 |
||||
|
||||
|
||||
|
||||
|
||||
Previous Article | Next Article
The Journal of Neuroscience, July 1, 2002, 22(13):5727-5733
Thermotaxis in Caenorhabditis elegans Analyzed by Measuring Responses to Defined Thermal Stimuli
William S. Ryu and Aravinthan D. T. Samuel Department of Molecular and Cellular Biology, Harvard University, Cambridge, Massachusetts 02138, and Rowland Institute for Science, Cambridge, Massachusetts 02142
ABSTRACT
TOP
ABSTRACT
INTRODUCTION
In a spatial thermal gradient, Caenorhabditis elegans migrates toward and then isothermally tracks near its cultivation temperature. A current model for thermotactic behavior involves a thermophilic drive (involving the neurons AFD and AIY) and cryophilic drive (involving the neuron AIZ) that balance at the cultivation temperature. Here, we analyze the movements of individual worms responding to defined thermal gradients. We found evidence for a mechanism for migration down thermal gradients that is active at temperatures above the cultivation temperature, and a mechanism for isothermal tracking that is active near the cultivation temperature. However, we found no evidence for a mechanism for migration up thermal gradients at temperatures below the cultivation temperature that might have supported the model of opposing drives. The mechanisms for migration down gradients and isothermal tracking control the worm's movements in different manners. Migration down gradients works by shortening (lengthening) the duration of forward movement in response to positive (negative) temperature changes. Isothermal tracking works by orienting persistent forward movement to offset temperature changes. We believe preference for the cultivation temperature is not at the balance between two drives. Instead, the worm activates the mechanism for isothermal tracking near the cultivation temperature and inactivates the mechanism for migration down gradients near or below the cultivation temperature. Inactivation of the mechanism for migration down gradients near or below the cultivation temperature requires the neurons AFD and AIY.
Key words: thermotaxis; nematode; sensorimotor integration; thermosensation; behavioral models; navigation
INTRODUCTION
In their classic study of thermotaxis in Caenorhabditis elegans, Hedgecock and Russell (1975)
demonstrated that worms navigating spatial thermal gradients aggregate near their cultivation temperature (Tc). Within 3°C of this temperature, worms track isotherms, deviating from a given isotherm by as little as ~0.05°C. Hedgecock and Russell (1975)
Mori and Ohshima (1995)
Although the labels thermophilic, cryophilic, and atactic describe aberrant aggregation patterns on spatial gradients, they do not explain how putative thermophilic and cryophilic drives direct the worm's movements toward the cultivation temperature. Also, it is unclear whether thermophilic and cryophilic drives are active during isothermal tracking or whether isothermal tracking represents a distinct mechanism.
The present study aimed to determine the mechanisms underlying thermotaxis, the manner in which they direct the worm's movements, and the roles of participating neurons. We studied the movements of worms as they performed thermotaxis by (1) tracking worms crawling on the surface of agar plates with defined spatial or temporal thermal gradients and (2) monitoring the swimming motions of a worm suspended in a droplet subjected to thermal stimuli. In addition to wild-type (N2) worms, we studied thermotaxis mutants that have been shown to have developmental defects in AFD or AIY neurons, which have been identified by Mori and Ohshima (1995)
We found strong evidence for a mechanism for migration down gradients toward the cultivation temperature that might correspond to the cryophilic drive of the prevailing model, but no compelling evidence for a mechanism for migration up gradients that might correspond to the thermophilic drive. The mechanism for migration down gradients modulates run duration but not run orientation, shortening runs in response to positive changes in temperature and lengthening runs in response to negative changes in temperature. The mechanism for isothermal tracking modulates run orientation to offset either positive or negative temperature changes. These data (the asymmetry between navigation above and below the cultivation temperatures and the different nature of the motor commands between migration down gradients and isothermal tracking) seem to undermine the prevailing simple model of competing cryophilic and thermophilic drives.
