Networks of common inputs to motor neurons of the lower limb reveal neural synergies that only partly overlap with muscle innervation

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 through the measurement of its activation. However, the muscle is not the lowest neural level of movement control. In this human study, we identified the common synaptic inputs received by motor neurons during an isometric multi-joint task. We decoded the spiking activities of dozens of spinal motor neurons innervating six lower limb muscles in 10 participants. Furthermore, we analyzed these activities by identifying 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. Moreover, we showed that common input to motor neurons is an essential feature of the neural control of movement. We conclude that the central nervous system controls flexible groups of motor neurons by distributing common inputs to substantially reduce the dimensionality of movement control.

Inter-muscular networks of synchronous muscle fiber activation

“…Our findings of complex hierarchically-structured network interactions of muscle fibers across topologically distant leg and back muscles align with recent works investigating motor neuron recruitment during exercise and inter-muscular coherence (Hug et al, 2021), which demonstrated that motor neurons from distant muscles (e.g., hamstrings and gastrocnemii) may receive common neuronal input during dynamic pedaling. Other works have reported the presence of common neural inputs also to other pairs of distinct muscles such as hamstrings and plantar flexors (Hug et al, 2011), as well as glutei and quadriceps during gait (Dominici et al, 2011).…”

Heksor: the central nervous system substrate of an adaptive behaviour

“…Furthermore, evidence that beta (13-30 Hz) activity in EEG over sensorimotor cortex underlies and reflects muscle synergies (Aumann & Prut, 2015) suggests that it might be possible to detect the initial and ongoing interactions among the new and old heksors. These studies might also incorporate parallel analyses of the spinal motoneuron synergies recently hypothesized by Hug et al (2021). Once again, a video game format in which the participants control EMG activity in specific muscles (or EMG produced by specific groups of motoneurons) could be useful.…”

“…These studies might also incorporate parallel analyses of the spinal motoneuron synergies recently hypothesized by Hug et al. (2021). Once again, a video game format in which the participants control EMG activity in specific muscles (or EMG produced by specific groups of motoneurons) could be useful.…”

Handedness is associated with less common input to spinal motor neurons innervating different hand muscles

“…To account for the fact that the strength of common synaptic inputs between two motor neurons is not proportional to the degree of correlation between their outputs (de la Rocha et al ., 2007), we only interpreted the correlation coefficients based on their significance (Hug et al ., 2021b). Specifically, we defined a significance threshold as the 95 th percentile of the cross-correlation coefficient distribution generated with resampled versions of the motor unit spike trains.…”