Flexible neural control of motor units.

Voluntary movement requires communication from cortex to the spinal cord, where a dedicated pool of motor units (MUs) activates each muscle. The canonical description of MU function rests upon two foundational tenets. First, cortex cannot control MUs independently but supplies each pool with a common drive. Second, MUs are recruited in a rigid fashion that largely accords with Henneman's size principle. Although this paradigm has considerable empirical support, a direct test requires simultaneous observations of many MUs across diverse force profiles. In this study, we developed an isometric task that allowed stable MU recordings, in a rhesus macaque, even during rapidly changing forces. Patterns of MU activity were surprisingly behavior-dependent and could be accurately described only by assuming multiple drives. Consistent with flexible descending control, microstimulation of neighboring cortical sites recruited different MUs. Furthermore, the cortical population response displayed sufficient degrees of freedom to potentially exert fine-grained control. Thus, MU activity is flexibly controlled to meet task demands, and cortex may contribute to this ability.

Motor Cortex Embeds Muscle-like Commands in an Untangled Population Response.

Primate motor cortex projects to spinal interneurons and motoneurons, suggesting that motor cortex activity may be dominated by muscle-like commands. Observations during reaching lend support to this view, but evidence remains ambiguous and much debated. To provide a different perspective, we employed a novel behavioral paradigm that facilitates comparison between time-evolving neural and muscle activity. We found that single motor cortex neurons displayed many muscle-like properties, but the structure of population activity was not muscle-like. Unlike muscle activity, neural activity was structured to avoid "tangling": moments where similar activity patterns led to dissimilar future patterns. Avoidance of tangling was present across tasks and species. Network models revealed a potential reason for this consistent feature: low tangling confers noise robustness. Finally, we were able to predict motor cortex activity from muscle activity by leveraging the hypothesis that muscle-like commands are embedded in additional structure that yields low tangling.

Criticality Maximizes Complexity in Neural Tissue.

The analysis of neural systems leverages tools from many different fields. Drawing on techniques from the study of critical phenomena in statistical mechanics, several studies have reported signatures of criticality in neural systems, including power-law distributions, shape collapses, and optimized quantities under tuning. Independently, neural complexity-an information theoretic measure-has been introduced in an effort to quantify the strength of correlations across multiple scales in a neural system. This measure represents an important tool in complex systems research because it allows for the quantification of the complexity of a neural system. In this analysis, we studied the relationships between neural complexity and criticality in neural culture data. We analyzed neural avalanches in 435 recordings from dissociated hippocampal cultures produced from rats, as well as neural avalanches from a cortical branching model. We utilized recently developed maximum likelihood estimation power-law fitting methods that account for doubly truncated power-laws, an automated shape collapse algorithm, and neural complexity and branching ratio calculation methods that account for sub-sampling, all of which are implemented in the freely available Neural Complexity and Criticality MATLAB toolbox. We found evidence that neural systems operate at or near a critical point and that neural complexity is optimized in these neural systems at or near the critical point. Surprisingly, we found evidence that complexity in neural systems is dependent upon avalanche profiles and neuron firing rate, but not precise spiking relationships between neurons. In order to facilitate future research, we made all of the culture data utilized in this analysis freely available online.