MATERIALS AND METHODS
Media and strains. C. elegans strains were grown and maintained as described by Sulston and Hodgkin (1988)
Thermal gradients on surfaces. Linear thermal gradients were established on agar surfaces by placing Petri dishes in the middle of rectangular aluminum plates, the ends of which were fixed at different temperatures. Glycerol was used to ensure good thermal contact between the Petri dish and the metal surface. In one apparatus, thermoelectric controllers (TECs) were fixed to the ends of an aluminum plate (5 × 12.7 × 0.32 cm). The TECs (3 cm square, 50 W) were thermostatically controlled to 0.1°C with a linear-bipolar Proportional Command Integral Control controller (HTC-3000; Wavelength Electronics, Bozeman, MT). With this apparatus, arbitrary gradients (as steep as 5°C/cm) could be programmed. An apparatus of the type used by Hedgecock and Russell (1975)
The choice of temperatures for cultivating and testing worms was not arbitrary. Worms cultivate well in the range 15-25°C (Sulston and Hodgkin, 1988
Temporal thermal ramps were produced by controlling the temperature of a brass plate (11 cm in diameter, 0.32 cm thick) in contact with a TEC. Plates (9 cm) containing nematode growth medium (NGM) (Sulston and Hodgkin, 1988
All experiments were done in a temperature-controlled room set to a temperature between the limiting temperatures of the gradient. For example, for a gradient between 17 and 19°C, the room temperature was set to 18 ± 0.1°C. The numbers of worms analyzed in each experiment are listed in the figure legends.
Thermal gradients in droplets. Temporal thermal ramps in droplets were produced by controlling the temperature of an anodized aluminum plate (43 × 48 × 5 mm) in contact with a TEC. NGM buffer (60 µl; same inorganic ion concentration as NGM plates) was placed in a 4 mm circular hole in the plate, forming a transparent, hanging droplet. Temperatures were stable to 0.1°C; ramping rates up to 20°C/min could be achieved.
Crawling assays. Populations were synchronized by selecting eggs to OP50-seeded NGM plates (Sulston and Hodgkin, 1988
A CCD camera (wv-BP550; Panasonic, Secaucus, NJ) equipped with a 9-27 mm zoom lens (f/2.0) was used to image the worms. Worms were illuminated obliquely by a ring of superbright red light-emitting diodes, producing a dark-type illumination. Magnification was set such that the Petri dish filled the field of view. Video images were captured at 1 frame per second (fps) by a Scion Image LG-3 capture board (Scion Corp., Frederick, MD) on either a Macintosh computer (PowerMac G3; Apple Computers, Cupertino, CA) or a personal computer (Pentium III; Dell Computer Company, Round Rock, TX).
For the spatial assays, worms at a specific cultivation temperature were prepared as described above. A glass plate was used to cover the Petri dish to reduce convection. After waiting 15 min to ensure that the worms and plate had reached thermal equilibrium, video images of the plate were captured for 500 sec at 1 fps.
For the temporal assays, we waited for 1 min after the onset of the ramp before capturing images. During the subsequent linear part of the ramp, images were captured for 120 sec at 1 fps.
Worm trajectories were scored by hand using the imaging program Scion Image (Scion Corp.) Worm paths within 1 cm of the plate edge were not scored to avoid artifacts arising from thermal edge effects. Numerical analysis was performed with conventional and customized algorithms using Matlab (MathWorks Inc., Natick, MA).
Swimming assays. Worms cultivated at specific temperatures were prepared as described above; single worms were placed in the droplet. Worms were imaged using a stereomicroscope and a CCD camera. Worms swam vigorously, but sinking to the bottom of the curved droplet, they stayed in the center of the field of view. Bends that terminated the swimming run were scored by eye. We did not sort large bends based on the degree or direction of bending. For swimming worms, we did not score reversals of the direction of wave propagation; reversals were rare, and they did not contribute significantly to the statistics of run termination.
