State-dependent neural representations of muscle synergies in the spinal cord revealed by optogenetic stimulation

The central nervous system controls movement by combining neuromotor modules, known as muscle synergies. Previous studies suggest that spinal premotor interneurons (PreM-INs) contribute to the encoding of stable muscle synergies for voluntary movement. But descending and sensory inputs also influence motor outputs through the spinal interneuronal network, which may be configured by its inputs to encode different sets of muscle synergies depending on the network state, thereby recruiting different selections of synergies. Here we tested this possibility of state-dependent synergy encoding by examining the muscle synergies represented by the same upstream spinal interneurons under different activity states induced by various optogenetic stimulation patterns. Lumbosacral spinal units and electromyographic (EMG) activities of hindlimb muscles were simultaneously recorded from anaesthetized Thy1-ChR2 mice as the spinal cord was stimulated by one or two optic fibres at different intensities. The synergy encoded by each unit was revealed as a 'muscle field' derived from spike-triggered averages of EMG, whereas the entire muscle synergy set was factorized from the EMG. We found that although the muscle synergy set remained stable across stimulation conditions, the muscle fields of the same units were matched to different synergies within the set in different states. Thus the interneurons may flexibly adjust their connectivity with the motoneurons of the muscles as descending and sensory afferents impose different states on the spinal network. State-dependent encoding of muscle synergies may allow different synergies to be selected for producing stable movement in an ever-changing workspace environment. KEY POINTS: Muscle synergies for locomotion can be represented by spinal interneurons, as revealed by the interneurons' muscle fields derived from spike-triggered averages of EMG. The muscle field of a single spinal interneuron may vary under different stimulation conditions, as demonstrated by optogenetic stimulation. Encoding of muscle synergies is dependent on the state of spinal activities, thus facilitating the selection of appropriate synergies in different dynamic environments.