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The transition from larval to adult locomotion in the anuran, Xenopus laevis, involves a dramatic switch from axial to appendicular swimming including intermediate stages when the tail and hindlimbs co-exist and contribute to propulsion. Hatchling tadpole swimming is generated by an axial central pattern generator (CPG) which matures rapidly during early larval life. During metamorphosis, the developing limbs are controlled by a de novo appendicular CPG driven initially by the axial system before segregating to allow both systems to operate together or independently. Neuromodulation plays important roles throughout, but key modulators switch their effects from early inhibitory influences to facilitating locomotion. Temperature affects the construction and operation of locomotor networks and global changes in environmental temperature place aquatic poikilotherms, like amphibians, at risk. The locomotor control strategy of anurans differs from other amphibian groups such as salamanders, where evolution has acted upon the thyroid hormone pathway to sculpt different developmental outcomes.
Figure 1. Multiple and opposing modulation of Xenopus locomotor CPG network output from hatching through metamorphosis. In larvae (a), exogenous NO and DA, acting on D2-like receptors, reduce (downward arrows) the occurrence of spontaneous fictive swim episodes (a1), whilst NA decreases swim cycle frequencies (a2). In premetamorphic larvae (b), both NO and DA switch modulatory effects to promote (upward arrows) episode occurrences (b1). Whereas low DA still activates inhibitory D2-like receptors, high DA levels activate low-affinity, newly incorporated excitatory D1-like receptors that facilitate swimming activity. 5-HT now decreases cycle frequencies (b2). During prometamorphosis (c), limb CPG network output is initially coordinated with the axial CPG rhythm. At metamorphic climax (d), co-existing axial and limb CPGs can operate independently at different rhythm frequencies. 5-HT can coordinate the two rhythms, by decelerating and accelerating the axial and limb CPGs, respectively. In contrast, NA, can uncouple already coupled rhythms. In the postmetamorphic frog (e), locomotion is solely limb-based. NO and DA exert similar effects on the limb CPG as the tadpole's axial CPG (E1), whilst 5-HT and NA maintain their opposing effects as during metamorphosis (E2). Figure adapted from the study by Sillar et al. [26].
Figure 2. Proposed phylogenetic conservation of motor neuron (MN) subtypes subserving ambulatory movements in vertebrates. In ancestral vertebrates, fin MNs, defined by expression of the transcription factor FoxP1, are distributed longitudinally in the Lateral Motor Column (LMC; top left) and divided into adductor (flexor homologue) and abductor (extensor homologue) motor pools (top right). In the little skate, LMC MNs innervating the adjacent pectoral and pelvic fin muscles also express specific Hox genes and FoxP1 to control swimming and pelvic fin walking. Similarly, in quadrupeds like frogs and mice, fore- and hindlimb locomotor control involves flexor and extensor muscles innervated by LMC MNs in cervical and lumbar cord regions, respectively. In inter-limb (thoracic) regions, FoxP1 expression is repressed by Hoxc9 so that thoracic segments are innervated only by axial MNs. In skates, a natural deletion of the HoxC cluster led to a lack of Hoxc9 along the spinal cord and thus to an inability for LMC Hoxc9-related specification. Together these findings suggest that the gene regulatory system required for appendicular motor control evolved from a common ancestral vertebrate possessing paired appendages. Figure adapted from the studies by Gillis et al. [49] and Jung et al. [50].
Figure 3. Developmental adaptation to cold temperature. In animals grown in cold temperatures (left), cold-sensitive TRPM8 channels are activated and trigger higher frequency Ca2+ spikes (blue insert), which increases Hb9-dependent MN differentiation and survival. Consequently, MN numbers are greater than in animals grown in warm temperature (right). This developmental temperature-dependent adaptation allows tadpoles to escape more quickly in cold water than if they had been reared in warm water, increasing their chances of escaping predators. Figure adapted from the study by Spencer et al. [53].
