Functional Organization of the Spinal Locomotor Network Based on Analysis of Interneuronal Activity

Abstract

Locomotion is a vital motor function for any living being. In vertebrates, a basic locomotor pattern is controlled by the spinal locomotor network (SLN). Although SLN has been extensively studied, due to technical difficulties, most data were obtained during fictive locomotion, and data about the activity of spinal neurons during locomotion with intact sensory feedback from limbs are extremely limited. Here, we overcame the technical problems and recorded the activity of putative spinal interneurons from spinal segments L4–L6 during treadmill forward locomotion evoked by stimulation of the mesencephalic locomotor region in the decerebrate cat. We found that neurons were activated and inactivated preferably within one of the four phase ranges presumably related to preparation for the limb lift-off, the limb lift-off, transition from the limb flexion to limb extension during swing, and the limb touch-down. We analyzed the activity phases of recorded interneurons by using a new method that took into account the previously ignored information about the stability of neuronal modulation in the sequential locomotor cycles. We suggested that neurons with stable modulation (i.e., small dispersion of their activity phase in sequential cycles) represent the core of SLN. Our analysis revealed groups of neurons active approximately out of phase and presumably contributing to the control of vertical (VC) and horizontal (HC) components of the step. We found that most VC- and HC-related neurons were located in the intermediate and dorsal/ventral parts of the grey matter, respectively. Our experimental data can be used as a benchmark for computational models of locomotor neuronal networks.