RESULTS
Migration toward cultivation temperature
Worms swim through fluids or crawl on surfaces using snake-like movements. We define a run as a period of uninterrupted forward motion (either swimming or crawling) in which bending waves propagate continuously from nose to tail. Crawling and swimming worms terminate runs in analogous manners: crawling worms terminate runs by abrupt reorientations that might be either turns or pirouettes (Fig. 1); swimming worms terminate runs by abrupt bends larger than those of the forward swimming rhythm (Fig. 1) or by reversing the direction of wave propagation. See Croll (1975)
View larger version (54K):[in this window]
[in a new window]
Figure 1. Run termination in crawling and swimming worms. Crawling worms terminate runs by turns (a) or by pirouettes (b), which involve reversals and coiling. c, Swimming worms terminate runs by abrupt bends larger than those of the rhythmic bends of forward swimming.
To determine whether worms modulate the run duration in response to thermal stimuli, we measured run durations of worms exposed to rising and falling temperatures (ramps). In assessing the run duration of crawling worms, we scored both turns and pirouettes, because both terminate the previous run and choose a new orientation for the subsequent run. In assessing the run duration of swimming worms, we scored the frequency of large bends.
In assays of crawling worms, we ramped the temperature of entire plates, eliminating spatial gradients. We found that above Tc, the run durations in negative temporal gradients (i.e., falling temperatures) were lengthened, whereas the run durations in positive temporal gradients (i.e., rising temperatures) were shortened compared with the run durations in isotropic environments at temperatures within the range of the temporal ramps (Tables 1 and 2). Below Tc, run durations were the same regardless of whether the temperature rose or fell (Table 2). Run durations were exponentially distributed, suggesting Poisson statistics (Fig. 2). The rate of run termination in isotropic environments, attributable to background activity not evoked by temperature changes, rose monotonically with ambient temperature and by itself cannot drive aggregation at Tc (Table 1).
View this table: [in this window]
[in a new window]
Table 1. Run durations of N2 worms cultivated at different temperatures crawling on agar surfaces at fixed temperatures (i.e., without temporal or spatial variation)
View this table: [in this window]
[in a new window]
Table 2. Run durations of N2 worms cultivated at different temperatures crawling on agar surfaces subjected to temporal ramps
View larger version (22K):[in this window]
[in a new window]
Figure 2. A sample histogram of run durations of N2 worms crawling in an isotropic environment (21°C). The data shown correspond to ~150 runs of worms raised at 22°C; the mean of this distribution corresponds to an entry in Table 1. The distribution is fit by a single exponential line: run termination might be a first-order kinetic process obeying Poisson statistics. The histogram was binned with 10 sec width.
In assays of swimming, we ramped the temperature of droplets (60 µl) containing single worms. Confined to a droplet, a worm made visible swimming motions but did not leave the field of view. Run termination events were more frequent for swimming worms than for crawling worms. We measured the durations of all runs of populations of worms crawling on plates, and we scored the times of occurrence of run termination events of individual worms swimming in droplets (Fig. 3). We found that the thermotactic response for swimming worms was analogous to that of crawling worms. Above Tc, the number of run termination events per unit time was lower during negative ramps and higher during positive ramps compared with measurements using droplets of a fixed temperature within the range of the temporal ramps. Below Tc, the rate of run termination was the same regardless of whether the temperature rose or fell.
View larger version (25K):[in this window]
[in a new window]
Figure 3. Times of occurrence of run termination events of N2 worms cultivated at 20°C swimming in droplets. Experiments at temperatures below Tc are at the left, and experiments at temperatures above Tc are at the right. Experiments at fixed temperatures are at the top (19°C for T < Tc; 24°C for T > Tc). Experiments subjecting the drops to positive temporal ramps of +4°C/min are in the middle (17-19°C for T < Tc; 22-24°C for T > Tc). Experiments subjecting the drops to negative temporal ramps of 4°C/min are at the bottom (19-17°C for T < Tc; 24-22°C for T > Tc). Within a panel, individual experimental trials are aligned along the vertical axis. Run termination events during a trial are indicated by closed squares; their horizontal positions indicate their times of occurrence from the beginning of each trial. (In the case of the ramp experiments, trials begin at the onset of the ramp.) All trials lasted 30 sec. For T < Tc, the rate of run termination was 0.26 ± 0.04 and 0.33 ± 0.04 Hz for positive and negative ramps, respectively; for T > Tc, the rate of run termination was 0.56 ± 0.03 and 0.08 ± 0.02 Hz for positive and negative ramps, respectively. The rate of run termination at fixed temperatures was 0.33 ± 0.08 and 0.22 ± 0.03 Hz for 19°C and 24°C, respectively. Values are means ± SEM.
