Development of locomotor mechanisms in the frog.

Abstract

Tadpoles swim by undulations of the body and tail, whereas frogs locomote by alternate (stepping) and synchronous (frog-kick) movements of the hindlimbs. The development of interlimb coordination was studied by recording the activity of hindlimb motoneurons from the left and right ninth ventral roots of the isolated central nervous system (CNS). Results showed that mechanisms responsible for interlimb coordination of stepping are functional when the hindlimb is still composed of undifferentiated mesenchyme and before the lateral motor column has stabilized (stage III). The early appearance of coordinated activation of hindlimb motoneurons suggests that innervation of appropriate target muscles is not a prerequisite for normal development of circuits that mediate interlimb coordination of stepping. Synchronous activation of left and right hindlimb motoneurons (fictive frog kicks) appeared later in development (stage XIV). Throughout larval development 1:1 frequency coupling between both alternating and synchronous bursts of hindlimb motoneurons and bursts of primary motoneurons (those innervating axial muscles) was found. Recordings of peripheral nerve activity showed that motoneurons innervating antagonistic muscles of the thigh burst in antiphase. This intralimb coordination was present at stage X, a foot paddle stage that was the earliest stage in which the peripheral nerves were successfully dissected. That the neural activity of the isolated nervous system described above indeed underlies coordinated locomotor movements of the hindlimbs was shown by single-frame videotape analysis of hindlimb movements produced by the otherwise isolated CNS. The stepping movements displayed by those preparations were consistent with patterns of electrophysiological burst activity recorded from the ventral roots and peripheral nerves. The ontogenetic sequence in which the different patterns of electrophysiological activity emerged is the same as that of the corresponding behaviors in the intact tadpole. Although there were developmental changes in the reliability with which coordinated activity in the ventral roots and peripheral nerves was observed, each mode of coordination remained qualitatively unchanged from its earliest appearance through metamorphosis. These results show that mechanisms underlying locomotor coordination of the hindlimbs develop very early in larval ontogeny of the frog and can function when isolated from the periphery.