Edging toward entelechy in motor control

Abstract

The organization and functional logic of corticospinal motor neurons and their target connections remains unclear, despite their evident influence on movement. Spinal interneurons mediate much of this influence, yet we know little about the way in which corticospinal neurons engage spinal interneurons. This is perhaps not surprising given that the principles of organization of local spinal microcircuits remain elusive--we have glimpses of an underlying order but lack a comprehensive view of their functional architecture. In this brief essay we make a case that a new focus on the intersection of cortical and spinal circuits may provide clarity to the interpretation of corticospinal motor neuron firing patterns and help specify the logic of corticospinal motor neuronal function.

Figure 1.. Strategies for Spinal Motor Control

Distinct motor neuron pools innervate limb muscles with different biomechanical functions at specific joints. The logic of engagement of motor pools by spinal interneurons and descending inputs, including those from motor cortex, remain unclear. This diagram attempts to capture some of the many unresolved issues about interneuron and motor neuron engagement, with an eventual emphasis on the way in which descending inputs engage spinal interneurons. (A) Two possible modes of engagement of motor pools by zero-order premotor interneurons. Specifist engagement indicates the selection of motor pools in a manner that respects basic biomechanical function—flexor or extensor functions at a joint. Group Ia inhibitory interneurons, and possibly Renshaw interneurons, represent examples of this interneuron category. Generalist engagement links pools of differing function, as may underlie the simultaneous activation of muscle groups during particular behaviors. Cervical propriospinal interneurons involved in reaching movements represent one example of this class, and V0_C interneurons may represent a second example. (B) Two possible modes of organization of first-order, nonpremotor interneurons. Specifist neurons obey the rules of basic motor pool biomechanics, whereas generalist neurons supercede them. Some generalists may form recurrent connections with themselves or other interneuronal populations, eroding the clarity of this hierarchical organization. Hb9⁺ interneurons and GAD2⁺ GABApre neurons appear to be examples of first order arrangement, but their roles as specifists or generalists have not been resolved. (C) Engagement of spinal interneurons by sensory (S) or corticospinal (CS) projection neurons. The left-hand diagram shows one example of specifist engagement—the ability of group Ia proprioceptive afferents to capture a given motor pool and concurrently to activate reciprocal inhibitory interneurons that target an antagonist motor pool. The right-hand diagram indicates a generalist CSMN that innervates zero-order premotor interneurons. Such an arrangement could conceivably contribute to the task-dependent transition from motor pool alternation to co-contraction. Mixing and matching descending and local interneuron rules of engagement offers numerous possibilities for motor flexibility. For details see text.