During runs, worms crawled at the same speed in both positive and negative temporal ramps (Table 3). Therefore, controlling run speed is not part of the thermotactic strategy. Run speed had a much weaker dependence on ambient temperature than the rate of run termination (compare Tables 1 and 3).
View this table: [in this window]
[in a new window]
Table 3. Run speeds of N2 worms cultivated at 22°C in isotropic environments of different temperatures and subjected to temporal ramps toward or away from 22°C In spatial gradients, worms might arrive more quickly at Tc by biasing reorientation or run curvature toward Tc rather than by picking run direction and curvature randomly. To address this issue, we studied the trajectories of worms migrating toward Tc on the surfaces of agar plates with spatial thermal gradients. On spatial gradients in which worms rapidly migrated down gradients toward Tc, abrupt reorientations did not direct worms toward the favorable direction (Fig. 4a), nor did worms steer by gradually turning toward Tc (Fig. 4b).
View larger version (22K):[in this window]
[in a new window]
Figure 4. a, Initial and final run orientations interrupted by single abrupt reorientations (n = 413). Here, N2 worms cultivated at 22°C navigated a linear spatial gradient between 24 and 26°C of steepness 0.4°C/cm. The direction down the gradient was 0 radians. Final run orientations were not more clustered at 0 radians than initial run orientations, as would be the case if the angle of abrupt reorientation was not random and angle selection was weighted toward the favorable direction of movement. Along both axes there is a greater frequency of events between /2 and +
In our hands, when navigating even the steepest spatial gradients (4°C/cm) at temperatures below Tc, worms did not actively migrate toward Tc. Neither the run duration nor the run orientation was modulated to bias the worms up (or down) the gradients. Worms navigating at temperatures below Tc are atactic. Worms were able to aggregate near Tc by tracking isotherms on random arrival near Tc, but if they have a strategy for active migration up gradients toward Tc, it is undetectably weak using our assays.
In summary, when migrating toward Tc, worms modulate run duration but do not modulate run speed or orientation. When worms navigate at temperatures above Tc, they modulate the frequency of abrupt reorientations to migrate down the gradient: worms terminate runs more rapidly when moving away from Tc than when moving toward Tc. However, worms do not choose the angle of abrupt reorientations to direct runs in the more favorable direction. In contrast, when worms navigate at temperatures below Tc, we found no compelling evidence of a mechanism for migration up gradients toward higher temperatures.
Isothermal tracking
Worms crawling on a spatial thermal gradient track isotherms near Tc. On linear spatial gradients, they move along lines; on radial spatial gradients, they move in circles (Hedgecock and Russell, 1975
We measured the trajectories of isothermal tracks on linear spatial gradients of varying steepness (Fig. 5). Worms zigzagged along isothermal tracks (i.e., when they crawled too far from the targeted isotherm, they turned back toward it). The frequency of the zigzag increased and the width of the zigzag decreased on steeper thermal gradients (Fig. 5b,c). Whatever the gradient steepness, worms responded by turning when they arrived at the temperature boundaries of the targeted isotherm. These boundaries were within ~0.05°C of that isotherm.
