© 2012 Nature America, Inc. All rights reserved.
NATURE NEUROSCIENCE VOLUME 15 | NUMBER 1 | JANUARY 2012 107
ARTICLES
How animal behaviors are regulated by the nervous system is a
difficult question to answer because the complexity of the nervous
system is so profound in most animals. It can be possible to dissect the
regulatory mechanism of how neurons regulate behaviors if a simple
model organism is studied. The nematode C. elegans is one such model
organism; its nervous system is composed of mere 302 neurons, whose
connectivity is almost completely known anatomically. In this study,
we decided to elucidate the mechanism of nictation, a stage-specific
behavior only shown in the dauer stage. Nictation was originally
reported in parasitic nematodes
1
. Specifically, parasitic nematodes
are thought to perform nictation to increase their infection efficiency
in host animals
2
. Parasitic nematodes nictate in their infective larval
stage, which is similar to the dauer stage in C. elegans
3
. Unlike the
infective larval stage of parasitic nematodes, however, which is a
part of normal development, the dauer larval stage in C. elegans is an
alternative developmental stage, specialized for long-term survival.
Thus, C. elegans develops into the dauer stage only when it encounters
harsh external conditions. Nictation was first described for
C. elegans dauers more than 30 years ago
4
, and conserved mechanisms
are likely to be responsible for this conserved behavior. So far, the
mechanism of nictation has not been discernible with molecular and
genetic approaches for two main reasons. First, genetics is not avail-
able for parasitic nematodes. Second, nictation is usually observed
in C. elegans on old plates with contaminating fungi, the hyphal tips
of which serve as the projections necessary for adherence and nicta-
tion of the dauers. On standard agar plates, C. elegans movement
is limited to two dimensions, preventing the observation of a three-
dimensional activity such as nictation. In this study, we developed
two efficient assays for nictation and dissected the mechanism of
nictation using genetics and other molecular tools available for
C. elegans. We show that IL2 ciliated head neurons are essential
for nictation. We also discuss evolutionary aspects of the nictation
behavior in the nematode.
RESULTS
Establishment of assays for nictation
We first identified materials that would substitute for fungal hyphae
as projections on which dauers could nictate in the lab condition so
that one could systematically analyze nictation. Among our tested
materials, cotton medical gauze, which morphologically mimics
fungal hyphae, was the best substrate on which to observe nictat-
ing dauers (Fig. 1a and Supplementary Movie 1). Medical gauze
could cover the surface area of a plate on which several hundred
dauers were grown, making it possible to analyze the behavior at the
population level.
Although medical gauze is a simple and convenient tool for the
basic observation of nictation, it is inadequate for individual track-
ing and quantitative behavioral analysis. To overcome this drawback,
we developed another assay that uses polydimethylsiloxane (PDMS)-
based microfluidic structures that provide the necessary architecture
for nictating dauers
5
. Considering their three-dimensional shape and
microscopic size, the structures can be thought of as mimicking the
natural dirt environment of soil nematodes
5
. Using PDMS as a mold,
we produced assay plates made of agar. The structures, which we
named micro-dirt chips because of their resemblance to the natural soil
environment, were composed of posts of a fixed size with regular gaps.
1
Research Center for Functional Cellulomics, Institute of Molecular Biology and Genetics, Seoul National University School of Biological Sciences, Seoul, Korea.
2
Department of Chemistry and Nano Sciences, Ewha Womans University, Seoul, Korea.
3
Department of Biochemistry, College of Life Sciences and Biotechnology,
Yonsei Proteome Research Center, Yonsei University, Seoul, Korea.
4
World Class University Department of Biophysics and Chemical Biology, Seoul National University,
Seoul, Korea.
5
These authors contributed equally to this work. Correspondence should be addressed to J.L. (elegans@snu.ac.kr).
Received 25 April; accepted 21 September; published online 13 November 2011; corrected after print 10 August 2012; doi:10.1038/nn.2975
Nictation, a dispersal behavior of the nematode
Caenorhabditis elegans, is regulated by IL2 neurons
Harksun Lee
1,5
, Myung-kyu Choi
1,5
, Daehan Lee
1
, Hye-sung Kim
1
, Hyejin Hwang
2
, Heekyeong Kim
3
, Sungsu Park
2
,
Young-ki Paik
3
& Junho Lee
1,4
Many nematodes show a stage-specific behavior called nictation in which a worm stands on its tail and waves its head in
three dimensions. Here we show that nictation is a dispersal behavior regulated by a specific set of neurons, the IL2 cells,
in C. elegans. We established assays for nictation and showed that cholinergic transmission was required for nictation.
Cell type–specific rescue experiments and genetic ablation experiments revealed that the IL2 ciliated head neurons were
essential for nictation. Intact cilia in IL2 neurons, but not in other ciliated head neurons, were essential, as the restoration of
the corresponding wild-type gene activity in IL2 neurons alone in cilia-defective mutants was sufficient to restore nictation.
Optogenetic activation of IL2 neurons induced nictation, suggesting that signals from IL2 neurons are sufficient for nictation.
Finally, we demonstrated that nictation is required for transmission of C. elegans to a new niche using flies as artificial carriers,
suggesting a role of nictation as a dispersal and survival strategy under harsh conditions.