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First published online November 2, 2007
Journal of Experimental Biology 210, 4043-4052 (2007)
Published by The Company of Biologists 2007
doi: 10.1242/jeb.006551
Temperature and food mediate long-term thermotactic behavioral plasticity by association-independent mechanisms in C. elegans
1 Department of Physics, Harvard University, Cambridge, MA 02138,
USA
2 Department of Biology and National Center for Behavioral Genomics,
Brandeis University, Waltham, MA 02454, USA
3 Center for Brain Science, Harvard University, Cambridge, MA 02138,
USA
Author for correspondence (e-mail:
samuel{at}physics.harvard.edu)
Accepted 5 September 2007
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Summary |
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 TOP Summary IntroductionMaterials and methodsResultsDiscussionReferences |
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4 h of sustained exposure to a new
temperature. Long-term plasticity in C. elegans thermotactic behavior
has been proposed to represent an associative learning of specific
temperatures conditioned in the presence or absence of bacterial food. Here,
we use quantitative behavioral assays to define the temperature and
food-dependent determinants of long-term plasticity in the different modes of
thermotactic behavior. Under our experimental conditions, we find that
starvation at a specific temperature neither disrupts TS
resetting toward the starvation temperature nor induces learned avoidance of
the starvation temperature. We find that prolonged starvation suppresses the
cryophilic mode of thermotactic behavior. The hen-1 and
tax-6 genes have been reported to affect associative learning between
temperature and food-dependent cues. Under our experimental conditions,
mutation in the hen-1 gene, which encodes a secreted protein with an
LDL receptor motif, does not significantly affect thermotactic behavior or
long-term plasticity. Mutation in the tax-6 calcineurin gene
abolishes thermotactic behavior altogether. In summary, we do not find
evidence that long-term plasticity requires association between temperature
and the presence or absence of bacterial food.
Key words: C. elegans, behavior, thermotaxis, navigation, long-term plasticity
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Introduction |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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). Starvation causes a variety of changes in C.
elegans' behavior that may improve its likelihood of finding food. For
example, when C. elegans is removed from food, its initial behavioral
strategy is area-restricted search of its immediate vicinity. After several
minutes of prolonged starvation, C. elegans changes its strategy to
long-range dispersal, which is characterized by extended periods of
uninterrupted forward movement (Hills et
al., 2004; Tsalik and Hobert,
2003; Wakabayashi et al.,
2004; Gray et al.,
2005). Rhythmic pumping of the pharyngeal muscles enables C.
elegans to consume food, and starvation increases the pumping rate,
presumably increasing the likelihood of ingesting food by chance
(Avery and Horvitz, 1990). Such
behavioral alterations are triggered directly by starvation and do not require
integration of different sensory inputs. Food also modulates behavior in ways
that imply associative links between different sensory inputs. For example,
starving or feeding animals in the presence of salt or certain volatile
chemicals modulates chemotaxis with respect to those chemicals
(Saeki et al., 2001;
Nuttley et al., 2002;
Torayama et al., 2007).
Thermotaxis is one of the best-studied forms of long-term
experience-dependent behavior in C. elegans
(Bargmann and Mori, 1997).
Hedgecock and Russell (Hedgecock and
Russell, 1975) discovered that, when placed on a spatial thermal
gradient, C. elegans is able to track isotherms and accumulate near
the temperature of its previous cultivation, as well as avoid temperatures at
which they were starved. An attractive interpretation of thermotactic behavior
is that it helps C. elegans to find food, either by driving worms
towards their previous cultivation temperature or away from starvation
temperatures. Along this vein, mechanisms for long-term plasticity in C.
elegans thermotaxis have been postulated to involve direct association
between temperature and food-dependent cues.