View larger version (16K):[in this window]
[in a new window]
Figure 5. a, A single isothermal track of an N2 worm cultivated at 22°C on a linear thermal gradient of steepness 0.4°C/cm. b, Isothermal tracks were narrower as the steepness of thermal gradients increased. One metric of the width of isothermal tracks is y2
1/2, the mean square deviation from the midline of the track. Here, excursion amplitude is defined as the mean
As found by Hedgecock and Russell (1975)
View larger version (15K):[in this window]
[in a new window]
Figure 6. a, N2 worms cultivated at 22°C tracked isotherms in a range within 2°C of that cultivation temperature. The histogram shows the positions of the isotherms of ~40 worms drawn from a single plate tracked on a linear thermal gradient of steepness 0.4°C/cm and binned at a width of 0.4°C. b, Individual worms often stopped tracking one isotherm and resumed tracking a different one. This trace is an unusually clear example: the worm initially tracked at 21°C, fell off the isotherm, and continued to track at 22°C.
We suggest that isothermal tracking represents a behavioral mechanism that is active within a band of temperatures near Tc, and that it is not derived from the worm's behaviors when navigating at temperatures above or below Tc. Worms, when navigating at temperatures near Tc, track isotherms by avoiding temporal changes in temperature, turning to offset any changes exceeding ~0.05°C. In this case, as we have observed, a worm deviating from an isothermal track in steeper gradients would react more quickly (higher zigzag frequency) and within a shorter distance (smaller zigzag width). We suggest that the decision whether to track isotherms depends on the worm's comparison of the ambient temperature with Tc; the decision is yes if the worm is within 2-3°C of Tc.
Analysis of mutants
To determine the roles of individual neurons in the identified thermal circuit, we analyzed worms lacking AFD or AIY because of the developmental mutations ttx-1 (Satterlee et al., 2001
Worms that lack AIY are cryophilic and do not track isotherms (Mori and Ohshima, 1995
View this table: [in this window]
[in a new window]
Table 4. Run durations of N2 and ttx-3 (ks5) worms navigating isotropic environments and subjected to temporal ramps Laser ablation of AFD produces cryophilic or atactic worms (Mori and Ohshima, 1995
View larger version (19K):[in this window]
[in a new window]
Figure 7. Trajectories of crawling ttx-1 worms. Circling is either CW or CCW and is independent of ambient temperature or spatial gradients.
DISCUSSION
Our results do not easily reconcile with current opinion that thermotaxis is a balance between separate thermophilic and cryophilic drives (Thomas, 1995
Both mechanisms for tracking isotherms and for migration down gradients toward lower temperature respond to positive and negative changes in temperature, but the two mechanisms are active in different temperature regimes and control the worm's movements in different manners. The mechanism for isothermal tracking is active at temperatures near Tc. This mechanism controls run orientation, responding to positive and negative changes in temperature by prompting turns to offset the changes. The mechanism for migration down gradients toward lower temperatures is active at temperatures above Tc. This mechanism controls run duration but not run orientation, responding to positive or negative changes in temperature by shortening or lengthening runs.
A calcium-binding protein, expressed in AFD, AIY, and other neurons, is essential for isothermal tracking (Gomez et al., 2001
In mutants with developmental defects in AFD or AIY, the mechanism for migration down gradients toward lower temperatures is active at all temperatures irrespective of Tc. We suggest that the mechanism for isothermal tracking (involving AFD and AIY) is needed to suppress the mechanism for migration down gradients at temperatures near or below Tc. We do not know which neurons comprise the mechanism for migration down gradients toward lower temperatures.
Pierce-Shimomura et al. (1999)
Others have reported both thermophilic and cryophilic phenotypes attributable to mutation or laser ablation (Hedgecock and Russell, 1975
Also, the worm's preference for Tc has been explained as the balance between thermophilia and cryophilia. This explanation is also no longer adequate. Isothermal tracking reflects a capacity to compare ambient temperature with Tc: worms have a long-term memory of Tc; they track any isotherm near Tc. While tracking isotherms, worms react to small temperature changes by modulating run orientation, turning to offset these changes. In our view, the worm's behavior near Tc is not derivative of its behaviors above and below Tc. The behavior near Tc is qualitatively different from its behaviors above and below Tc: above Tc, the worm modulates run duration and not run orientation to migrate down gradients; below Tc, there is no active thermotactic mechanism.
