Development of a spinal locomotor rheostat

Locomotion in immature animals is often inflexible, but gradually
acquires versatility to enable animals to maneuver efficiently
through their environment. Locomotor activity in adults is produced
by complex spinal cord networks that develop from simpler
precursors. How does complexity and plasticity emerge during
development to bestow flexibility upon motor behavior? And how
does this complexity map onto the peripheral innervation fields of
motorneurons during development? We show in postembryonic
Xenopus laevis frog tadpoles that swim motorneurons initially
form a homogenous pool discharging single action potential per
swim cycle and innervating most of the dorsoventral extent of the
swimming muscles. However, during early larval life, in the prelude
to a free-swimming existence, the innervation fields of motorneurons
become restricted to a more limited sector of each muscle
block, with individual motorneurons reaching predominantly ventral,
medial, or dorsal regions. Larval motorneurons then can also
discharge multiple action potentials in each cycle of swimming and
differentiate in terms of their firing reliability during swimming
into relatively high-, medium-, or low-probability members. Many
motorneurons fall silent during swimming but can be recruited with
increasing locomotor frequency and intensity. Each region of the
myotome is served by motorneurons spanning the full range of
firing probabilities. This unfolding developmental plan,which occurs
in the absence of movement, probably equips the organism with
the neuronal substrate to bend, pitch, roll, and accelerate during
swimming in ways that will be important for survival during the
period of free-swimming larval life that ensues.