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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.
Fig. 3. Differentiation of larval MN anatomy and peripheral innervation fields. (A) Examples of MN morphology at stage 42 with innervation fields restricted mainly to different sectors of the myotome (i, dorsal; ii, medial; iii, ventral). Note the laterally projecting process in medialneuron in A, ii. (B) Innervation fields of 31 MNs; 11 innervated exclusively the dorsal half and 9 exclusively the ventral half, and the remaining 11 spanned the midline of the myotome. The data are plotted as in Fig. 1D to show the innervation ranges of stage 42 MNs and compared with equivalent data from stage 37/38 (gray, Left). (C, i) Graph of soma sizes of stage 42 MNs versus spinal position labeled from all dorsoventral (1–0) locations. (C, ii) Backfill from ventralmuscle with rhodamine dextran reveals somata occupying medial-ventral location. Stage 42 MNs have a more extensive dendritic field compared with stage 37/38 (19). (C, iii) Simultaneous backfill from ventral (rhodamine, red) and dorsal (FITC, green) muscle regions. Note nonoverlapping groups occupying similar dorsoventral region of cord.
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