Long-term memory of Tc determines the regimes of activity of the mechanisms for tracking isotherms and migration down gradients. Both mechanisms appear to make short-term comparisons of temperature, enabling responses to positive and negative temperature changes. However, these mechanisms control the worms' movements in different manners, the mechanism for migration down gradients controls only run duration; the mechanism for tracking isotherms controls run orientation. Elucidating the relationships between these two mechanisms, determining their shared and distinct neural circuit elements, and determining which neuron(s) are the primary transducers of temperature (specifically which neurons compare ambient temperature with a long-term memory of Tc and which neurons make short-term comparisons of temperature) are future goals uncovered by the present work.
FOOTNOTES Received Nov. 27, 2001; revised April 3, 2002; accepted April 15, 2002.
This work was supported by the Rowland Institute for Science. The C. elegans Genetics Center, a facility supported by the National Institutes of Health, provided mutant strains. A.D.T.S. is an Amgen Fellow of the Life Sciences Research Foundation. We thank Venkatesh Murthy and Howard Berg, and members of their laboratories, for useful discussions, sharing resources, and critical reading of this manuscript. We thank an anonymous reviewer for critical comments.
Correspondence should be addressed to Dr. Aravinthan Samuel, Cold Spring Harbor Laboratories, 1 Bungtown Road, Cold Spring Harbor, NY 11724. E-mail: samuel{at}cshl.org.
REFERENCES
- Croll NA (1975) Components and patterns in the behavior of the nematode Caenorhabditis elegans. J Zool Lond 16:159-176.
- Gomez M, DeCastro E, Guarin E, Sasakura H, Kujara A, Mori I, Bartfai T, Bargmann CI, Nef P (2001) Ca2+ signaling via the neuronal calcium sensor ncs-1 regulates associative learning and memory in C. elegans. Neuron 30:241-248[Web of Science][Medline].
- Hedgecock EM, Russell RL (1975) Normal and mutant thermotaxis in the nematode Caenorhabditis elegans. Proc Natl Acad Sci USA 72:4061-4065
[Abstract/Free Full Text] .- Hobert O, Mori I, Yamashita Y, Honda H, Ohshima Y, Liu Y, Ruvkun G (1997) Regulation of interneuron function in the C. elegans thermoregulatory pathway by the ttx-3 LIM homeobox gene. Neuron 19:345-357[Web of Science][Medline].
- Mori I (1999) Genetics of chemotaxis and thermotaxis in the nematode Caenorhabditis elegans. Annu Rev Genet 33:399-422[Web of Science][Medline].
- Mori I, Ohshima Y (1995) Neural regulation of thermotaxis in Caenorhabditis elegans. Nature 376:344-348[Medline].
- Mori I, Ohshima Y (1997) Molecular neurogenetics of chemotaxis and thermotaxis in the nematode Caenorhabditis elegans. BioEssays 19:1055-1064[Web of Science][Medline].
- Pierce-Shimomura JT, Morse TM, Lockery SR (1999) The fundamental role of pirouettes in Caenorhabditis elegans chemotaxis. J Neurosci 19:9557-9569
[Abstract/Free Full Text] .- Satterlee JS, Sasakura H, Kuhara A, Berkeley M, Mori I, Sengupta P (2001) Specification of thermosensory neuron fate in C. elegans requires ttx-1, a homolog of orthodenticle/Otx. Neuron 31:943-956[Web of Science][Medline].
- Sulston J, Hodgkin J (1988) Methods. In: The nematode Caenorhabditis elegans (Wood WB, ed), pp 587-606. Cold Spring Harbor, NY: Cold Spring Harbor.
- Thomas J (1995) Thermosensation: some like it hot. Curr Biol 5:1222-1224[Medline].
- Wittenburg N, Baumeister R (1999) Thermal avoidance in Caenorhabditis elegans: an approach to the study of nociception. Proc Natl Acad Sci USA 96:10477-10482
[Abstract/Free Full Text] .
