Sensory gating precedes motor command in evolution of the corticospinal tract

Throughout mammals evolution, the contribution of the corticospinal tract (CST) to motor control progressively increases, culminating in primates with tight control of skilled movements such as independent finger dexterity. Although cortico-motoneuronal connections have been shown to be absent or very rare in rodents, it is generally assumed by analogy with primates that the main function of the CST is to convey motor commands. Yet the CST has been shown to have other functions, such as sensory gating. By differentially filtering out sensory signals at their entry point in the spinal cord, sensory gating is thought to have evolved to increase the gain of relevant feedback information during voluntary movement to improve execution of skilled movements. Here we show that, unexpectedly, sensory gating is the essential function of the lumbar CST in mice while lumbar motor command mainly involves non-CST pathways. By sequentially investigating each stage of the corticofugal pathways for motor command and sensory gating, we found that they both originate in the same cortical area but follow segregated paths. The hindlimb motor command is mainly relayed through subcortical supraspinal motor centers, and is only anecdotally encoded by the CST, requiring a propiospinal relay in the upper cord. In contrast, corticospinal neurons are essential for sensory gating, and act directly through a population of lumbar interneurons. Our results reveal that the original function of the CST in mammals, still prominent in rodents, is sensory gating, not motor control. This pathway appears to have been later selected through evolution to serve other functions, such as refined motor commands, eventually yielding direct CST-to-motoneuron connection in primates. The rodent lumbar CST thus serves as a prototypical paradigm to study, in isolation, the primary role of CST in sensory gating.