C. elegans exhibits different modes of thermotactic behavior in
different temperature ranges. When C. elegans is placed on a spatial
thermal gradient within 2–3°C of its previous cultivation
temperature, it tends to track isotherms, exhibiting a stored memory that we
call the thermotactic set-point (TS). Luo et al. analyzed
the strength of isothermal tracking behavior and found that the frequency or
duration of isothermal tracks exhibited by worms navigating near their
TS was not significantly affected by starvation at their
TS for as long as 4 h
(Luo et al., 2006). They also
found that worms exhibit isothermal tracking behavior on spatial thermal
gradients both in the presence and absence of bacterial food
(Luo et al., 2006). Thus,
isothermal tracking behavior may not be a mechanism by which C.
elegans locates food, but simply a mechanism for staying near an
acclimated temperature, irrespective of bacterial food.
The TS can be reset by cultivation of animals at a new
temperature (Hedgecock and Russell,
1975). Recently, we studied the determinants of
TS resetting by analyzing isothermal tracking behavior
(Biron et al., 2006). We grew
worms overnight at 15°C or 25°C, shifted the worms for defined periods
of time to new temperatures, and quantified the temperature range of the
isothermal tracking behavior on steep linear thermal gradients. We found that
worms gradually reset their TS from 15 to 25°C or from
25 to 15°C over about 4 h with exponential time courses, and these time
constants for TS resetting were unaffected by the presence
or absence of bacterial food at the new temperature. These observations
suggested that TS resetting occurs via
integration of temperature history over time and does not require an
association between temperature and food cues.
When C. elegans is placed more than 2°C above its previous
cultivation temperature (T>TS), it crawls
towards lower temperatures in what is called cryophilic movement
(Hedgecock and Russell, 1975).
The behavioral strategy that underlies cryophilic movement is the biased
random walk (Ryu and Samuel,
2002; Clark et al.,
2007). C. elegans motility in isotropic environments is a
random walk that is characterized by successive periods of forward movement
(runs) interrupted by spontaneous reorientation maneuvers (turns and
reversals). During cryophilic movement, C. elegans biases its random
walk towards lower temperatures by prolonging or shortening each run in
response to decreasing and increasing temperatures, respectively.
C. elegans has also been reported to exhibit thermophilic
movement, in which worms crawl towards their cultivation temperature from
lower temperatures or in which thermophilic mutants migrate to the warmest
point on a spatial thermal gradient
(Hedgecock and Russell, 1975;
Mori and Ohshima, 1995).
However, Ryu and Samuel (Ryu and Samuel,
2002) found that C. elegans exhibits an unbiased random
walk when it navigates at T<TS. Yamada and
Ohshima (Yamada and Ohshima,
2003) showed that, whereas C. elegans exhibits active
cryophilic movement towards its cultivation temperature from higher
temperatures, it is atactic at temperatures below its cultivation temperature.
One possibility is that C. elegans exhibits active thermophilic
behavior within a narrower range of experimental parameters than it does for
isothermal tracking behavior or cryophilic behavior. Such an argument may
reconcile reports of thermophilic behavior (e.g.
Hedgecock and Russell, 1975;
Mori and Ohshima, 1995) with
other reports that worms do not actively move up thermal gradients at
T<TS (e.g.
Ryu and Samuel, 2002;
Yamada and Ohshima, 2003).
The complexity of C. elegans thermotactic behavior and the
discrepancies between different studies underscore the importance of
quantifying thermotactic behavior during performance of the navigational task
and under well-defined and reproducible experimental conditions. Standard
behavioral assays define thermotactic phenotypes by allowing worms to navigate
thermal gradients and then measuring the temperature at which they accumulate
(Ito et al., 2006). However,
it is difficult to dissect thermotactic behavior using snapshots of worm
accumulation after thermotactic behavior has already taken place. It is more
informative to track and quantify the movements of individual worms as they
actively respond to well-defined thermal gradients
(Clark et al., 2007;
Luo et al., 2006).
