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

Linjiao Luo, Nathan Cook, Vivek Venkatachalam, Luis A. Martinez-Velazquez, Xiaodong Zhang, Ana C. Calvo, Josh Hawk, Bronwyn L. MacInnis, Michelle Frank, Jia Hong Ray Ng, Mason Klein, Marc Gershow, Marc Hammarlund, Miriam B. Goodman, Daniel A. Colón-Ramos, Yun Zhang, Aravinthan D T Samuel

    Research output: Contribution to journalArticle

    Abstract

    The nematode Caenorhabditis elegans navigates toward a preferred temperature setpoint (Ts) determined by long-term temperature exposure. During thermotaxis, the worm migrates down temperature gradients at temperatures above Ts (negative thermotaxis) and performs isothermal tracking near Ts. Under some conditions, the worm migrates up temperature gradients below Ts (positive thermotaxis). Here, we analyze positive and negative thermotaxis toward Ts 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 Ts. 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.

    Original languageEnglish (US)
    Pages (from-to)2776-2781
    Number of pages6
    JournalProceedings of the National Academy of Sciences of the United States of America
    Volume111
    Issue number7
    DOIs
    StatePublished - Feb 18 2014

    Fingerprint

    Caenorhabditis elegans
    Neurons
    Temperature
    Taxis Response
    Behavioral Genetics
    Interneurons
    Calcium

    ASJC Scopus subject areas

    • General

    Cite this

    Bidirectional thermotaxis in Caenorhabditis elegans is mediated by distinct sensorimotor strategies driven by the AFD thermosensory neurons. / Luo, Linjiao; Cook, Nathan; Venkatachalam, Vivek; Martinez-Velazquez, Luis A.; Zhang, Xiaodong; Calvo, Ana C.; Hawk, Josh; MacInnis, Bronwyn L.; Frank, Michelle; Ng, Jia Hong Ray; Klein, Mason; Gershow, Marc; Hammarlund, Marc; Goodman, Miriam B.; Colón-Ramos, Daniel A.; Zhang, Yun; Samuel, Aravinthan D T.

    In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 111, No. 7, 18.02.2014, p. 2776-2781.

    Research output: Contribution to journalArticle

    Luo, L, Cook, N, Venkatachalam, V, Martinez-Velazquez, LA, Zhang, X, Calvo, AC, Hawk, J, MacInnis, BL, Frank, M, Ng, JHR, Klein, M, Gershow, M, Hammarlund, M, Goodman, MB, Colón-Ramos, DA, Zhang, Y & Samuel, ADT 2014, 'Bidirectional thermotaxis in Caenorhabditis elegans is mediated by distinct sensorimotor strategies driven by the AFD thermosensory neurons', Proceedings of the National Academy of Sciences of the United States of America, vol. 111, no. 7, pp. 2776-2781. https://doi.org/10.1073/pnas.1315205111
    Luo, Linjiao ; Cook, Nathan ; Venkatachalam, Vivek ; Martinez-Velazquez, Luis A. ; Zhang, Xiaodong ; Calvo, Ana C. ; Hawk, Josh ; MacInnis, Bronwyn L. ; Frank, Michelle ; Ng, Jia Hong Ray ; Klein, Mason ; Gershow, Marc ; Hammarlund, Marc ; Goodman, Miriam B. ; Colón-Ramos, Daniel A. ; Zhang, Yun ; Samuel, Aravinthan D T. / Bidirectional thermotaxis in Caenorhabditis elegans is mediated by distinct sensorimotor strategies driven by the AFD thermosensory neurons. In: Proceedings of the National Academy of Sciences of the United States of America. 2014 ; Vol. 111, No. 7. pp. 2776-2781.
    @article{4617bcd0e8ba48318d066b512be06068,
    title = "Bidirectional thermotaxis in Caenorhabditis elegans is mediated by distinct sensorimotor strategies driven by the AFD thermosensory neurons",
    abstract = "The nematode Caenorhabditis elegans navigates toward a preferred temperature setpoint (Ts) determined by long-term temperature exposure. During thermotaxis, the worm migrates down temperature gradients at temperatures above Ts (negative thermotaxis) and performs isothermal tracking near Ts. Under some conditions, the worm migrates up temperature gradients below Ts (positive thermotaxis). Here, we analyze positive and negative thermotaxis toward Ts 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 Ts. 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.",
    author = "Linjiao Luo and Nathan Cook and Vivek Venkatachalam and Martinez-Velazquez, {Luis A.} and Xiaodong Zhang and Calvo, {Ana C.} and Josh Hawk and MacInnis, {Bronwyn L.} and Michelle Frank and Ng, {Jia Hong Ray} and Mason Klein and Marc Gershow and Marc Hammarlund and Goodman, {Miriam B.} and Col{\'o}n-Ramos, {Daniel A.} and Yun Zhang and Samuel, {Aravinthan D T}",
    year = "2014",
    month = "2",
    day = "18",
    doi = "10.1073/pnas.1315205111",
    language = "English (US)",
    volume = "111",
    pages = "2776--2781",
    journal = "Proceedings of the National Academy of Sciences of the United States of America",
    issn = "0027-8424",
    number = "7",

    }

    TY - JOUR

    T1 - Bidirectional thermotaxis in Caenorhabditis elegans is mediated by distinct sensorimotor strategies driven by the AFD thermosensory neurons

    AU - Luo, Linjiao

    AU - Cook, Nathan

    AU - Venkatachalam, Vivek

    AU - Martinez-Velazquez, Luis A.

    AU - Zhang, Xiaodong

    AU - Calvo, Ana C.

    AU - Hawk, Josh

    AU - MacInnis, Bronwyn L.

    AU - Frank, Michelle

    AU - Ng, Jia Hong Ray

    AU - Klein, Mason

    AU - Gershow, Marc

    AU - Hammarlund, Marc

    AU - Goodman, Miriam B.

    AU - Colón-Ramos, Daniel A.

    AU - Zhang, Yun

    AU - Samuel, Aravinthan D T

    PY - 2014/2/18

    Y1 - 2014/2/18

    N2 - The nematode Caenorhabditis elegans navigates toward a preferred temperature setpoint (Ts) determined by long-term temperature exposure. During thermotaxis, the worm migrates down temperature gradients at temperatures above Ts (negative thermotaxis) and performs isothermal tracking near Ts. Under some conditions, the worm migrates up temperature gradients below Ts (positive thermotaxis). Here, we analyze positive and negative thermotaxis toward Ts 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 Ts. 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.

    AB - The nematode Caenorhabditis elegans navigates toward a preferred temperature setpoint (Ts) determined by long-term temperature exposure. During thermotaxis, the worm migrates down temperature gradients at temperatures above Ts (negative thermotaxis) and performs isothermal tracking near Ts. Under some conditions, the worm migrates up temperature gradients below Ts (positive thermotaxis). Here, we analyze positive and negative thermotaxis toward Ts 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 Ts. 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.

    UR - http://www.scopus.com/inward/record.url?scp=84894363844&partnerID=8YFLogxK

    UR - http://www.scopus.com/inward/citedby.url?scp=84894363844&partnerID=8YFLogxK

    U2 - 10.1073/pnas.1315205111

    DO - 10.1073/pnas.1315205111

    M3 - Article

    VL - 111

    SP - 2776

    EP - 2781

    JO - Proceedings of the National Academy of Sciences of the United States of America

    JF - Proceedings of the National Academy of Sciences of the United States of America

    SN - 0027-8424

    IS - 7

    ER -