Thermotaxis in<i>Caenorhabditis elegans</i>Analyzed by Measuring Responses to Defined Thermal Stimuli

Ryu, William S.; Samuel, Aravinthan D. T.

doi:10.1523/jneurosci.22-13-05727.2002

Cited by 174 publications

(241 citation statements)

References 10 publications

(28 reference statements)

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“…Reorientation maneuvers are either turns or reversal turns (also called pirouettes) (12,13,15) (Fig. 2 A and B and Movie S1).…”

Section: Resultsmentioning

confidence: 99%

“…E-mail: samuel@physics.harvard.edu, lluo@ fas.harvard.edu, mbgoodman@stanford.edu, daniel.colon-ramos@yale.edu, or yzhang@ oeb.harvard.edu. components of the worms' underlying behavioral strategies (12)(13)(14). Negative thermotaxis involves modulation of run length that is reminiscent of the biased random walk that was originally observed in bacterial chemotaxis (15,16).…”

Section: Significancementioning

confidence: 99%

“…If worms sense positive temperature gradients, they exhibit short runs. Thus, net migration is down temperature gradients (13). Isothermal tracking is deterministic, a steering behavior in which the worm continuously makes temperature comparisons and movement corrections with every undulation to maintain isothermal alignment (14).…”

Section: Significancementioning

confidence: 99%

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Bidirectional thermotaxis in Caenorhabditis elegans is mediated by distinct sensorimotor strategies driven by the AFD thermosensory neurons

Luo

Cook

Venkatachalam

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

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114

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The nematode Caenorhabditis elegans navigates toward a preferred temperature setpoint (T s ) determined by long-term temperature exposure. During thermotaxis, the worm migrates down temperature gradients at temperatures above T s (negative thermotaxis) and performs isothermal tracking near T s . Under some conditions, the worm migrates up temperature gradients below T s (positive thermotaxis). Here, we analyze positive and negative thermotaxis toward T s to study the role of specific neurons that have been proposed to be involved in thermotaxis using genetic ablation, behavioral tracking, and calcium imaging. We find differences in the strategies for positive and negative thermotaxis. Negative thermotaxis is achieved through biasing the frequency of reorientation maneuvers (turns and reversal turns) and biasing the direction of reorientation maneuvers toward colder temperatures. Positive thermotaxis, in contrast, biases only the direction of reorientation maneuvers toward warmer temperatures. We find that the AFD thermosensory neuron drives both positive and negative thermotaxis. The AIY interneuron, which is postsynaptic to AFD, may mediate the switch from negative to positive thermotaxis below T s . We propose that multiple thermotactic behaviors, each defined by a distinct set of sensorimotor transformations, emanate from the AFD thermosensory neurons. AFD learns and stores the memory of preferred temperatures, detects temperature gradients, and drives the appropriate thermotactic behavior in each temperature regime by the flexible use of downstream circuits.N avigational behaviors provide a framework for exploring the interplay among sensorimotor circuits, learning, and memory. During a navigational task, animals eventually reach their goals by implementing strategies composed of sensorimotor rules. Experience can modify navigational goals, so memory can also be integrated into sensorimotor pathways. Studying navigation in the nematode Caenorhabditis elegans offers the possibility of understanding the plasticity and programming of sensorimotor circuits from input to output in a small nervous system (1).Previous studies established C. elegans thermotaxis as a model for experience-dependent navigation (2-6). When worms are exposed to specific temperatures between 15°C and 25°C for at least 4 h, they adopt those temperatures as their thermotactic setpoint (T s ) (2, 3, 5, 7). When placed on a spatial temperature gradient, worms seek the T s . When arriving near T s , worms track isotherms. Genetic analysis of thermotaxis has yielded mutants that are athermotactic (crawling randomly on temperature gradients), cryophilic (crawling to the coldest point on a temperature gradient irrespective of T s ), or thermophilic (crawling to the warmest point on a temperature gradient). This observation led to the suggestion that thermotaxis might involve separate circuits for negative thermotaxis (movement down gradients) and positive thermotaxis (movement up gradients) that balance near T s (2, 4).Systematic laser ablation a...