In the present study, we continue our analysis of associativity in
long-term thermotactic plasticity since recent results suggest that
associative learning may not be required. In particular, Yamada and Ohshima
(Yamada and Ohshima, 2003)
found that worms do not specifically avoid temperatures at which they were
starved, and Biron et al. (Biron et al.,
2006) showed that TS resetting is not affected
by the presence or absence of bacterial food. Here, we quantify the
thermotactic movements of C. elegans on spatial thermal gradients
after sustained exposure to specific temperatures with and without bacterial
food. After confirming that unstarved worms exhibit cryophilic behavior at
T>TS and isothermal tracking behavior near the
TS under our experimental conditions, we went on to
demonstrate that TS resetting towards ambient temperature
is unaffected by food and, more specifically, that C. elegans does
not actively avoid temperatures at which it has been starved. While starvation
did abolish cryophilic behavior, it did not induce behavior that was
correlated to the starvation temperature. We found no evidence that long-term
thermotactic behavioral plasticity requires associative learning between
temperature and food-dependent cues.
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Materials and methods |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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). The wild-type strain (var. Bristol N2) and
hen-1(tm501), ttx-3(ks5) and tax-6(p675) mutant strains were
obtained from the C. elegans Genetics Center
(http://www.cbs.umn.edu/CGC/).
Worms were grown on bacterial lawns of the Escherichia coli strain
OP50. In cases that worms were starved for defined periods of time, they were
removed from overnight cultivation with bacterial food, rinsed in NGM buffer
(Sulstan and Hodgkin, 1988) and placed on clean agar plates without bacterial
food.
Quantitative analysis of thermotactic behavior at temperatures above or below the cultivation or starvation temperature
Young adult worms that were cultivated overnight and/or starved at 15°C
or 25°C were transferred to the surface of a 9 cm-diameter plate with a
linear spatial thermal gradient spanning 18–22°C without bacterial
food. The plate was allowed to thermally equilibrate for 5 min and then the
positions of individual worms were recorded every 2 s for 60 min. A ring of
glycerol was distributed around the rim of the Petri plate to prevent worms
from crawling up the agar meniscus and the plastic walls of the Petri plate,
allowing us to monitor a population of worms for long periods of time without
losing sight of individual worms. Individual worm trajectories were analyzed
using MATLAB (The Mathworks, Natick, MA, USA) using custom-written software
for population-wide behavioral quantification as described in Clark et al.
(Clark et al., 2007). The
position of each worm over time allowed us to calculate the distribution of
positions on the gradient and the mean migration over time. In addition, the
trajectories of individual worms were broken down into alternating periods of
runs and reorientations. Run duration was calculated by flagging the
reorientation at the start and end of each run as any change in the direction
of worm movement by >45° in 4 s, a procedure that is insensitive to
small-angle turns. Run orientation was calculated with respect to gradient
direction. The statistics of run duration as a function of run orientation
were calculated using MATLAB.
Quantitative analysis of isothermal tracking behavior
Young adult worms were cultivated overnight at 15°C or 25°C and
then transferred as young adults to 25°C or 15°C, respectively, for
fixed intervals of time. Individual worms were then transferred onto a 9
cm-diameter plate with a linear spatial thermal gradient of 0.5 deg.
cm–1 without bacterial food. The movements of individual
animals were recorded for 25 min. Isothermal tracks were defined as straight
vertical trajectories significantly longer (>2 cm) than the vertical
trajectories exhibited by worms at temperatures far from the
TS. The temperature corresponding to each isothermal track
was scored manually. The TS for each set of conditions was
measured as an average of tracking temperatures for each population of
animals.
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Results |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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;
Luo et al., 2006). Over the
course of observation, worms actively migrated towards the cold side of the
plate, and the mean temperature of the population decreased over time
(Fig. 1A; Movie 1 in
supplementary material). By contrast, when worms cultivated at 25°C were
placed on the same spatial thermal gradients, again to avoid evoking the
isothermal tracking behavior, they moved randomly and distributed themselves
uniformly between 18 and 22°C (Fig.
1B; Movie 2 in supplementary material). Thus, under these
experimental conditions, well-fed C. elegans exhibits an active
mechanism for cryophilic movement at T>TS and
is atactic at T<TS.
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). Thus, by analyzing the trajectories of individual worms
navigating spatial thermal gradients and quantifying the amount of bias in the
random walk, we are able to obtain a microscopic measure of navigational
strategy.
