonal to synergies, making it unlikely that they form the neural substrate. By contrast, spinal microstimulation often generated the same co-activation of muscles as in synergies. Our results suggest that synergies arise from spinal interneurons; this may allow future therapeutic strategies which target spinal circuits.