Copyright © 2002 Society for Neuroscience 0270-6474/02/22135727-07$05.00/0
This article has been cited by other articles:
Y. Iino and K. Yoshida
Parallel Use of Two Behavioral Mechanisms for Chemotaxis in Caenorhabditis elegans
J. Neurosci., April 29, 2009; 29(17): 5370 - 5380.
[Abstract] [Full Text] [PDF]
G. P. Harris, V. M. Hapiak, R. T. Wragg, S. B. Miller, L. J. Hughes, R. J. Hobson, R. Steven, B. Bamber, and R. W. Komuniecki
Three Distinct Amine Receptors Operating at Different Levels within the Locomotory Circuit Are Each Essential for the Serotonergic Modulation of Chemosensation in Caenorhabditis elegans
J. Neurosci., February 4, 2009; 29(5): 1446 - 1456.
[Abstract] [Full Text] [PDF]
E. Izquierdo, I. Harvey, and R. D. Beer
Associative Learning on a Continuum in Evolved Dynamical Neural Networks
Adaptive Behavior, December 1, 2008; 16(6): 361 - 384.
[Abstract] [PDF]
D. Ramot, B. L. MacInnis, H.-C. Lee, and M. B. Goodman
Thermotaxis is a Robust Mechanism for Thermoregulation in Caenorhabditis elegans Nematodes
J. Neurosci., November 19, 2008; 28(47): 12546 - 12557.
[Abstract] [Full Text] [PDF]
D. Biron, S. Wasserman, J. H. Thomas, A. D. T. Samuel, and P. Sengupta
An olfactory neuron responds stochastically to temperature and modulates Caenorhabditis elegans thermotactic behavior
PNAS, August 5, 2008; 105(31): 11002 - 11007.
[Abstract] [Full Text] [PDF]
S. R. Lockery, K. J. Lawton, J. C. Doll, S. Faumont, S. M. Coulthard, T. R. Thiele, N. Chronis, K. E. McCormick, M. B. Goodman, and B. L. Pruitt
Artificial Dirt: Microfluidic Substrates for Nematode Neurobiology and Behavior
J Neurophysiol, June 1, 2008; 99(6): 3136 - 3143.
[Abstract] [Full Text] [PDF]
L. Luo, C. V. Gabel, H.-I. Ha, Y. Zhang, and A. D. T. Samuel
Olfactory Behavior of Swimming C. elegans Analyzed by Measuring Motile Responses to Temporal Variations of Odorants
J Neurophysiol, May 1, 2008; 99(5): 2617 - 2625.
[Abstract] [Full Text] [PDF]
C. A. Chi, D. A. Clark, S. Lee, D. Biron, L. Luo, C. V. Gabel, J. Brown, P. Sengupta, and A. D. T. Samuel
Temperature and food mediate long-term thermotactic behavioral plasticity by association-independent mechanisms in C. elegans
J. Exp. Biol., November 15, 2007; 210(22): 4043 - 4052.
[Abstract] [Full Text] [PDF]
J. L. Anderson, L. Albergotti, S. Proulx, C. Peden, R. B. Huey, and P. C. Phillips
Thermal preference of Caenorhabditis elegans: a null model and empirical tests
J. Exp. Biol., September 1, 2007; 210(17): 3107 - 3116.
[Abstract] [Full Text] [PDF]
N. A. Dunn, J. S. Conery, and S. R. Lockery
Circuit Motifs for Spatial Orientation Behaviors Identified by Neural Network Optimization
J Neurophysiol, August 1, 2007; 98(2): 888 - 897.
[Abstract] [Full Text] [PDF]
C. V. Gabel, H. Gabel, D. Pavlichin, A. Kao, D. A. Clark, and A. D. T. Samuel
Neural Circuits Mediate Electrosensory Behavior in Caenorhabditis elegans
J. Neurosci., July 11, 2007; 27(28): 7586 - 7596.
[Abstract] [Full Text] [PDF]
D. A. Clark, C. V. Gabel, H. Gabel, and A. D. T. Samuel
Temporal Activity Patterns in Thermosensory Neurons of Freely Moving Caenorhabditis elegans Encode Spatial Thermal Gradients
J. Neurosci., June 6, 2007; 27(23): 6083 - 6090.
[Abstract] [Full Text] [PDF]
D. A. Clark, C. V. Gabel, T. M. Lee, and A. D. T. Samuel
Short-Term Adaptation and Temporal Processing in the Cryophilic Response of Caenorhabditis elegans
J Neurophysiol, March 1, 2007; 97(3): 1903 - 1910.