In order to show that changes in thermotactic behavior for the data shown
in Figs 1 and
2 can be attributed to changes
in navigational strategy, we quantified run duration as a function of run
orientation for the detailed trajectories of individual worms in the manner
described by Clark et al. (Clark et al.,
2007). For well-fed wild-type animals at
T>TS, mean run duration is a smoothly varying
function of the angle between the run and gradient directions: runs pointed
down (or up) the gradient are extended (or shortened)
(Fig. 3A,B). For well-fed
animals at T<TS, run duration is not modulated
by the gradient direction (Fig.
3A,B). Using the average duration of all runs pointed down the
gradient (
dn) (within 36° of down) and the average
duration of all runs pointed up the gradient (up) (within
36° of up), we may compute an index for cryophilic bias:
 | (1) |
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A simple way to quantify macroscopic cryophilic migration in the experiments shown in Figs 1 and 2 is to quantify the net change in the mean temperature of the population of worms after 15 min of navigation. Indeed, as prolonged starvation reduced the macroscopic measure of cryophilic migration, the microscopic measure of cryophilic bias was correspondingly reduced (Fig. 3C). Thus, the effect of prolonged starvation on cryophilic movement is directly linked to changes in the biased random walk strategy.
Long-term plasticity does not require associative learning between temperature and food
Biron et al. showed that worms cultivated overnight at 15°C (or
25°C) and then shifted as adults to 25°C (or 15°C) will shift
their TS within roughly 4 h as measured by the temperature
range of isothermal tracking behavior
(Biron et al., 2006). Since we
find that prolonged starvation suppresses cryophilic movement, we can make
specific predictions regarding the movement of worms on spatial thermal
gradients after growing worms at one temperature and then shifting them to a
new temperature in the presence or absence of food.
We grew worms overnight at 15°C or 25°C, shifted them as adults
with or without food to 25°C or 15°C for 4 h and then analyzed their
movements on spatial thermal gradients spanning 18–22°C
(Fig. 4A,B). We chose the 4 h
interval for starvation as it allows time for readjustment of
TS (Biron et al.,
2006) without completely eliminating cryophilic movement
(Fig. 2B). As expected,
unstarved worms that had been grown overnight at 15°C exhibited robust
cryophilic movement on the spatial thermal gradients
(Fig. 4B). When worms were
grown overnight at 15°C and starved at 15°C for an additional 4 h,
they exhibited weakened cryophilic movement
(Fig. 4B). However, when worms
were grown overnight at 15°C and starved at 25°C for 4 h, they
exhibited atactic movement, consistent with the TS having
shifted to higher temperatures. In this case, worms distributed themselves
uniformly across the thermal gradient, and we did not observe avoidance of the
25°C starvation temperature (Fig.
4A). Similar results were obtained with worms grown overnight at
15°C and shifted to 25°C for 4 h in the presence of food (data not
shown). Unstarved worms that had been grown overnight at 25°C exhibited
random dispersal on the 18–22°C spatial thermal gradients since
their T<TS. When worms were grown overnight at
25°C and starved at 25°C for an additional 4 h, they continued to
exhibit random dispersal. However, when worms were grown overnight at 25°C
and starved at 15°C, cryophilic movement is restored, consistent with the
TS having shifted to lower temperatures
(Fig. 4B).
|
). Upon
starvation, similar to wild-type worms, the cryophilic movement of
ttx-3 mutants is also decreased
(Fig. 4C). If worms actively avoid the specific temperatures at which they had been starved, then, if placed on a spatial thermal gradient that spans the starvation temperature, they might seek to evacuate themselves from the starvation temperature. To study this possibility, we placed worms that had been starved at 20°C on spatial thermal gradients that span 20°C. However, worms simply crawled randomly to all temperatures on such spatial thermal gradients, spreading themselves uniformly over time on 18–22°C gradients and on 15–25°C gradients (Fig. 5A,B).
