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Neural control of swimming depth in marine zooplankton

Cilia-based locomotion is the major form of locomotion for the microscopic planktonic organisms which inhabit the ocean. This type of locomotion is widespread among the larval stages of marine invertebrates, including sponges, cnidarians, and many protostomes and deuterostomes. Freely swimming ciliated larvae often spend days to months drifting in the currents as part of the zooplankton. Given their negative buoyancy, these organisms must control ciliary activity to maintain an appropriate depth. We study the neuronal bases of depth regulation in the ciliated planktonic larvae of the marine annelid Platynereis.

The primary axis for ciliated plankton is vertical, and body orientation is maintained either by passive (buoyancy) or active (gravitaxis, phototaxis) mechanisms. When cilia beat, larvae swim upward, and when cilia cease beating, the negatively buoyant larvae sink. During swimming, the thrust exerted on the body is proportional to the beating frequency of cilia. The alternation of active upward swimming and passive sinking, together with swimming speed and sinking rate, is thought to determine vertical distribution in the water. Because several environmental parameters, including water temperature, light intensity, and phytoplankton abundance, change with depth, swimming depth will influence the speed of larval development, the magnitude of UV damage, and the success of larval feeding and settlement. To stay at an appropriate depth, planktonic swimmers must therefore sense environmental cues and regulate ciliary beating.


In Platynereis larvae we described several neuropeptides, small neuronal signaling molecules, expressed in distinct sensory neurons that innervate locomotor cilia. These neuropeptides alter the beat frequency of cilia and the rate of calcium-evoked ciliary arrests. Changes in ciliary beating influence 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. The simple circuitry found in these ciliated larvae may represent an ancestral state in nervous system evolution. Currently we are focusing on various sensory inputs from the marine environment that may trigger the release of these neuropeptides within the Platynereis larva.

Expression of 9 Platynereis neuropeptides in the larval nervous system visualized in a common acetylated tubulin (white) reference scaffold using computational image registration.

Platynereis trochophore larvae swimming in a vertical column.Note the occasional episodes of sinking, that correlate with the closure of all cilia.

References

Jékely, G., Origin and early evolution of neural circuits for the control of ciliary locomotion. Proc Biol Sci, 2011. 278(1707): p. 914-22.

Conzelmann, M., et al., Neuropeptides regulate swimming depth of Platynereis larvae. Proc Natl Acad Sci U S A, 2011. 108(46): p. E1174-83.