[Abstract] [Full Text] [PDF]
P. A. Garrity
Role of Adaptation in C. elegans thermotaxis. Focus on "Short-Term Adaptation and Temporal Processing in the Cryophilic Response of Caenorabditis elegans"
J Neurophysiol, March 1, 2007; 97(3): 1874 - 1876.
[Full Text] [PDF]
L. Luo, D. A. Clark, D. Biron, L. Mahadevan, and A. D. T. Samuel
Sensorimotor control during isothermal tracking in Caenorhabditis elegans
J. Exp. Biol., December 1, 2006; 209(23): 4652 - 4662.
[Abstract] [Full Text] [PDF]
D. A. Clark, D. Biron, P. Sengupta, and A. D. T. Samuel
The AFD sensory neurons encode multiple functions underlying thermotactic behavior in Caenorhabditis elegans.
J. Neurosci., July 12, 2006; 26(28): 7444 - 7451.
[Abstract] [Full Text] [PDF]
S. Faumont, T. Boulin, O. Hobert, and S. R. Lockery
Developmental Regulation of Whole Cell Capacitance and Membrane Current in Identified Interneurons in C. elegans
J Neurophysiol, June 1, 2006; 95(6): 3665 - 3673.
[Abstract] [Full Text] [PDF]
H. Inada, H. Ito, J. Satterlee, P. Sengupta, K. Matsumoto, and I. Mori
Identification of Guanylyl Cyclases That Function in Thermosensory Neurons of Caenorhabditis elegans
Genetics, April 1, 2006; 172(4): 2239 - 2252.
[Abstract] [Full Text] [PDF]
J. M. Gray, J. J. Hill, and C. I. Bargmann
Inaugural Article: A circuit for navigation in Caenorhabditis elegans
PNAS, March 1, 2005; 102(9): 3184 - 3191.
[Abstract] [Full Text] [PDF]
A. Mohri, E. Kodama, K. D. Kimura, M. Koike, T. Mizuno, and I. Mori
Genetic Control of Temperature Preference in the Nematode Caenorhabditis elegans
Genetics, March 1, 2005; 169(3): 1437 - 1450.
[Abstract] [Full Text] [PDF]
Y. Yamada and Y. Ohshima
Distribution and movement of Caenorhabditis elegans on a thermal gradient
J. Exp. Biol., August 1, 2003; 206(15): 2581 - 2593.
[Abstract] [Full Text] [PDF]
H. A. Zariwala, A. C. Miller, S. Faumont, and S. R. Lockery
Step Response Analysis of Thermotaxis in Caenorhabditis elegans
J. Neurosci., May 15, 2003; 23(10): 4369 - 4377.
[Abstract] [Full Text] [PDF]
A. D. T. Samuel, R. A. Silva, and V. N. Murthy
Synaptic Activity of the AFD Neuron in Caenorhabditis elegans Correlates with Thermotactic Memory
J. Neurosci., January 15, 2003; 23(2): 373 - 376.
[Abstract] [Full Text] [PDF]
This Article Abstract 
Full Text (PDF) Submit an eLetter Alert me when this article is cited Alert me when eLetters are posted Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in Web of Science Similar articles in PubMed Alert me to new issues of the journal Download to citation manager 
Citing Articles Citing Articles via HighWire Citing Articles via Web of Science (44) Citing Articles via Google Scholar Google Scholar Articles by Ryu, W. S. Articles by Samuel, A. D. T. Search for Related Content PubMed PubMed Citation Articles by Ryu, W. S. Articles by Samuel, A. D. T.
|
|
|
|
 |
|