Neuropeptides regulate swimming depth of Platynereis larvae

Cilia-based locomotion is the major form of locomotion for microscopic planktonic organisms in the ocean. Given their negative buoyancy, these organisms must control ciliary activity to maintain an appropriate depth. The neuronal bases of depth regulation in ciliary swimmers are unknown. To gain ins...

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Bibliographic Details
Published in:Proceedings of the National Academy of Sciences - PNAS 2011-11, Vol.108 (46), p.E1174-E1183
Main Authors: Conzelmann, Markus, Offenburger, Sarah-Lena, Asadulina, Albina, Keller, Timea, Münch, Thomas A, Jékely, Gáspár
Format: Article
Language:English
Subjects:
Animals
Annelida
Behavior, Animal
Biological Sciences
Cells
cilia
Cilia - metabolism
Electrophysiology - methods
evolution
FMRFamide - pharmacology
Gene expression
Image Processing, Computer-Assisted - methods
Larva - metabolism
Larva - physiology
larvae
Locomotion
Molecular Sequence Data
Muscles - physiology
Neurons
Neurons - metabolism
neuropeptides
Neuropeptides - metabolism
Peptides
Platynereis
PNAS Plus
Polychaeta - embryology
Polychaeta - physiology
sensory neurons
Swimming
Worms
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Summary:Cilia-based locomotion is the major form of locomotion for microscopic planktonic organisms in the ocean. Given their negative buoyancy, these organisms must control ciliary activity to maintain an appropriate depth. The neuronal bases of depth regulation in ciliary swimmers are unknown. To gain insights into depth regulation we studied ciliary locomotor control in the planktonic larva of the marine annelid, PLATYNEREIS: We found several neuropeptides expressed in distinct sensory neurons that innervate locomotor cilia. Neuropeptides altered ciliary beat frequency and the rate of calcium-evoked ciliary arrests. These changes influenced larval orientation, vertical swimming, and sinking, resulting in upward or downward shifts in the steady-state vertical distribution of larvae. Our findings indicate that Platynereis larvae have depth-regulating peptidergic neurons that directly translate sensory inputs into locomotor output on effector cilia. We propose that the simple circuitry found in these ciliated larvae represents an ancestral state in nervous system evolution.
ISSN:0027-8424
1091-6490
DOI:10.1073/pnas.1109085108