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Thermotactic behavior in putative associative learning mutants
We next examined worms carrying mutations in genes previously suggested to
alter associative learning between temperature and food cues. Mutations in the
hen-1 gene, which encodes a secretory protein with an LDL receptor
motif, have been suggested to affect associative learning in thermotaxis
between temperature and the absence of food. Worms carrying the
hen-1(tm501) mutation have been claimed to be defective in avoiding
temperatures at which they have been starved
(Ishihara et al., 2002). One
interpretation is that hen-1 affects integrative behavior, as it is
expressed in interneurons that are downstream of the AFD thermosensory neuron,
as well as other chemosensory neurons potentially required for food sensation.
We grew hen-1(tm501) worms overnight at 15°C or 25°C, shifted
them as adults without food to 25°C or 15°C for 4 h and then analyzed
their movements on spatial thermal gradients at intermediate temperatures. In
all of these cases, we found that the behavior of hen-1(tm501) worms
was indistinguishable from that of wild-type worms
(Fig. 6A). Thus, we found no
evidence that the hen-1 gene affects behavior related to associative
learning under our experimental conditions.
|
Mutation in the tax-6 gene, which encodes calcineurin, has been
reported to cause a thermophilic phenotype, causing worms to accumulate at the
warmest point on a spatial thermal gradient
(Kuhara et al., 2002). By
rescuing the expression of tax-6 in subsets of neurons, Kuhara and
Mori found that expression of tax-6 in specific interneurons affects
associative learning between temperature and bacterial food
(Kuhara and Mori, 2006).
However, in our experimental conditions, we found that tax-6(p675)
mutant worms are simply atactic at all temperatures
(Fig. 6B), such that
tax-6(p675) mutant worms neither move up nor down spatial thermal
gradients, irrespective of feeding state or temperature experience. Since
tax-6(p675) mutant worms did not exhibit any thermotactic movement in
our experimental conditions, we cannot conclude whether tax-6 affects
integrative behavior.
For each of the experiments shown in Figs
4 and
6, we also verified that the
observed macroscopic changes in cryophilic migration were correlated with
changes in navigational strategy. In every case that worms exhibited rapid
cryophilic migration, they exhibited strong cryophilic bias. When worms
exhibited slow cryophilic migration, they exhibited weak cryophilic bias
(Fig. 7A). Collecting the data
from all of our experiments, the macroscopic metric of cryophilic migration
and the microscopic metric of cryophilic bias are highly correlated
(r2=0.74) (Fig.
7B). Linear proportionality between these two metrics has been
predicted in the theory of biased random walks
(De Gennes, 2004;
Clark and Grant, 2005).
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First, we verified that hen-1(tm501) mutant worms cultivated at specific temperatures are capable of tracking isotherms near those temperatures on a spatial thermal gradient (Fig. 8B). We cultivated hen-1(tm501) mutant animals at 15°C (and 25°C), then shifted the animals to 25°C (and 15°C), with or without food at the new temperature. At defined times following the temperature shift, we quantified the TS of these animals by monitoring their isothermal movements on steep spatial thermal gradients spanning the TS. We found that the hen-1(tm501) mutation does not affect the rate of TS resetting. Like wild-type animals (Fig. 8A), hen-1(tm501) mutant worms reset their TS to the new temperature of the environment after about 4 h. Also like wild-type animals, TS resetting in hen-1(tm501) mutant worms is unaffected by the presence or absence of food (Fig. 8C–F).
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Discussion |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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; Ryu and
Samuel, 2002). In addition, although both temperature and
food-dependent cues induce long-term changes in C. elegans
thermotactic behavior, whether long-term plasticity requires direct
associations between these cues has not been conclusively verified.
Hedgecock and Russell showed that C. elegans tracks isotherms near
its previous cultivation temperature
(Hedgecock and Russell, 1975).
Recently, we showed that adult C. elegans reset their thermotactic
set-point (TS) irrespective of the presence or absence of
food at new temperatures (Biron et al.,
2006). Thus, resetting the TS does not require
associative mechanisms. Hedgecock and Russell found evidence that C.
elegans disperses from temperatures at which they had been starved
(Hedgecock and Russell, 1975).
