How neurons generate behaviour in a hatchling amphibian tadpole: an outline

Abstract

Adult nervous systems are so complex that understanding how they produce behavior remains a real challenge. We chose to study hatchling Xenopus tadpoles where behavior is controlled by a few thousand neurons but there is a very limited number of types of neuron. Young tadpoles can flex, swim away, adjust their trajectory, speed-up and slow-down, stop when they contact support and struggle when grasped. They are sensitive to touch, pressure, noxious stimuli, light intensity and water currents. Using whole-cell recording has led to rapid progress in understanding central networks controlling behavior. Our methods are illustrated by an analysis of the flexion reflex to skin touch. We then define the seven types of neuron that allow the tadpole to swim when the skin is touched and use paired recordings to investigate neuron properties, synaptic connections and activity patterns. Proposals on how the swim network operates are evaluated by experiment and network modeling. We then examine GABAergic inhibitory pathways that control swimming but also produce tonic inhibition to reduce responsiveness when the tadpole is at rest. Finally, we analyze the strong alternating struggling movements the tadpole makes when grasped. We show that the mechanisms for rhythm generation here are very different to those during swimming. Although much remains to be explained, study of this simple vertebrate has uncovered basic principles about the function and organization of vertebrate nervous systems.

Development of a spinal locomotor rheostat

“…This approach therefore precludes an appreciation of the complexity of naturally evoked and sustained motor network activity, which can operate like a rheostat over an almost infinitely wide range of frequencies and intensities. Two simpler model systems, the zebrafish and the Xenopus frog tadpole, generate fictive locomotion in the absence of drugs, which allows investigations of neuronal networks during near-normal operation and affords an opportunity to study how these networks emerge during development (3,10,13,14). We focused on changes in MNs controlling the swimming behavior of postembryonic Xenopus frog tadpoles.…”

“…This system has already allowed a detailed description of the locomotor CPG (13). We have focused on how MNs change during the first day of postembryonic development, a period when the motor system is changing rapidly and acquiring the flexibility that will soon be required for efficient free-swimming larval life (3,14).…”

Delineating the Diversity of Spinal Interneurons in Locomotor Circuits

“…This work, which was primarily performed in the cat, identified potential component interneurons of the locomotor CPGs, but provided limited information on how they might interact with one another and was not amenable to studying their function during locomotion. Subsequent work in lamprey and Xenopus has provided important insights into the organization of the locomotor CPGs (Grillner, 2003;Roberts et al, 2010).…”

Initiation of Locomotion in Adult Zebrafish

“…Each of these behaviors can vary in pattern, speed, and force (e.g., activation and coordination of segmental muscles during escape and swimming in fish or coordination of limb movements during walking, trot, gallop, and scratch in legged animals). Thereby, some of the neurons can be dedicated to a specific motor microcircuit underlying a given behavior, while others are shared by different microcircuits to mediate different behaviors (El Manira and Clarac, 1994;Svoboda and Fetcho, 1996;Grillner, 2006;Grillner and Jessell, 2009;Berkowitz et al, 2010;Fetcho and McLean, 2010;Roberts et al, 2010).…”