A Neural Basis for Motor Primitives in the Spinal Cord

Abstract

Motor primitives and modularity may be important in biological movement control. However, their neural basis is not understood. To investigate this, we recorded 302 neurons, making multielectrode recordings in the spinal cord gray of spinalized frogs, at 400, 800, and 1200 m depth, at the L2/L3 segment border. Simultaneous muscle activity recordings were used with independent components analysis to infer premotor drive patterns. Neurons were divided into groups based on motor pattern modulation and sensory responses, depth recorded, and behavior. The 187 motor pattern modulated neurons recorded comprised 14 cutaneous neurons and 28 proprioceptive neurons at 400 m in the dorsal horn, 131 intermediate zone interneurons from ϳ800 m depth without sensory responses, and 14 motoneuron-like neurons at ϳ1200 m. We examined all such neurons during spinal behaviors. Mutual information measures showed that cutaneous neurons and intermediate zone neurons were related better to premotor drives than to individual muscle activity. In contrast, proprioceptive-related neurons and ventral horn neurons divided evenly. For 46 of the intermediate zone interneurons, we found significant postspike facilitation effects on muscle responses using spike-triggered averages representing short-latency postspike facilitations to multiple motor pools. Furthermore, these postspike facilitations matched significantly in both their patterns and strengths with the weighting parameters of individual primitives extracted statistically, although both were initially obtained without reference to one another. Our data show that sets of dedicated interneurons may organize individual spinal primitives. These may be a key to understanding motor development, motor learning, recovery after CNS injury, and evolution of motor behaviors.

On the Origins of Modularity in Motor Control

“…In a recent study published in The Journal of Neuroscience, Hart and Giszter (2010) addressed this question in an innovative way, by developing a new methodology linking the neural input to the motor output. They supported the hypothesis that modularity is directly embodied in the neural circuitry of the spinal cord.…”

“…The neurons in the IZ depths (700 -800 m) thus qualified as putative interneurons and consequently, were selected for further analysis. The authors also looked at the neural activity in the shallowest depth (400 -500 m) and demonstrated that firing of neurons at that level were also uniformly better related to independent components than EMGs [Hart and Giszter (2010), their Fig. 3D], but only for firing in response to light touch stimulation: such a preference for independent components was not observed in responses to the other two types of stimuli [Hart and Giszter (2010), their Fig.…”

“…In a final phase of analysis, Hart and Giszter (2010) performed spike-triggered averaging to reveal direct relationships between neural spiking and muscle recruitment. Neurons in the IZ showed significant postspike facilitations to groups of muscles [Hart and Giszter (2010), their Fig.…”

“…To cope with the large number of degrees of freedom, humans and animals likely rely on a modular control architecture. In other words, the CNS may activate flexible combinations of motor primitives instead of controlling each muscle independently, a motor primitive being a premotor drive generated by some neuronal population (for example, in the spinal cord) that recruits a covarying group of muscles that remain in a fixed relationship during recruitment (Hart and Giszter, 2010). Hence, motor primitives may represent the building blocks of movement organization.…”

“…Hart and Giszter used the mutual information coefficient (MI), measuring the amount of information that the firing rate shared with the independent components or EMG values. This method suggested that neuronal firing was more closely related to independent components than to contraction of individual muscles [Hart and Giszter (2010), their Fig. 4].…”