However, Yamada and Ohshima found evidence that C. elegans does not
actively avoid temperatures correlated with starvation
(Yamada and Ohshima, 2003).
Several genetic studies have been performed to identify molecules that affect
associative learning between temperature and food-dependent cues, but without
detailed analyses of the behavioral strategies underlying the presumed
associative learning behavior in wild-type worms. The hen-1 gene has
been interpreted as affecting the worm's ability to associate temperature and
starvation (Ishihara et al.,
2002). Genetic screens have been conducted for aho
(abnormal hunger orientation) mutants, which are also presumed to be defective
in associating temperature and starvation
(Mohri et al., 2005).
Insulin-like pathways have also been investigated for roles in
starvation-induced learning of specific temperatures
(Kodama et al., 2006).
We sought additional tests of association between temperature and food-dependent cues. In this study, we used precise and well-defined experimental conditions and analyzed both the macroscopic and microscopic metrics of worm navigation behavior on thermal gradients. Our results indicate that (1) TS resetting is induced by exposing worms to new temperatures, irrespective of the presence or absence of food at the new temperature; (2) worms do not appear to actively avoid temperatures at which they had been starved; (3) cryophilic movement is suppressed after prolonged starvation. In short, under our experimental conditions, association between temperature and food-dependent cues is not required. Sustained exposure to specific temperatures resets the TS to those temperatures. Starvation suppresses cryophilic movement, causing worms to randomly disperse on spatial thermal gradients.
Non-associative models for long-term plasticity in thermotactic behavior
would be simpler than associative models, as neural circuits would not be
required to integrate different sensory inputs. The regulation of thermotactic
behavior in C. elegans involves the AFD sensory neurons, the AIY
interneurons and the AIZ interneurons, which form a synaptically
interconnected minicircuit in the nervous system
(Mori and Ohshima, 1995).
Recent physiological measurements have shown that patterns in the activity of
the AFD sensory neurons are correlated with the stored TS
(Kimura et al., 2004;
Clark et al., 2006). In
particular, temperature changes evoke Ca2+-dynamics in the AFD
neuron and drive AFD synaptic output to the AIY interneuron only at
temperatures above a certain threshold temperature, which is near the
TS. Moreover, exposing the animal to new temperatures
resets the threshold temperature of AFD neuronal activity in physiological
measurements with time courses that correspond to TS
resetting in behavioral measurements (Biron
et al., 2006). Mutations in the dgk-3 gene, which encodes
a diacylglycerol kinase expressed in the AFD thermosensory neuron, have
parallel effects on the rate of TS resetting measured at
the levels of behavior and AFD physiological activity
(Biron et al., 2006). These
observations suggest that the physiological operating range of the AFD neuron
defines the temperature range of thermotactic behavior. Sustained exposure to
new temperatures shifts the sensitivity of the AFD neuron to different
temperatures, thereby shifting the set-point of thermotactic behavior to
different temperatures.
Our observations suggest that prolonged starvation simply abolishes
migration up or down spatial thermal gradients, allowing C. elegans
to rapidly disperse from any temperature. The mechanisms by which starvation
suppresses cryophilic movement are not known. One possibility is that specific
pathways in the C. elegans nervous system are modified, as in the way
that serotonergic circuits are modified to mediate the enhanced slowing
response of C. elegans when it encounters food after prolonged
starvation (Sawin et al.,
2000). Another possibility is that starvation induces hormonal
changes with broad effects on the nervous system. For example, Tomioka et al.
found that an insulin-like signaling pathway may mediate the worm's salt
avoidance behavior after starvation in the presence of ordinarily
chemoattractive salt (Tomioka et al.,
2006).
Our experimental conditions are capable of evoking robust cryophilic behavior, isothermal tracking behavior and long-term plasticity from C. elegans. However, based on our quantitative measurements of cryophilic behavior and isothermal tracking behavior under our experimental conditions, we are unable to conclude that C. elegans thermotaxis involves associative learning between temperature and food-dependent cues.
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Acknowledgments |
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Footnotes |
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* These authors contributed equally to this work 
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References |
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