Functional connectivity networks of common synaptic inputs to motor neurons reveal neural spinal synergies during a multi-joint task

Abstract

Movements are reportedly controlled through the combination of synergies that generate specific motor outputs by imposing an activation pattern on a group of muscles. To date, the smallest unit of analysis has been the muscle. In this human study, we decoded the spiking activities of spinal motor neurons innervating six lower limb muscles during an isometric multi-joint task. We identified their common low-frequency components, from which networks of common synaptic inputs to the motor neurons were derived. The vast majority of the identified motor neurons shared common inputs with other motor neuron(s). In addition, groups of motor neurons were partly decoupled from their innervated muscle, such that motor neurons innervating the same muscle did not necessarily receive common inputs. Conversely, some motor neurons from different muscles - including distant muscles - received common inputs. Our results provide evidence of a synergistic control of a multi-joint motor task at the spinal motor-neuron level. TeaserThe generation of movement involves the activation of many spinal motor neurons from multiple muscles. A central and unresolved question is how these motor neurons are controlled to allow flexibility for adaptation to various mechanical constraints. Since the computational load of controlling each motor neuron independently would be extremely large, the central nervous system presumably adopts dimensionality reduction. We identified networks of functional connectivity between spinal motor neurons based on the common synaptic inputs they receive during a multi-joint task. Our findings revealed functional groupings of motor neurons in a low dimensional space. These groups did not necessarily overlap with the muscle anatomy. We provide a new neural framework for a deeper understanding of movement control in health and disease.