Embryonic assembly of a central pattern generator without sensory input

Abstract

Locomotion depends on the integration of sensory information with the activity of central circuitry, which generates patterned discharges in motor nerves to appropriate muscles1,2. Isolated central networks generate fictive locomotor rhythms (recorded in the absence of movement), indicating that the fundamental pattern of motor output depends on the intrinsic connectivity and electrical properties of these central circuits3,4. Sensory inputs are required to modify the pattern of motor activity in response to the actual circumstances of real movement. A central issue for our understanding of how locomotor circuits are specified and assembled is the extent to which sensory inputs are required as such systems develop5. Here we describe the effects of eliminating sensory function and structure on the development of the peristaltic motor pattern of Drosophila embryos and larvae. We infer that the circuitry for peristaltic crawling develops in the complete absence of sensory input; however, the integration of this circuitry into actual patterns of locomotion requires additional information from the sensory system. In the absence of sensory inputs, the polarity of movement is deranged, and backward peristaltic waves predominate at the expense of forward peristalsis.

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Figure 1: Genetic elimination of sensory function or structure in the Drosophila embryonic peripheral nervous system.
Figure 2: Peristalsis in embryos expressing active and inactive TeTxLC in the peripheral nervous system.
Figure 3: Elimination of sensory input disrupts episodes of forward but not backward peristaltic waves.
Figure 4: Expression of tetanus toxin (TeTxLC) in the embryonic peripheral nervous system results in severely disrupted larval locomotion.
Figure 5: Bursts of forward peristalsis but not sporadic forward waves are eliminated by removal of sensory input.

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Acknowledgements

We thank our colleagues in Cambridge and Toronto for comments on this work, and M. Sokolowski for providing support during its completion. M.L.S was funded by a Luis Velez Scholarship from the Venezuelan National Academy of Sciences at Clare College, Cambridge. M.B. is a Royal Society Research Professor. This work was supported by a grant from the Wellcome Trust.

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Correspondence to Maximiliano L. Suster.

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Suster, M., Bate, M. Embryonic assembly of a central pattern generator without sensory input. Nature 416, 174–178 (2002). https://doi.org/10.1038/416174a

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