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“…Reorientation maneuvers are either turns or reversal turns (also called pirouettes) (12,13,15) (Fig. 2 A and B and Movie S1).…”

Section: Resultsmentioning

confidence: 99%

Section: Significancementioning

confidence: 99%

See 1 more Smart Citation

Bidirectional thermotaxis in Caenorhabditis elegans is mediated by distinct sensorimotor strategies driven by the AFD thermosensory neurons

Luo

Cook

Venkatachalam

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

Self Cite

114

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“…We found that in the presence of a velocity gradient next to stationary surface, most undulatory swimmers align themselves against the direction of the flow (positive rheotaxis) with their heads facing upstream. In contrast to other tactic behaviors, such as chemotaxis (26), thermotaxis (27), and electrotaxis (28), which require active involvement of the nervous system, rheotaxis results from purely mechanical interactions.…”

Section: Resultsmentioning

confidence: 99%

Propensity of undulatory swimmers, such as worms, to go against the flow

Yuan¹,

Raizen

Bau³

2015

Proc. Natl. Acad. Sci. U.S.A.

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The ability to orient oneself in response to environmental cues is crucial to the survival and function of diverse organisms. One such orientation behavior is the alignment of aquatic organisms with (negative rheotaxis) or against (positive rheotaxis) fluid current. The questions of whether low-Reynolds-number, undulatory swimmers, such as worms, rheotax and whether rheotaxis is a deliberate or an involuntary response to mechanical forces have been the subject of conflicting reports. To address these questions, we use Caenorhabditis elegans as a model undulatory swimmer and examine, in experiment and theory, the orientation of C. elegans in the presence of flow. We find that when close to a stationary surface the animal aligns itself against the direction of the flow. We elucidate for the first time to our knowledge the mechanisms of rheotaxis in worms and show that rheotaxis can be explained solely by mechanical forces and does not require sensory input or deliberate action. The interaction between the flow field induced by the swimmer and a nearby surface causes the swimmer to tilt toward the surface and the velocity gradient associated with the flow rotates the animal to face upstream. Fluid mechanical computer simulations faithfully mimic the behavior observed in experiments, supporting the notion that rheotaxis behavior can be fully explained by hydrodynamics. Our study highlights the important role of hydrodynamics in the behavior of small undulating swimmers and may assist in developing control strategies to affect the animals’ life cycles.

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“…The net result of this strategy is to allow the animal to move towards and accumulate at the point source. Similar mechanisms are also employed by worms to navigate thermal gradients above their preferred temperature [79,80].…”

Section: Navigating Towards or Away From A Chemicalmentioning

confidence: 96%

Generation and modulation of chemosensory behaviors in C. elegans

Sengupta

2007

Pflugers Arch - Eur J Physiol

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C. elegans recognizes and discriminates among hundreds of chemical cues using a relatively compact chemosensory nervous system. Chemosensory behaviors are also modulated by prior experience and contextual cues. Because of the facile genetics and genomics possible in this organism, C. elegans provides an excellent system in which to explore the generation of chemosensory behaviors from the level of a single gene to the motor output. This review summarizes the current knowledge on the molecular and neuronal substrates of chemosensory behaviors and chemosensory behavioral plasticity in C. elegans.

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Thermotaxis inCaenorhabditis elegansAnalyzed by Measuring Responses to Defined Thermal Stimuli

Cited by 174 publications

References 10 publications

Bidirectional thermotaxis in Caenorhabditis elegans is mediated by distinct sensorimotor strategies driven by the AFD thermosensory neurons

Bidirectional thermotaxis in Caenorhabditis elegans is mediated by distinct sensorimotor strategies driven by the AFD thermosensory neurons

Propensity of undulatory swimmers, such as worms, to go against the flow

Generation and modulation of chemosensory behaviors in C. elegans

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